Wesleyan University The Honors College

Situating Place Cells in Ecologically Embodied Cognition

by

William H. Fraker Class of 2014

A thesis submitted to the faculty of Wesleyan University

in partial fulfillment of the requirements for the Degree of Bachelor of Arts

with Departmental Honors in the Science in Society Program Middletown, Connecticut April, 2014

 

 

Table o f Contents Acknowledgements Introduction 1 An Overview of the Organism-Environment Relationship 4 What are Internal Representations and What Is Their Supposed Function? 8 Part I—Ecologically Embodied Cognition Embodied Enaction 14

Coupling and Construction 24 Narcissistic Affordances and Nested Significance 32 Part II—A View from Within The Place of the Brain in Ecological Embodiment 40 Descriptive Aspects of Place Cell Phenomena 44 Representing or Embedding? Three Case Studies 57 Concluding Remarks 80 References 83

 

 

Acknowledgements This thesis would not have been possible without the generous support of many

individuals. First and foremost, I want to thank my advisor Joseph Rouse. Over the past three years he has transformed my perspective and encouraged me to think critically and creatively in the process of integrating diverse disciplines. The foundations of the foregoing content stem from materials he has taught and made available to me, conversations we have had, and pieces he has written. I thank him for his enthusiasm, his unparalleled wisdom, and his consistent feedback and encouragement.

Secondly, I want to thank Mary-Jane Rubenstein for teaching me to think big but

write small. Three semesters of her courses transformed my writing ability more drastically than all my years of prior education. I thank her for providing me with the tools to write clearly and concisely, without having to sacrifice the messy intricacies of thought and theory.

Thirdly, I want to thank the College of the Environment for housing my intellectual

endeavors throughout the past year. Furthermore, I want to thank all the members of the 2013-2014 CoE Think Tank—Gillian Goslinga, Paul Erickson, Frederique Apffel-Marglin, Nicole Stanton, Helen Poulos, Joshua Krugman, Manon Lefevre, and Lauren Burke—for providing a nurturing space for intellectual growth and stimulating discussion. I want to especially thank Gillian and Paul for serving as mentors within the SiSP department. Their commitment to my learning has made an immeasurable contribution to my development as a student.

Finally, I want to thank my family. I am grateful to my Mom and Dad for their

unwavering love and support, and for allowing me the freedom to take an untraditional academic path. Their faith in and commitment to my growth as an individual have enabled me to become the person I am today. I love you. I thank my brother, Colin, for keeping me grounded and always reminding me of both my strengths and my weaknesses. I look up to you more than you know.

 

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Introduct ion

As you arrive in Middletown on Highway 9 South, there is a massive billboard with

an image of a colorful brain housed within the faint outline of a transparent human head.

The advertisement is for Middlesex Hospital, and the text reads, ‘An MRI so clear it can

read your mind.’ Such an advertisement seems perfectly sensible, nothing more than a

creative hyperbole that seeks to draw attention to the cutting-edge medical imaging

technology boasted by the hospital. But when looked at critically, the advertisement

reveals specific philosophical implications.

Of course, the hospital is not actually claiming an ability to read minds. On the

contrary, their MRIs serve profoundly important diagnostic purposes that have little to

do with the minds of their patients beyond providing the peace of mind that comes with

sound evidence. And yet, the advertisement gets this exact point across, which prompts

various questions: what makes this hyperbole intelligible in the first place? What about

this advertisement makes intuitive sense?

I would like to argue that the intelligibility of this advertisement rests on a very

particular understanding of what and where the mind is. Whether approached as an

internal space of consciousness or as the brain itself (or as the relation between these

two), the mind is consistently regarded as an interior sphere ‘inside the head,’ separable

from the body and environment. And, as evinced by the billboard and its audience, it is

clear that this assumption moves beyond erudite academic debates. Instead, it

exemplifies a common intuition that is rarely called into question (Thompson 2010;

Dennett 1991). If this were not the case, such an advertisement would cease to make

sense. My goal is to challenge and revise this intuition by resituating the mind within the

 

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body and environment. The task is to show how situated embodiment—where the mind

is embedded in the world through active engagement—overcomes the necessity for the

internal representation of a world that is separate and exterior.

By arguing that the mind is not exclusively in the brain, I am neither negating the

naturalness of the mind, nor the importance of the brain. But to provide a naturalistic

conception of mind requires that we peer deeper into the evolutionary biology of the

organism-environment relationship. Upon doing so, one of the first discoveries is that

neurons evolved to coordinate action within and control over the environment that

shapes and constrains it, not to produce thought (Stewart 2010). As Michael Anderson

states,

“Whereas on the Cartesian view the body is understood as the source of afferent stimulus and the target of efferent output […] on the enactive view, the body and its activity play not a peripheral, but a central role in the process of mind, and, in fact, the activity of an organism in relation to its environment can be considered […] its constitution” (Anderson 2009, 3).

The belief that the mind has the brain as its physical substrate exists, to be sure,

within the realm of naturalism. But, even when the mind is seen as a property of the

brain exclusively, we still retain the interior/exterior, subjective/objective oppositions

that are fundamentally Cartesian, and in ways that make them almost invisible

(Haugeland 1998). To take a different route, a naturalistic conception of mind can begin

with the integral relationship between an organism and its environment in order to

observe how ‘higher’ cognitive functions emerge from and are dependent upon this active

entanglement. Instead of ‘I think therefore I am,’ a genuine naturalism should contend

that I am (an active body embedded in a world) therefore I think. Of course there is a

complex realm of internal thought and representation that is associated with neural

processes, and of course the brain’s internal processes are centrally involved in

 

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organismal action and perception, but the brain’s connection to and dependence upon

the body must be drastically re-framed. To take the interiority of the mind as a starting

point in a naturalistic philosophy and science of mind is to ignore the rich history of an

evolved phenomenon and mistake what comes last for what comes first.

Thus, a positive naturalistic account of mind shall begin with an exposition of the

relationship between an organism and its environment in order to demonstrate their

integralness and discover the central role of the active body in cognitive processes. In

doing so, it is necessary to shed the pre-given distinctions between the interior and exterior

and re-discover the foundational unity between an organism and the environment with

which it is actively engaged. In the process, originary priority is given to action within and

construction of an environment to which the organism is inseparably coupled, over the

passive perception of and adaptation to an environment that is exterior and separate.

In part one, I will articulate some essential components of ecologically embodied

cognition, focusing primarily on three central themes: the co-constitutiveness of action

and perception, the coupling or coordination between the organism’s individuated

processes and the environment in which these processes occur, and finally, the way in

which the details of the organism’s biology render an environment that is specific to that

organism. The broader goal of part one is to establish the body as the foundational unit

for understanding an organism’s integrated relationship with its environment and in

doing so, point towards the body as a central pillar in cognitive processes. It is helpful to

regard part one as a sampling and synthesis of the literature of ecological and embodied

cognition. It is my attempt to establish a coherent framework that can then serve as the

groundwork for the second section.

 

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Part two will proceed into the bounds of the skull in order to understand how the

brain’s internal processes are derived in relation to the brain’s involvement with and

embeddedness within the active organism. In doing so, I hope to develop a cursory

understanding of how the brain’s endogenous processes (i.e. its processes that are de-

coupled from the body and environment) are deeply predicated upon this involvement.

Thus, it is important to note that the goal of this project is not to negate the centrality of

the brain’s internal processes in what we might call mind, but rather to arrive at a novel

understanding of how the brain’s internal processes emerge from embodied activity. As

opposed to presupposing the presence of internal representations in our explanation of

an organism’s action and perception, I will come to show how the brain’s internal

processes can be explained through its involvement in the organism’s embodied action.

This inversion will shed new light on the brain’s endogenous internal processes, and

ultimately broaden our understanding of the framework of ecologically embodied

cognition. Thus, it is helpful to understand part two as a critical application of the

framework established in part one. It is my attempt to contribute to the framework by

both demonstrating its explanatory power and expanding its purview. In the process of

striving towards these goals, I hope to release the mind from its black box inside the

head and return it to its embeddedness within the body and environment.

An Overview of the Organism-Environment Relat ionship

The pioneering work of the psychologist James Gibson sent ripples throughout the

cognitive sciences because his account of ecological perception undermined the

internal/external opposition in the relationship between an organism and its

environment. Gibson argued that information is out in the world and that this information

 

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is directly perceived by means of an organism’s active engagement with its environment

(Gibson 1979). Gibson’s account is richly nuanced and extensively articulated, but very

specific features of his work contain broader implications that points towards a novel

framework and possess profound resonances with other accounts from cognitive

science, evolutionary biology, and phenomenology. By demonstrating that there is an

intimate coupling between action and perception, perception is no longer a passive

activity in which the organism receives stimuli from an exterior world and represents the

information internally.

Instead, the organism discovers this information within the environment itself by

means of an unceasing and intimate coupling between its active locomotion and the

environment perceived. This reveals that, although the information perceived by the

organism is in the world, those aspects of the environment that are disclosed are

completely dependent upon the particularities of the organism’s embodied activity,

which adaptively selects aspects of the surroundings that are pertinent to it in and

through the process of its self-perpetuation. These selected (and constructed) aspects of

the surroundings are what configure and constitute the ‘environment’ of the organism.

Broadly speaking, this is to say that what constitutes ‘the environment’ is not the same

for different species or even different organisms within the same species, whereas ‘the

physical surroundings’ are shared by organisms in a given region. While the distinction

between physical surroundings and environment will be parsed out in more detail, the

important thing to grasp here is that a given organism forms a foundational unity with its

environment—those aspects of its physical surroundings relevant to the ongoing

perpetuation of the organism’s life-activity.

 

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Implicit within this is a revision of assumptions in evolutionary biology that maintain

the strict boundary between the organism’s internal processes and the exterior

happenings of an independent environment. Neo-Darwinian approaches to Evolution

have long held that external environmental forces select the genetic traits and random

variation of individual organisms, creating pressures that enable a pre-existing

environment to ‘pick’ those aspects of an organism that best ‘fit’ within the environment.

Organisms ‘fill’ niches by meeting the demands of an environment, which must

necessarily exist independent of the organism (Lewontin 2001). This account therefore

presupposes the pre-given separateness of an organism and its external environment and,

subsequently, that evolution is a unidirectional and linear process that enables

environmental forces to shape the organism’s genome.

Once the environment is understood not as the sum of all that is external to the

organism but as features of the world that are disclosed and enacted as relevant relative

to a particular organism’s life-activity, there is an evolutionary force that moves in the

other direction. An organism, in part, constructs and ‘picks’ its environment, just as the

environment picks the traits of an organism. Instead of a unidirectional process of

external impingement, the organism and its environment form a constitutive feedback

loop such that each is constantly shaping and defining the other; in short, they are

coupled. Instead of simply filling niches, organisms construct them within the

constraints of the given environment. These niches (features and processes of the

environment ‘picked’ and constructed by the organism) in turn become properties of the

environment that feed back to and change the selection pressures on the organism itself

and other biota within the environment. I place the word ‘pick’ in scare quotes because

of the semantic limitations of such a conception. To say the organism ‘picks’ is to

 

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suggest that the organism is a pre-given entity that subsequently selects features of the

environment. However, an organism is the process of ‘picking’ and selection in which its

actions and the environment form a foundational unity (Rouse in press).

In conjunction, these two accounts—the direct perception of the environment by

means of active engagement and the ‘construction’ or selection of the environment as

constituted by the organism’s life activity—point towards a novel understanding of the

organism-environment relationship. The distinction between an organism and its

environment can now be understood as dependent upon their fundamental integralness.

This has two implications. Firstly, instead of internally representing a separate exterior

sphere, the organism can be seen as disclosing the environment in the process of action,

which in turn places constraints on the possibilities for action. As the philosopher of

biology Peter Godfrey-Smith states, “cognition [is] a collection of capacities which, in

combination, allow the organisms to achieve certain kinds of coordination between their

actions and the world” (Godfrey-Smith 2002, 235). Secondly, instead of a linear process

of adaptation to an exogenous environment, evolution can be understood as a highly

non-linear process in which organism and environment are reciprocally transformative.

In both cases, the body plays a foundational role.

Thus, it is essential to grasp that organism and environment are not separate entities

that are then brought into interaction, but rather are integrated and intra-acting (Barad

2007). This is to say that a non-arbitrary boundary between the organism and its

environment is achieved on the condition of their constitutive entanglement (Rouse in

press). A boundary, the condition upon which an organism maintains itself, is upheld

only by means of the dynamic exchange across this boundary—it is not given, it is

achieved and perpetually (re)-enacted. Broadly speaking, an organism and its

 

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environment are mutually dependent such that the environment is only in relation to the

presence of a given organism, as that organism’s environment. Conversely, the organism

is only through its situated position within a surrounding environment. Describing either

will necessitate or imply an illumination of the other, which indicates the primacy of their

integration.

What are internal representat ions and what i s the ir supposed funct ion?

The next section will explore the organism-environment phenomenon at the level of

action and perception. From the standpoint of traditional cognitive science, in order to

successfully perceive and engage with its environment, an organism needs to operate on

‘internal representations.’ Some of the flaws of this account have already been indicated,

if not made explicit. But in order to clearly describe embodied and embedded cognition,

it is necessary to give a careful explanation of the framework to be called into question.

Therefore, I will devote the ensuing section to delineating what it means to say and why

it has been largely assumed that organisms need to internally represent the exterior world

in order to successfully engage with it (Shapiro 2010). Doing so will enable a

demonstration of the shortcomings of this presupposition in the midst of providing an

alternative, positive account, one that not only undermines the need for internal

representation in the processes of embodied action, but also offers a novel and

compelling conception of internal representations as emergent phenomena, evolved on

the condition of embodiment.

The most basic definition of an internal representation in traditional cognitive

science is that which ‘stands in’ for something in the exterior world (Bechtel 1998). Such

a capacity is most lucidly exemplified by an ability to deal with what is absent or covert.

 

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For example, when someone asks me how many pictures there are on the wall back in

my living room at home in Berkeley, I would need to possess a vivid internal

representation to answer the question accurately. This internal representation stands in for

the room in its absence, and enables me to perform cognitive functions (i.e., counting

the pictures) on its basis.

But, of course, this internal representation could never be as detailed and error-free

as standing within and perceiving the room itself, taking the time to count each picture

individually. This is because the internal representation is an extreme simplification of

the room itself, as it involves a profound reduction in information, notwithstanding the

shakiness and malleability of enduring memories (Haugeland 1998). And yet, traditional

cognitive science contends that the perceptual state (when I am actually in the room) still

involves internal representations. Therefore, it is clear that a more nuanced conception

of ‘standing-in’ is required to fully grasp the traditional argument.

The stronger argument is that not only do representations stand in for what is absent

or covert, but also that cognition must operate on internal representations, even whilst

standing in the midst of the room perceived (Bechtel 1998). When this is taken to be the

case, the internal representation loses the error-proneness of memory, and gains the

benefit of up-to-date stimuli from the room itself. Therefore, standing-in is not only in

order to represent that which is absent and covert, but also to represent that which is

immediately present. This definition of representative standing-in is better referred to as

covariance, and is exemplified by brain states that are active only in the process of

perceiving the room. In other words, these brain states carry information about the room,

and thus represent it internally. According to the traditional model, cognition operates

 

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on these dynamic brain states in the process of solving problems (counting) or

coordinating action.

This account seems more plausible because, of course, when I perceive the room I

don’t take what I see to be an internal model, especially when this supposed internal

model is caused by and is covariant with the external environment. And, of course,

cognition absolutely contains brain states (or processes, rather) that co-vary with the

exterior world and thus carry information about it. And yet, to argue for their status as

‘representations’ that an organism operates on in the process of action places the organism

at one remove from the world by framing cognition as a process that is exclusively

internal. The second half of this thesis will inquire at great lengths into the question and

quality of covariance in the hopes of achieving a novel conception of covariance as a

representation that is predicated on embodied action. But as of now, I would argue that

this traditional account is solipsistic in a way that is nearly invisible (Haugeland 1998).

This is because the account rests on various assumptions, all of which are more deeply

rooted in the assumption that the mind is a separable interior sphere that is brought into

subsequent interaction with the world.

The first assumption is that the purpose of perception is to strive towards the

veridical representation of what is ‘out there’ in the world (Akins 1996). In such an

account, the mind not only operates on representations, but also is the very process of

generating these representations—the senses are the material through which these

representations are generated, and these representations enable behavioral outputs that

make possible a successful engagement with the world as it is ‘objectively.' An immediate

problem in this account is that it presupposes that these representations model the world

as it exists apart from the organism, and not merely those features of the world that

 

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selectively or adaptively matter to it. This is a weakness in the traditional account because

the organism need not represent the environment as it exists apart from itself. To do so

is a heavy burden on the cognitive system in that it requires an unnecessarily high

information load and adds an extra step to a process that is much simpler (Haugeland

1998). However, it could be argued that representations are oriented towards modeling

only those features of the environment that matter to the organism, but such an account

still equates the organism’s environment with a subjective interior sphere and thus

remains within the framework to be refuted. Contrary to representing and then picking

or picking by representing, the organism is adaptively coupled to aspects of the

environment that are perceived and enacted as relevant to it through the process of its

embodied life-activity. Such an account is thus suggesting that the very distinction

between the subjective and objective in the organism-environment relationship is

erroneously presupposed.

The second assumption of the traditional model, which is rooted in the first, is that

sense organs possess a shortage of information, requiring that the brain fill in the gaps in

the process of successfully representing the exterior world (Rowlands 1995; Noë 2004;

Gibson 1976). The most vivid example of this assumption is the visual system, which is

frequently regarded as generating representations based on retinal pictures, or snapshots.

Most psychology and neuroscience textbooks have a familiar illustration: lines from an

isolated object converge on a retina and produce an inverted projection into the brain.

Indeed, in these neat models, there actually is a shortage of information, since the retinal

image of the singular object is a two-dimensional snapshot and thus does not contain the

rich detail of the three-dimensional object embedded in its environment. As a result, it is

logically necessary that the brain produce some sort of internal representation. However,

 

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this ‘shortage’ assumption operates on a false premise. It isolates an object from its

environmental context and treats vision as a series of snapshots, not an extended and

active process (Churchland et al. 1994; Gibson, 1976). In so doing, it ignores the

dynamics of an embodied agent and the contextual cues provided by interactions within

the environment as a whole.

This points toward the third assumption—that perception is a passive process in

which the senses simply receive information. Such an account is in line with the

computational approach to cognition, a central component of the traditional model. For

the computational approach, cognition involves linear steps with clear causal linkages:

"Computational descriptions have a beginning, a middle, and an end. An algorithm is

essentially a recipe that makes explicit the steps involved in transforming an input into an

output” (Shapiro 2010, 122). In such a conception, cognition is the algorithm itself. The

senses are the input, and action is the output. When moving from the premise that the

mind is a separate interior sphere, the logical conclusion is that its only access to the

world is through the receptive senses, which enable it to generate an internal model that

is the basis of its active engagements with the world. But perception is not a passive

process that leads to action, and in the context of a dynamically intricate environment,

operating on internal representations would create a mal-adaptive bottleneck of

information (Haugeland 1998). Alva Noë vividly articulates the ludicrousness of such a

conception:

“If the animal is present in the world, with access to environmental detail by movements […] then why does it need to go to the trouble of producing internal representations good enough to enable it, so to speak, to act as if the world were not immediately present?” (Noë 2004, 22)

Instead of placing an internal representation as a causal intermediary between action and

perception, the two are co-constitutive, such that every action is a form of perception

 

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and vice versa. This enables an organism to be constantly in touch with the world itself,

not a representation of it. This claim is the culmination of the ensuing section, and will

be unpacked carefully.

The final mistaken assumption of the traditional model is that it retrospectively

identifies capacities for internal representation in ‘lower’ life forms as a means of

explaining their activity. In so doing, it uses a phenomenon that evolved through action in

order to explain cognitive action, and to do so is homuncular (Rouse, personal

communication; Lewontin 2001). The term homuncular, which means ‘little man,’ stems

from the preformationist theory of developmental biology, which held that sperm were

in fact ‘little men’ that were placed inside women in order to grow to normal size. To

hypothesize a dependence on internal representations in organismal activity is to place a

phenomenon with a complex evolution at its own origin. In so doing, it provides its own

ground while simultaneously going unexplained, just like the homunculus. A more

thoroughly parsimonious account inquires as to how action and perception co-evolved

prior to and as a condition for the emergence of representational capacities (Noë 2004;

Stewart 2010; Sober 2009).

To conclude, the homuncular problem helps to specify and clarify a central argument

of this thesis, which has already been intimated. By negating the necessity of internal

representation in organismal activity within an environment (including our own), I am

not negating the phenomenon of internal representation, but rather seeking to become

clearer on its meaning by situating it within the framework of embodied cognition. (After

all, as I sit in Middletown and count the pictures on my wall in Berkeley, I am indeed

dependent upon an internal representation.) To be more specific, my goal is to invert our

standard understandings by arguing that it is not an internal mind that makes possible

 

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engagements with the environment, but rather that it is as embodied agents immersed

and embedded in an exterior environment that we are able to have any capacities for

internal thought. As Rodney Brooks points out, “it may be the case that our

introspective descriptions of our internal representations are completely misleading and

quite different from what we really use” (Brooks 1991, 4). What we really use are our

bodies. Organismal embodiment is thus the condition for the possibility of internal

representation. As John Haugeland states, “it’s not that all of the structure of intelligence

is ‘external,’ but only that some of it is, in a way that is integral to the rest” (Haugeland

1998, 235). In the next section, I intend to show how organismal perception overcomes

a dependence upon internal representations by demonstrating that embodied action

holistically immerses the organism in an environment and provides it with access to

relevant information through sensorimotor enactment.

Part I—Ecolog i ca l ly Embodied Cognit ion

Embodied Enaction

The environment of the organism consists of those features that matter to it, which

implies that it is highly specific to that organism. Furthermore, the environment depends

upon but is distinct from the organism’s physical surroundings, which are simply the

totality of biotic and abiotic constituents. In this section, I will demonstrate how specific

information in the physical surroundings is revealed to the organism as its environment in

the process of its embodied activity. Overall, I will argue for a middle ground between to

extreme positions. The first extreme is that the organism internally represents a separate

and objective environment by generating an internal representation and proceeds to

‘pick’ those aspects that it deems relevant. The second extreme is that the environment is

 

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externally fixed, such that all organisms have a common experience of a single,

independently existing environment. I argue, instead, that while information resides in

the physical surroundings, it is thoroughly dynamic, nested at different levels, and

unveiled through specific processes of embodied action. For example, with the case of

vision, “a sighted animal is not responsive […] to physically simple properties of light

[…] but rather visible features of the environment that matter to it” (Haugeland 1998,

222). Thus, while physical surroundings do exist independently of a given organism, the

term “environment” can only be understood in relation to the activity of a given

organism. As James Gibson states, “The words animal and environment form an

inseparable pair. Each term implies the other,” and just a page later he clarifies by saying

that “there are no atomic units of the world considered as an environment” (Gibson

1976, 8 and 9). The environment, those aspects of the physical surroundings that matter

to the organism, is enacted and directly perceived, not inferred from a mechanistic world and

represented internally.

Before moving on, I feel compelled to clarify the distinction between an organism’s

physical surroundings and its environment. This distinction is deeply predicated on a

capacity for conceptual articulation. In other words, only from our perspective is the

organism’s environment distinct from its physical surroundings. This distinction has a

long history that is deeply rooted in a scientific worldview that subsumes nature within a

totalized system of physical-biological processes, and it is this understanding of nature

that has come to be equated with the term “environment.” The details of this history

could fill many volumes, but what is essential for the foregoing account is that I use the

term “physical surroundings” to describe the total system of biotic and abiotic processes.

If the sum of those processes was synonymous with the term “environment,” then the

 

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account of ecologically embodied cognition would crumble. Contrary to coming into

interaction with an independent environment, organisms relate directly to the way the

environment reveals itself in the process of the organism’s action. This is the motivation

for Gibson’s claim that there are no ‘atomic units in the environment.’ Thus, “what’s

important here is […] that [the environment] can be perceived—as opposed to inferred”

from the physical surroundings (Haugeland 1998, 222).

The integrated organism-environment is most lucidly exemplified by visual

perception, a process that is predicated upon active disclosure. Motion through the physical

surroundings unveils detailed information that is specific to the organism in motion; it

reveals an environment. This is because every point within the organism’s environment

has its own ‘perspective structure’ and ‘invariant structure’ (Gibson 1976). The former

regards the position of the organism with relation to the environment while the latter

regards the structures and relationships within the environment that are relatively

constant (McCabe 1986). Thus, every perspective structure is essentially a particular

configuration of invariant structure. When the optic array converges on a particular

position within the environment, it carries information about the specific configuration

of invariant features in the environment that are to be perceived by the organism.

Furthermore, it situates these features within their broader context. This enables “the

observer [to specify] a unity as an entity distinct from a background” (Maturana and

Varela 1980, xxii).

But what enables the unveiling of the relationships within the environment that

are constituted by this invariance? The answer is action. When an organism moves

through the physical surroundings, its perspective structure changes in ways that are

relatively constant, which indicates the underlying invariance of the features that form

 

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this perspective structure. Furthermore, the dynamic perspective structure can only be

constituted as such from the particular path of locomotion taken by the organism, which

enables the optic array to simultaneously specify the organism’s dynamic position, or its

trajectory. Invariant structure hinges the dynamic flow of perspective structure, which

makes motion the fulcrum for the entangled processes of exteroception and

proprioception. In each case, the latter underlies the former, enabling a simultaneous

perception of both the dynamic position of the organism and the stable structures in the

environment. As Gibson states, “although they specify different things, locomotion […]

in the first instance and the layout […] in the second instance, they are like two sides of

the same coin, for each implies the other” (Gibson 1976, 76).

Consider the perception of relevant landmarks. If an organism is using a particular

tree to navigate through its environment, how does it determine which tree is the correct

landmark as it changes its position within the environment? Advocates of the traditional

model would assume that the organism must maintain up-to-date internal

representations in order to perceive the tree and act in accordance with it: “In the

traditional model, the brain takes in data, performs a complex computation that solves

the problem and then instructs the body where to go” (Clark 1999, 246). But Gibson’s

theory undermines this three-step process. Instead, since the dynamic flow of

perspective structure illuminates the invariance of features in the environment such as

the landmark, action and perception become a single process. As Gibson states, “If

change means to become different but not to be converted into something else […]

whatever is invariant is more evident with change than it would be without change”

(Gibson 1976, 73). The perception of the navigational landmark is dependent upon the

change that is enacted through motion. It is an embodied knowledge predicated on the

 

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organism’s ability to coordinate its action with the landmark. For example, as the organism

moves toward the landmark, the position of the landmark within the configuration of

the environment will shift in a way that is indicative of both the invariant position of the

landmark as well as the details the organism’s trajectory, prompting the organism to

either continue or alter its route. The perception of the landmark and the action that

relates to it thus become simultaneous and interdependent processes, which embed the

organism in its surrounding environment.

Andy Clark demonstrates the co-constitutiveness of perception and action with an

example from humans—the capacity to catch a fly ball:

“It used to be thought that this problem required complex calculations of the arc, acceleration and distance of the ball [...but] put simply, the fielder continually adjusts his or her run so that the bell never seems to curve toward the ground… The task is to maintain, by multiple, real-time adjustments […] a kind of co-ordination between the inner and outer worlds” (Clark 1999, 246).

Thus, the perception of the ball’s trajectory is dependent upon the outfielder’s capacity

to move in relation to it, not the generation of an internal model.

The various examples of the co-implication of action and perception suggest that

perception is more deeply form of doing, not something that happens to us (Akins 1996).

Even perceptive processes that appear to be more thoroughly passive possess active

components. Philosopher and architect Sarah Robinson gives the following example:

“When eighteen different blind children were each isolated in an anechoic chamber, they were able to reliably detect a four by one foot wooden panel. This means they […] heard the echo of their internal symphony [their circulation] reverberating from the wooden panel!” (Robinson 2011, 45).

The blind children did not perceive the wooden panel passively or statically. Rather, their

bodies interacted with the environment to produce the perception. Of course, examples

of echolocation in other organisms abound in nature, and they reveal a deeper point: in

order to perceive, and organism has to do.

 

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My account so far has revealed how invariant structures are disclosed through the

coordination of action and perception, but has not yet accounted for precisely how these

invariant structures are perceived as individual objects. Importantly, perceiving an

invariant as ‘this or that’ requires capacities for conceptual articulation endemic to

humans (Rouse, personal communication). For example, an organism using a tree to

navigate does not perceive the tree as a tree or even as a landmark, but rather uses the

tree’s invariance to coordinate its action with the environment. However, the capacity to

perceive an object with semantic meaning is deeply predicated upon this organismal

capacity to coordinate motion with relevant features of the environment. It very well

may be that the only significant difference between the organism perceiving the tree by

coordinating its motions and the human perceiving the tree as an individual Redwood,

let’s say, is the enactment or construction of semantic or discursive meaning (Clark

2006). Now this may sound strange, but when looked at critically, it shouldn’t be

surprising that the capacity to bind semantic concepts to objects is entangled with the

capacity to coordinate action with objects.

Alva Noë eloquently describes how the perceptual sense of objects in the world

comes from knowledge or expectation about how these objects would pattern

sensorimotor action. Noë describes the conundrum of the perceived sense of individual

invariants as the problem of ‘perceptual presence’ (Noë 2004). Phenomenologically, even

when a tree is partially occluded, I still perceive the tree as a whole Redwood. Now, from

the traditional perspective, this phenomenological wholeness comes from an ability to

create an internal representation based on past knowledge about Redwoods. As in the

case of the impoverished retinal image, the brain fills in the ‘missing’ information by

generating an internal representation. But we are already prepared with a reason to refute

 

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this conception, namely that vision does not deal with static images, but uses extended

and active perceptual processes. And the moment we shift this fundamental premise, the

priority shifts from internal processes of representation to exterior and embedded

processes of action that are in touch with the world itself. Therefore, the whole tree is

not present or accessible as a picture in mind, but rather as available through the process

of sensorimotor enactment: “We take ourselves to have access to that detail, not all at

once, but thanks to movements of our eyes and heads and shifts of attention” (Noë

2004, 57).

At second look, this should seem obvious. When I perceive the partially occluded

tree, I perceive the sense of its wholeness while not actually seeing its entirety. Indeed, to

generate an image of its entirety without actually moving would in fact require the

generation of an internal representation. But the creation of such an image would

indubitably fail to provide the correct details of the whole tree—where certain branches

protrude, where the trunk gets thicker or thinner—and thus is not the source of my

perceptual sense of the Redwood tree as an individuated object. On the contrary, just as

Noë argues, my sense comes from my implicit competence to move in this or that

direction and gain ancillary information, from an expectation about how my actions will

relate to the object, and from an ability to actually approach and touch the tree, feel its

thickness and roundness, and immerse myself in the rich sensual information that is

provided by the world itself.

But there are indeed times in which this plethora of information is unavailable. Say,

for example, I look at the top of the tree from behind a window with a building blocking

the foreground. I still perceive the tree as a whole and, although I can grasp some of the

tree’s relationship to the building and other objects by moving a little, I can’t actually

 

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place myself in a position in which the whole Redwood tree is visible in its complete

dimensionality. So, what provides the sense of its individuated wholeness? Lawrence

Shapiro, a fairly harsh critic of Noë, offers two ways of interpreting his sensorimotor

theory of perception. In the ‘stronger’ interpretation, the perception of the wholeness

“requires that one actually practice those actions that reveal the sensorimotor

contingency” (Shapiro 2010, 168). On the weaker interpretation, “it is important only

that one has, sometime in the past, acted on the world in ways that created knowledge of

sensorimotor contingencies; perceptual experience now consists in the knowledge one has

acquired” (Shapiro 2010, 168). Shapiro goes on to say that Noë advocates the stronger

interpretation, but I would like to suggest that both of these interpretations radically

misconstrue Noë’s account.

As opposed to either the memory of (weak interpretation) or the actual enactment of

(strong interpretation) the sensorimotor contingencies, my sense of the tree’s wholeness

comes from my practical and implicit knowledge of how to acquire information regarding

the tree (Noë 2004). To make a comparison, the sense of a scientific theory’s accuracy,

or a genuine grasp of what it entails, does not stem from a memory of past experiments

that confirmed it or the abstract theoretical articulation, nor does it require that one

actually enact an experiment to prove it. Instead, it stems from a practical knowledge of

how it could be reliably confirmed given certain material instruments and arrangements.

In short, it comes from practical know-how about what it would take to re-enact the

theory within certain material constraints. Of course, I am not arguing that past

knowledge is irrelevant, but rather that the sure knowledge, the concrete sense of the

phenomenon (whether it be the tree’s individuated wholeness or the accuracy of the

 

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theory), first and foremost stems from a practical and implicit competence over how to

acquire information about the way it implicates itself in the sensorimotor world.

This implies, of course, a necessary openness to the possibility of being incorrect. In

order to go look at the whole tree, I would unthinkingly exit the structure I’m in and

walk around the building that blocks the tree, which would place it in plain sight. But,

upon arriving, I might discover that the tree had been cut down and had its trunk

replaced by a massive steel rod, forcing me to revise my sense of this particular

Redwood. This ridiculous example shows that internally represented memories are not

enough to guarantee a sure perceptual knowledge and, although the actual performance

of sensorimotor action will certainly confirm or disprove the sense of the tree’s

wholeness just as the enactment of an experiment will confirm or disprove a scientific

theory, the sense itself stems from an implicit expectation and practical competence over

what it would take to acquire further information in a world that has already been disclosed

by other sensorimotor enactments.

Shapiro’s belief that Noë’s account argues for the strong interpretation (the idea that

sensorimotor enactments have to actually be made) overlooks the fact that the mind is

always already embedded in a world disclosed by bodily enactments and frames perception

as something that has to be done to particular aspects within the world. Of course

perception depends on actual locomotion and enactment within an environment, but

only inasmuch as action opens a world of possibilities for perception. In other words, as

an agent that implicitly understands how embodied activity relates to the world within

which I have and will continue to move and respond, my perceptual sense of details in the

world comes from implicit knowledge about how my past actions have disclosed the

 

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world, as well as an expectation about how specific aspects of this world will continue to

respond to my sensorimotor activity.

To solidify what this means, I want to provide one more example—a case where

memories conflict. Let’s say you and your friend have a disagreement about how many

keys are on your keychain sitting in a pile at the other side of the table where you’re

seated. You are sure that there are 6—it’s your set and you use it almost every day to

drive your car, open your house, and get in to various lockers. But your audacious friend

is equally confident that there are eight because the last time he borrowed your keychain

he noted the individual keys, and he claims that he can ‘see them in his head.’ During the

escalating argument, you finally realize that you share an implicit agreement about

something even more basic—that the keychain is in fact an object that you use in various

contexts and, as such an object, in order to figure out who’s right about the number of

keys, all it would take is to go and count them. The sense of the keychain as an object

stems not from your explicit internal memories about how many keys it contains, the

times you’ve used them to drive, nor even from your necessarily going and counting

them. Rather, it stems from the deeper practical and non-conceptual knowledge that

going and looking will provide you with the answer, that the keychain is in fact a

keychain that is used in certain ways.

Of course, past experiences are essential to this competence, but what’s important is

not how they’re stored as representational memories, but rather their role as an

embodied knowledge, or ‘muscular gestalts’ (Dreyfus, 1972). The ‘gestalt’ of the

keychain, the sense of it as an individual object with a particular purpose, does not stem

from an internal memory (weak interpretation) or the actual counting or use of the keys

(strong interpretation). Instead, the sense of its wholeness is muscular inasmuch as it is

 

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predicated on an embodied awareness or expectation of how action has, can, and will

relate the object perceived. “As embodied, we need not check for specific characteristics

or a [of the object], but simply for whether, on the basis of our expectations, we are

coping with the object” (Dreyfus 1972, 162). To return to the broader argument,

enactive organismal disclosure opens up a field of possibility and orients you toward a

way of life in which a keychain is an intelligible object associated with certain

sensorimotor activities.

Coupling and Construction

Another way to demonstrate the primacy of the body in the organism-environment

relation is to show how the organism and the environment are intimately coupled. Let’s

place claim this in an evolutionary light: Must an organism perceive its physical

surroundings as a whole in order to successfully survive in its environment? No! Rather

than operating on an abstract model of the world and picking relevant features, an

organism is coupled to concrete aspects of the environment as they become relevant.

Furthermore, as previously noted, there is semantic limitation in the sentence ‘an

organism picks.’ It depends upon the pre-given separation between the organism and its

environment, the organism as an entity and its embodied behavior, and it is these very

separations that I hope to overcome. Instead of an organism as a pre-given entity, it is

necessary to understand the organism itself as a process. An organism is a pattern of

responsiveness to very specific aspects of the physical surroundings, and it is these

aspects that constitute its environment. In other words, particular invariant structures

that are disclosed matter to it in as far as they orient and change in relationship to the

 

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sensorimotor activity that is specific to the process of the organism’s ongoing self-

perpetuation (Rouse in press).

The theory of autopoiesis vividly articulates the organism as an emergent process

that is intimately coupled to its environment (Maturana and Varela 1980). An autopoietic

system is a process of self-production that constitutes and is constituted by its

components. In the process, these components

“continuously regenerate and realize the network of processes (relations) that produced them; and constitute it [the system] as a concrete unity in the space in which they (the components) exist by specifying the topological domain of its realization as such a network” (Maturana and Varela 1980, 79).

Thus, an organism, as distinct from a whirlpool, is an emergent process of individuation

that is oriented towards its own self-perpetuation in the context of an environment

(topological domain) that is specified in and through this process. It is not only that the

organism can only be ‘defined’ in relationship to its environment, as if the account I

were providing were merely a semantic observation. Rather, it is that the organism only is

an organism on the condition of its entangled unity with a specific environment. The

organism can only continue its self-differentiation if it is constantly coupled to the

environment within which it exists by means of an incessant exchange across the

boundary it constitutes. As John Stewart states, “a process of individuation is biological

[…if it] exerts a control of the relation between the organism and its ecological niche such

that the process of individuation can continue indefinitely” (Stewart 2010, 2). The

organismal process extends out into the environment over which it exerts control and

from which it distinguishes itself as an individuated process. The boundary between an

organism and its environment is not given, but achieved. The integrated organism-

environment feedback loop is the condition for the possibility of the organism’s

individuated life process; that is, it is constitutive of it.

 

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In grasping this, it becomes necessary to revise our assumptions about the nature of

the evolutionary process. It is often assumed that the environment is autonomous and

independent of the organisms within it, and that this environment imposes selective

pressures upon the internal and random genetic variation of the organism. But, we now

know that it is naïve to regard the environment as existing prior to the organism. As the

biologist Richard Lewontin states, “just as there can be no organism without the

environment, so there can be no environment without an organism” (Lewontin 2001,

48). After all, a lot of what constitutes the environment of a given organism is not the

autonomous features, but rather results of the actions of organisms themselves. As

organisms change, the environment changes, which feeds back and places evolutionary

pressures on organisms within this environment. There is a constant circularity between

the forces of natural selection and niche construction.

We are already prepared to understand one of the initial constituents of the niche

construction perspective: the organism is the process of selecting those aspects of the

environment that are relevant to its continued self-perpetuation. It does so by disclosing

the environment in the process of its extended locomotion and also by specifying the

‘topological domain’ of its successful self-perpetuation. But the mere selection of

relevant features of the physical surroundings that in turn constitute the organism’s

environment is not a forceful enough account for the paradigm of niche construction,

because it can be argued that these are simply by-products of previous natural selection,

which to a certain extent they are, given the constant feedback between construction and

natural selection (Odling-Smee, Laland, and Feldman 1996). Furthermore, the ways in

which an organism selects or unveils its own environment as relevant to its own life

activity may not necessarily place any relevant selective force on other organisms. As a

 

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result, it is necessary to demonstrate how organisms actually shape their environment so

as to influence the forces of natural selection both on themselves and other organisms.

There are various ways in which organisms construct their environment. As already

apparent in the quote from Stewart cited above, organisms must ‘exert control’ over

their environment, not merely specify it. Smaller organisms, such as bacteria, may exert

control by interacting with and transforming the chemical constitution of their

environment. Larger organisms create webs, nests, or burrows, which alter the

evolutionary pressures on other organisms in the environment. Such processes

prompted the biologist Kevin Laland to draw attention to the necessity to revise the

linear conception of evolution. Instead of a linear process, Laland offers an

understanding of evolution premised on the non-linear, reciprocal relationship between

the organism and its environment:

“The properties of environments cause (some of) the properties of organisms through the action of natural selection, but equally the properties of organisms cause (some of) the properties of selective environments through niche construction […] The selective environments of organisms are not independent of organisms but are themselves partly products of the prior niche-constructing activities” (Laland 2004, 4 and 5).

For example, new generations of species possess ecological inheritances (Lewontin

2001; Laland 2004). An eloquent example is that of forest succession: A forest of white

pine trees can emerge and thrive given enough sunlight, but the second generation of

these trees will be placed in an unfavorable environment due to the forest cover of the

generation before them, leading to the emergence of a new dominant species. There is a

succession that occurs as environmental conditions are altered by the various species in

the ecosystem.

Laland’s argument for non-linearity starts with the gene-centric conception of natural

selection, in which an organism is simply the result of genome’s attempts to adapt and

 

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propagate itself in an exterior environment, and unfolds its implications. In doing so, he

draws attention to a contradiction: If genes’ phenotypic effects do in fact extend into the

organism and its environment, how can it be that the genes are only adapting to an

environment that is separate and exterior? Indeed, if the genotypic makeup of an

organism results in adaptive alterations to this exterior environment, then it must be also

regarded as constructing the pressures to which it and other genotypes must adapt. Just as

perception does not receive an environment, but rather enacts it in ways that opens up

and constrains new possibilities for perception and action, an organism (and its genome)

do not simply receive selective pressures from an environment, but rather create them in

ways that open up and constrain the possibilities for adaptation. The analogous nature of

these respective revisions makes explicit the necessity for transforming conceptions of

both evolution and cognition when establishing the organism-environment relationship

as the launching pad for grasping the mind as embodied.

The eloquence of Laland’s argument is that it takes premises from an opposing

perspective and draws them out to their logical conclusion, leading to an articulation of

the account he hopes to provide. In other words, he starts from the premise of linear

gene-centered natural selection and performs a reductio ad construction. This compelling

technique can be (and has been) effectively implemented in a way that demonstrates the

coupling of brain, body, and world in the process of cognition. Ever since Descartes, it has

been hypothesized that, given the right tools and mechanisms, it could be possible to

place a brain in a vat and simulate reality. However absurd this may seem, the ‘mind as

brain’ intuition is complicit with an input-output perspective that opens up the feasibility

of this ‘envatment’ hypothesis (Anderson 2009). However, starting with the premise of a

 

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brain in a vat, it is all too easy to perform a reductio ad embodiment (Dennett 1991;

Thompson 2010; Haugeland 1998).

One way to do so is to grasp biological necessities of a brain in a vat. In order for a

brain to be, well, alive, it is necessary that it is given sufficient blood flow in order

provide the necessary nutrients, such as glucose, molecules, such as oxygen, and ions,

such as K+ or Ca2+, that are all essential for synapse formation and synaptic activity

(Cosmelli and Thompson 2010). Already, it is apparent that the brain is dependent

various resources and processes a body provides. However, we can theoretically grant

the possibility that they could be simulated in a lab. But all this provides is the condition

to enable neuronal activity, so what does it take to simulate thought, or experience? In

order to account for the neuronal activity of the brain, it is necessary that the blood flow

not only enables the activity, but also is responsive to it: “Once we take into account the

brain’s endogenous workings, it becomes obvious that [the vat…] and the brain need to

be seen as reciprocally coupled and mutually regulating systems” (Cosmelli and

Thompson 2010, 269). In other words, the blood flow not only determines or makes

possible neuronal activity, but also is thoroughly determined by this very activity; they

are constitutively coupled. Providing an envatted brain with something that mimics

blood flow is somewhat feasible, but simulating the coupling between neuronal activity

and brain flow is nothing short of providing the brain with a body. After all, the activity

of the brain (and whole nervous system) is thoroughly oriented towards coordinating

action. Therefore, the activity to which the blood flow is coupled is not internally

isolated, but rather is connected to an entire innervated body, such that the coupling of

the brain and the blood automatically implicates the body-in-the-world.

 

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This brings us back to the concept of internal representation and its role in

embodied action. The representationalist perspective is much more akin to the brain-in-

a-vat perspective, because it treats the body and environment as sources of input and

targets of output, not as constitutive elements in process of action. From this brain-

centered perspective, Dreyfus’ concept of muscular gestalts, and Noë’s concept of

sensorimotor enactment are phenomena that are ultimately stored in the brain. For

example, whilst critiquing Noë’s account, Lawrence Shapiro argues that his account falls

short of showing that sensorimotor competence is something that is always dependent

upon the brain-body-world as a whole, and not just the brain alone. He does so by

arguing that once sensorimotor competencies have been recorded in a brain, the same

brain placed in another body and could still enact those capacities (Shapiro 2010). Quite

frankly, this is massive oversight, and here’s why: Even if we grant that a given

sensorimotor competence is recorded in the brain as an output instruction, it is

impossible to separate this instruction from the specificities of the body in which it was

learned. As John Haugeland states,

“But that some particular [nerve] pulse pattern […] should result in my typing an ‘A’ depends on many contingencies […] It depends on the length of my fingers, the strength and quickness of my muscles, the shapes of my joints, and the like” (Haugeland 1998, 225).

As is evident here, output instructions are thoroughly dependent upon the particular

body in which they are put out, as it were.

But granting that sensorimotor competencies are output instructions, even ones that

are specific to the body in which they were learned, is already granting far too much.

Take the example of a musician. I have played classical piano since childhood, and I have

extremely vivid memories of the exasperated moments before a performance. What

would always imbue a panic is when, out of nervousness, I would attempt to ‘represent’

 

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the piece in my head, note by note, only to realize that I couldn’t. My knowledge of the

piece was not ‘in my head,’ it was embedded in my body and its interaction with the

piano. Much like locomotion in an environment carries information about past motions

and orients the organism towards future possibilities, while in the midst of a piano piece,

playing one note necessarily implicates the previous one’s played, the current notes with

which it harmonizes, and points towards the next ones. An output is not a stored

representation or instruction, but rather a flexible cascade of bodily enactments.

I admit that my anecdote is somewhat flawed, since the brain-centered

representational perspective does not argue that these outputs take the form of

conscious instructions. However, we’ve already noted one problem with the brain-

centered view: the output instructions are always specific to the body in which the skill

was learned and thus can’t be separated from them. But, there is a more compelling

reason that demonstrates why there are no pre-determined outputs at all. Not only does

an output have to be specific to the relatively constant aspects to the body, but also to

the features of the environment that are dynamic. For example, the neuronal outputs

required for two different pianos would have to be significantly different, given the

different texture and resistances of the pianos’ keys. So, not only does my performing a

piece depend upon the specific cascade of bodily enactments, but also the way in which

these cascades coupled with and responsive to the dynamic world. This is why I refer to

this cascade as flexible; it is coupled to the world itself.

Thus, action and perception must be viewed as co-regulating processes that traverse

the brain, body, and world in a closely coupled unity. As Randall Beer states, "strictly

speaking, behavior is a property of the entire coupled brain-body-environment system,

and cannot in general be properly attributed to any one subsystem in isolation from the

 

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others” (Beer in press). But unity is not synonymous with homogeny. All of this

obsession with unity may start to seem ridiculous when, of course, there is a visible

material boundary between the organism and its environment. Thankfully, a concern

such as this one doesn’t confabulate the account, but rather helps to sharpen its

articulation.

The point is not that there are no boundaries, but rather that these boundaries are

themselves enacted and upheld on the condition of constant coupling across and

between them. In other words, the boundaries delineating separation are themselves

properties of the unified system in which they function and from which the draw their

purpose. Recall the definition of autopoiesis: the organism individuates itself from its

environment by constructing a boundary that is maintained only through the constant

intra-action across the boundary. So, in the enactive account, we are not losing a

boundary, but, for the first time, we are gaining a legitimate non-arbitrary one (Rouse,

personal communication). As Karen Barad states, “the line between subject and object is

not fixed, but once the cut is made, the identification is not arbitrary but in fact

materially specified and determinate” (Barad 2007, 155).

Narcissistic Affordances and Nested Significance

Thus, far we’ve come to see how the environment is perceived relative to the action

of the organism. Through autopoiesis and niche construction, we’ve also seen how the

organism and environment are always reciprocally influencing such that they are

mutually constraining. This enabled us to grasp how action and perception are not

products of just the organism, or just the brain, but rather the entire system of organism

(brain, body) and environment (world). At this point, it is necessary to take stock of what

 

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has hitherto been indicated, but partially unexplained. I have previously argued for a

distinction between the physical surroundings of the organism and its environment. The

latter is those features of the physical surroundings that are disclosed as relevant relative

to the life-activity of a particular organism. Thus far, I’ve accounted for how embodied

action unveils the environment and, furthermore, I’ve demonstrated how the organism

specifies and constructs its environment by adaptively coupling with it. However, I have

yet to demonstrate how environments differ between organisms. In other words, I have yet

to fully unfold the implications of the distinction by providing concrete examples.

Consider the difference between a bee and a bear. For these two organisms

respectively, the relationships of invariance that are disclosed in the process of embodied

activity are thoroughly different. The most obvious difference arises from the fact that

the bear and the bee are vastly different in size and possess sensory apparatuses that are

distinct and phylogenetically distant. As a result of these differences, the bear might

perceive the complex invariant structures formed by various trees and boulders, which

may serve as a backdrop for prey that move within the foreground of these invariant

structures. The bee, on the other hand, will perceive the invariant structures formed by

the grass and shrubbery as it uses larger invariant landmarks as a backdrop for locating

food sources. Other organisms it perceives may arise as obstructions to a path or threats

to the availability of this food source. Thus, there are two important things to note. First

of all, the environment of an organism inevitably includes other organisms. Indeed,

“adaptive coupling occurs when a system (typically a plant or animal) evolves a

mechanism that allows it to track the behavior of another system” (Clark 1999, 347).

Secondly, it is important to note that when the bear and the bee perceive the same object

within the environment, the quality or relevance of the information is not the same for

 

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two inter-connected reasons. Firstly, its context provides it with a unique backdrop, and

secondly, the distinct nature of the sensory transducers of the two organisms unveils the

world in fundamentally distinct ways so as to generate this unique backdrop.

Furthermore, another source of the distinct quality of the environment perceived is

the fact that the bee and the bear have extremely different biological concerns. That is,

what each organism perceives is fundamentally shaped by its unique needs and actions

within an environment. As I have frequently invoked, perceptual capacities have not

evolved to reveal a veridical depiction of the exterior world. Instead, perceptual

capacities have evolved in order to reveal to the organism the information that is

relevant to the continuation of that organism’s life process. An organism’s life-activity

and its capacities for perception have a long and interconnected evolutionary history. In

contrast to veridical depiction, the way the world is revealed always has a “self-entered

glow” (Akins 1996, 345). That is, the world revealed can only be understood as having

been revealed to that particular organism in that particular embodied context. As

opposed to simply receiving information, sensory systems, according to Akins, should be

regarded as doing something, a concept that has now become familiar. Sensory systems

are telling the organism about relevant stimuli in a way that has adaptive purpose: there is

a symbiosis between “the information gathering of the sensory system and the motor

needs of the sensory system” (Akins 1996, 351).

The example she provides is the activity of thermo-receptors. Akins eloquently

delineates the fact temperature receptors respond non-linearly to heat and cold, forming

a bell curve of response activity in which the extremes are qualitatively indistinguishable.

Furthermore, she describes the unequal distribution of different kinds of receptors,

demonstrating how different parts of the body have different qualitative expressions and

 

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experiences of temperature. Consider placing your head under cold water—you are likely

familiar with the sensation of an initial burst of extreme cold followed by what feels like

the stabilization to a comfortable warmer sensation. This is because the head, more than

other places of the body, is full of dynamic thermo-receptors, those that respond only to

changes in temperature relative to the given baseline. This shouldn’t be surprising, since

for mammals, maintaining homeostasis around the head is critical for survival, more so

than other parts of the body. Once the new base temperature has been established, the

dynamic responders cease activity and the activity of the static receptors, those that

respond to stable temperatures, starts to kick in at the new baseline.

Such an example elucidates the fact that sensory ‘narcissism’ is not any less

prominent in Homo Sapiens. Indeed, “we, as perceivers [...] tend to mistake our

conscious perspective for insight into how things work […but] even as intentional

conscious perceivers, we are equally in need of narcissistic sensory strategies” (Akins

1996, 354). To state this more strongly, as embodied organisms, humans are thoroughly

dependent upon these strategies. Organisms are not concerned with representing an

objective environment, but rather with discovering and depending upon how the

environment offers itself in the process of an embodied life-activity.

Gibson’s account of ‘affordances’ paints a similar picture. Affordances are the way in

which features or processes within the environment afford possibilities for action and

engagement to particular organisms. Indeed, the organism’s environment could be

construed as a field of surrounding affordances. For example, as the bee flies along its

path, certain flowers and plants afford a source food and a place to land whereas, for the

bear, they afford nothing more than a place to step or sit. In a similar vain, a river

affords a bear a source of food while, for the bee, it may recede beneath the level of

 

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perception or afford a threat if sufficiently proximate. A tree in the environment affords,

for the bee, a place to construct a hive, whereas for the bear, it affords a source of

shelter and possibly food (the bee hive’s honey!).

The aspect of Gibson’s theory of affordances that is most evocative is that an

affordance simultaneously refers to an organism and its environment. It is a subsuming

term, one that highlights the constitutive relationship between them. Furthermore, he

argues that these affordances are directly perceived, which is to say that they are enacted in

the world. Thus, the subtlety of the account is that Gibson is neither saying that the

environment possesses these affordances as independently definable prior to the

organism’s engagement, nor that the organism first perceives the environment,

represents it, and then creates the affordances by engaging the environment in a

particular way. Instead, affordances are properties of the environment disclosed by the

organism:

“The verb to afford is found in the dictionary, but the noun affordance is not. I have made it up. I mean by it something that refers to both the environment and the animal in a way that no existing term does. It implies the complementarity of the animal and the environment” (Gibson 1976, 127).

But this introduces a slightly puzzling conundrum. If the information for affordances

is in the light waves themselves, how can two different organisms perceive a different

environment from the exact same vantage point? In order to provide an adequate

response to this apparent paradox, it is important to note that there is both overlap and

divergence in the environments perceived by respective organisms. Of course the bear

and the bee both can perceive an invariant. But, just like invariants, affordances are not

properties of isolated features of the environment and instead are a property of the entire

configuration disclosed by the organism’s life activity, a configuration that is specific to the

 

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particular engagements of the organism. It is in this holistic sense that the flower affords

nectar for the bee but not for the bear; they are “invariant combinations of invariants”

which are enacted as affordances relative to embodied activity (Gibson 1976, 140). As

Gibson states,

“An affordance cuts across the dichotomy of subjective-objective and helps us to understand its inadequacy. It is equally a fact of the environment and a fact of behavior. It is both physical and psychical, yet neither. An affordance points both ways, to the environment and the observer” (Gibson 1976, 129).

It thus becomes clear how two different organisms can perceive the same physical

surroundings as different environments. And, as already noted, this is largely to do with

evolved differences in the perceptive capacities and biological concerns of different

organisms. For example, humans can’t hear frequencies that other species can perceive,

just as some species can see frequencies that others cannot. The same goes for all

sensory capacities, such as the relatively weak ensemble of olfactory receptors in humans

relative to some of our mammalian ancestors such as rats. Therefore, there are important

divergences between what is enacted and perceived by particular organisms, and it is

these differences, in part, that help to shape how the shared physical surroundings

become distinct environments for different organisms.

Throughout the exposition, Gibson is adamant that ecological perception does not

occupy Newtonian space and time. “If what we perceived were the entities of physics

and mathematics, meanings would have to be imposed on them” (Gibson 1976, 33). In

contrast to the world of Newtonian particles, organisms dwell within an environment of

surrounding affordances that it relates to and perceives directly. Essential to this

possibility is the fact that parts and wholes are nested within each other in ways that are

highly dynamic and contextually determined by particular engagements. Think back to

the keychain thought experiment. Whereas I perceive the keychain as a keychain that’s a

 

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component part in a world disclosed by my particular way of life and the possibilities for

action in my current context, a dog perceives the rattling of a keychain as a solicitation

that warrants a particular sensorimotor response: run to the car! Indeed, when I’m using

the keychain to communicate with my dog, its affordance is as a prop for

communication. Similarly, for the bear, the perception of a tree is enabled by its

situatedness within its context; the tree’s affordance, what it offers, changes if it is

raining, if the bear is pursuing prey, or if it is resting. This tree, in turn, could serve as a

backdrop to the activity of the caterpillar crawling up its trunk, encountering other biota

on its surface, or the bird constructing a nest. In both cases, it affords a stable surface

upon which to move and act. This means that the tree as a unit for the bear can be

broken down into different parts for other organisms and might, at a given moment,

constitute the whole environment for that organism. The keychain as a component

object can in turn serve as the backdrop for the individual keys attached to it.

This account finds resonance with the philosophy of quantum physicist David

Bohm, who writes about the enfolded (implicate) and the unfolded (explicate) order.

According to Bohm, if quantum entities do indeed exist as waves throughout space, then

quantum entities are folded into each other such that every point within space possesses

information about the whole:

“In terms of the implicate order one may say that everything is enfolded into everything. This contrasts with the explicate order regarded in physics in which things are unfolded in the sense that each thing lies only in its own particular region of space (and time) and outside the regions belonging to other things” (Bohm 2002, 225).

In Gibson’s account, this means that every point within the physical surroundings

possesses information (light waves, sound waves, etc) about the entirety of the physical

surroundings. This information is enfolded into each point. What enables parts of this

 

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implicate order to become explicate is the unfolding of the information by means of

embodied action within the physical surroundings, which disclose an environment whose

features are dependent upon the light waves themselves, as well as the specificities of the

organism’s sensory apparatuses and the particular activity of the organism.

Based on this organismal locomotion and the specific goals of the active

engagements, certain aspects of the physical surroundings are unfolded as relevant (as an

environment), while others may remained enfolded or nested within; a flower may

constitute a part of a broader environment for a bee, but it may be the entire

environment for a bacterial cell. These processes are not absent for the bee, but they

remain enfolded, implicate. Perception is not a piecemeal process by which an organism

adds together the discrete or atomic aspects of the physical surroundings to configure a

whole environment. This is another reason why, as Gibson articulates, organisms

(including ourselves) do not perceive the world of Newtonian physics. Instead, an entire

environment is enacted and inhabited through embodied activity, which provides a

context for the significance of individual aspects of this environment.

However, it is also important to note that the whole is simultaneously dependent

upon the features within it. It is not some transcendental condition that is independent

of its parts. As Dreyfus states in relation to ‘gestalts,’ or perceptual wholes, “just as the

elements cannot be defined independently of the Gestalt, the Gestalt is nothing but the

organization of the elements” (Dreyfus 1972, 157). Take, for example, a symphony. A

symphony is nothing without the notes that constitute it, but the notes within it do not

possess their quality unless in relation to the given melody, harmony, and ultimately their

position within the whole piece. Thus, an organism can be regarded as enacting a

symphony where the qualities of its melody (affordance-perception and enaction) are

 

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shaped by the harmonies within which this action is occurring (the configuration of the

environment). This harmonic context is given a new illumination, a new texture, in the

face of this organism’s melody. In other words, the influence is bi-directional, moving

back-to-front and front-to-back, bottom-up and top-down, in a coupled process of

reciprocal unfolding.

The goal of part one has been to both outline and argue for the centrality of the

body in constituting the organism-environment relationship and the cognitive processes

that occur therein, as well as to undermine a dependence upon internal representations

as the foundation of cognitive action. The extent to which the organism-environment

relationship can be explained at the level of the active body demonstrates the importance

of considering the body as a unit in the process of cognition. Of course, the body as a

whole contains within it the nervous system as a component part, a part whose

contribution is indispensible to the body’s overall functioning, and thus it is at this point

that I turn to the brain’s contribution to the organism’s embodied processes. To

conclude, I transition with a quote that connects various threads of this section and

points towards the next:

“The nervous system is often seen as the conductor of the body […] The [tenets of ecological embodiment] suggest a different metaphor: the nervous system is one of a group of players engaged in jazz improvisation, and the final result emerges from the continued give and take between them” (Chiel and Bier 1997, 555).

Part II—A View From Within

The Place of the Brain in Ecological Embodiment From within the current framework, the brain can no longer be regarded as a central

processor with peripheral influence to and from the body and environment, but I take

 

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caution to note that the brain is still fundamentally central to the process of cognition.

Contrary to foreclosing discussions of the role of the brain in cognition, the frame shift

to ecological embodiment offers novel and compelling ways to interpret what the brain

is doing and how it is able to do so. Thus, the remainder of this project will be spent gazing

within the boundaries of the skull with the ultimate goal of elucidating how neural

processes are given a nuanced articulation once the body and environment are regarded

as the foundation of the cognitive system of the active ecological agent. Furthermore,

the movement is bi-directional—by demonstrating the ability of an ecologically

embodied framework to account for neural phenomena, I am simultaneously using

neural phenomena to modify the framework. In other words, the goal is not merely to

tailor the neurological literature to a framework that is complete in its absence, but rather

to integrate this literature into the framework such that it both helps to shape and comes

to fit within it. Overall, this will enable the account of ecological embodiment to become

more highly developed and penetratingly plausible.

Of course, I do not feign to provide a holistic account of the brain’s processes, so I

have chosen to focus on a phenomenon particular to the hippocampus—the activity of

what have been dubbed ‘place cells’ (O’Keefe 2006.). Place cells are pyramidal neurons

in the CA1 and CA3 regions of hippocampus whose activity is specific to particular

locations in a given environment. Individual place cells possess ‘place or firing fields,’

which are spatial distributions within a given environment within which the cell becomes

active; that is, emits excitatory action potentials at increased frequencies. In the words of

O’Keefe, who made one of the initial discoveries of place cell activity in rats, “as the

animal moves around a familiar environment, the typical hippocampal pyramidal cell will

be silent for most of the time, only springing into activity each time the animal enters a

 

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delimited area” (O’Keefe 2006, 1). Thus, place cells are indispensible to the cognitive

processes of spatial learning and navigation. While the neurosciences have, with great

success, come to extensively account for the various facets of place cell activity—their

relationships with each other and other neurons in the hippocampus, their dependence

and influence upon the activity of the organism, and their responsiveness to features of

the surrounding environment—the literature is notably lacking a unified and coherent

explanation of their activity. In other words, the details and the dynamics of place cell

activity are understood with great precision, but the location of place cells within a

broader framework of cognitive science is foggy, at best. It is my suggestion that the

framework of ecological embodiment provides the most exhaustive account of place cell

phenomena, while simultaneously having much to gain from their careful analysis and

incorporation.

The phenomenon of place cell activity serves as a salient topic for the ensuing

discussion of the brain in the context of ecological embodiment because the activity of

place cells can lead to starkly divergent interpretations. In fact, at first glance, the

majority of the explanations of place cell activity appear hostile to the conceptual

framework established thus far. This is because the prominent language for describing

hippocampal place cell activity is that of ‘internal representations.’ It is almost

ubiquitously asserted that place cells serve as internal representations of the

environment, providing an internal cognitive map that enables the organism to perform

spatial navigation tasks such as finding novel routes to known destinations (O’Keefe et

al. 2006; McNaughton et al. 1996; Best et al. 2001). In other words, after scanning the

literature and absorbing its language, it would appear as though the organisms under

study (which are almost exclusively rats) operate on an internal representation of space

 

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generated by the place cells, which is precisely the language that was refuted in the

previous section. For example, McNaughton et al. state that the discovery of place cells

draws attention to their role “in the development of high-level internal representations

of allocentric spatial relationships and in learning to solve problems that require memory

for those relationships” (McNaughton et al. 1996, 173).

It could be argued many of the scientists studying place cells are unconcerned with

the broader philosophical implications of such language. Furthermore, we will come to

see that they also offer plenty of descriptions that give credence to the framework of

ecologically embodied cognition. Indeed, it is partly the co-presence of these idioms that

makes the location of the place cell literature within a coherent framework of cognitive

science so unclear. However, notwithstanding an explicit awareness of the philosophical

implications, it is my fear that the use of the language of internal representation

exemplifies an intuitive pull towards a conception of cognition that is fundamentally

misguided, for all the reasons hitherto explained. Furthermore, by falling prey to this

pull, the science to some extent comes to misinterpret, and perhaps misunderstand, the

data that it has so successfully generated.

Thus, it is not merely that interpretations of the data depend upon philosophical

implications that are separate, but also that certain philosophical assumptions have

scientific implications—the questions that are asked, the experiments that are designed,

and ultimately the way that the data is presented. For example, “instead of asking, ‘What

is the neural basis of adaptive behavior?’, one should ask ‘What are the contributions of

all components of the coupled system and their interactions to adaptive behavior?’”

(Chiel and Beer 1997, 555). By wading through the scientific data and the philosophical

language that is in tension throughout the literature, I intend to shift our orientation and

 

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make explicit the extent to which the framework of ecologically embodied cognition

successfully accounts for the data, despite the persistent dependence upon the language

of ‘internal representation.’ In doing so, I hope to become clearer on a novel and precise

meaning of ‘internal representation’ in the context of ecological embodiment and

demonstrate the function these place cell representations may serve in the cognitive

processes of spatial navigation. By clarifying a framework that successfully accounts for

place cell phenomena, I hope to point towards questions that can influence the

continued study of neural processes that participate in cognitive systems.

The rest of part two will be divided into two sections. Firstly, I will outline some

essential components of place cell activity and demonstrate their indebtedness to the

organism’s embodied action and the environment within which this action occurs. This

will enhance our understanding of place cell phenomena while beginning to situate them

within the framework of ecologically embodied cognition. Secondly, I will confront the

tension between internal representation and embodied action head on through three case

studies.

The Descriptive Aspects of Place Cell Phenomena There is no sharp boundary between the description and explanation of place cell

phenomena, so as I move into a section that is predominantly descriptive, I will take

caution to indicate the ways in which the descriptive aspects of place cell phenomena can

be explained through the framework of ecologically embodied cognition hitherto

established. Conversely, in the second section, I will come to introduce novel descriptive

details as I ultimately assess and explain the relative merits of representational versus

 

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embodied frameworks for explaining place cell activity. To begin, the ensuing overview

will discuss three essential aspects of place cell activity:

i) The location versus the rate of place cell firing.

ii) Origins of place field formation—the complementarity between allocentric

(exteroception) and egocentric (proprioception) information and their relative

contributions to place field formation and activity.

iii) Plasticity—reuse and remapping.

In all cases, the importance of the organism’s active locomotion and the contextual

specificities of the environment as it relates to that motion will be shown to have

fundamental control over the various facets of place cell activity. This consideration will

thus serve as the launching pad for situating place cells within the framework of

ecological embodiment and enable us to come to a novel understanding of internal

representations and their indebtedness to and embeddedness within the framework of

ecological embodiment.

i) The location versus the rate of place cell firing—When considering place cell activity, it is

necessary to note the distinction between where they fire and how much they are firing. A

place field (or firing field) is the spatial distribution in a given environment within which

a particular hippocampal pyramidal neuron exhibits any activity above its resting firing

rate (O’Keefe 2006; Wilson and McNaughton 1993; Best et al. 2001). However, the

spatial distribution of the place field is heterogeneous with regard to the rate of place cell

firing. In other words, the center of a place field is the location in the environment

within which the cell exhibits maximal firing rates, whereas the peripheries of a place

field are the locations within which the cell is active at levels below maximal rates but

above resting rates. Thus, the firing frequency of a place cell is highest when the animal

 

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enters into the location that is equated with the center of its place field and becomes

progressively lower as the organism moves away from the center and towards the

periphery of its place field. Conversely, as the organism moves from the periphery

towards the center of its place field, the firing rate of the cell is gradually increasing.

Thus, the activity of the place cell is dependent upon and indicative of the active locomotion

of the organism through the environment.

The particular spatial distribution of place cell activity and its connection to

organismal locomotion introduces two interconnected considerations. Firstly, since place

cells possess place fields that are distributed and heterogeneous with regard to firing rate,

place fields between cells are often overlapping. However, at these shared points in space,

cells with overlapping place fields have different firing rates. Thus, at a given location,

there are always multiple place cells firing. That is, hippocampal place cells do not fire in

isolation, but rather fire as ensembles (Wilson and McNaughton 1993). The ensemble

activity of place cells has robust correlations with the locomotion of the organism

because, at a given location, there are cells whose activity relates to the organism’s

current location (cells that are at maximal firing rates) as well as the organism’s previous

and possible future locations (cells at firing rates below maximal but above resting).

Ensemble activity therefore encodes the trajectory of the organism’s action within the

environment.

This leads to the second consideration. It is important to note that the trajectory

encoded by the ensembles is always specific to the environment within which the action

is occurring, as well the specific details of the organism’s engagement. In other words,

the location of place fields and the firing activity of the place cells will vary whether the

 

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organism is exploring, pursuing a goal, in an open field cylindrical environment, or in a

linear track environment:

“As part of the rat’s cognitive system place cells are strongly influenced by what an individual animal is doing […] The response properties of place cells depend on the experience of individual rats, the task they are doing, and what can only be called their perception” (Bures et al. 1997, 348).

The beauty of this passage is the integration of action and perception that is fundamental

to place cell activity. The organism does not merely perceive the environment so as to

generate an internal model that governs action, but rather its action in conjunction with its

perceptive faculties enables place cell activity to be sensitive not only to the environment

by means of perception, but also to the unique trajectory of action within the

environment perceived. After all, “what the organism senses is a function of how it

moves, and how it moves is a function of what it senses” (Thompson and Varela 2001,

242).

The way this relates to ensemble dynamics is two-fold. First of all, an organism can

occupy the same location in the same environment and exhibit divergent place cell

ensemble dynamics, both in terms of which cells are firing and how much they are firing.

This is due to the contingencies of the physical trajectory (i.e. entering from north or

east) and the motivational behavior (i.e. pursuing a reward or exploring). Second of all,

the organism will perform the same action in different environments and exhibit

divergent ensemble dynamics. After all, an essential function of place cells is to

differentiate between environments by forming a distinct ensemble of place fields.

Through action-mediated encoding, the ensemble activity of place cells provides the

animal with an awareness of the details of the environment in which it is embedded and

how its body relates to these details. Ensemble dynamics will be taken up in all of the

case studies, so a discussion of their status as representations will be taken up later. At

 

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this point, however, it has become necessary to grasp the processes of place field

formation so as to better understand how the place fields of individual cells themselves

differ with respect to different environments.

ii) Origins of place field formation—Think back to Gibson’s account of the interdependence

of perspective structure and invariant structure. The perspective structure of the

environment is predicated on the trajectory of the organism’s locomotion, whereas

invariant structure is the stable features of the environment whose stability hinges the

dynamic perspective structure that emerges through this motion. As it turns out, the

intertwining of constancy (invariant structure) and change (perspective structure) in the

process of organismal action is indispensable to the formation of place fields—it is how

the organism comes to form stable place fields that are specific to a broader

environmental context and sensitive to a position within that context:

“The hippocampus […] encodes allocentric space, the location of the organism with respect to important places in the environment […] This information comes not only from the configuring of exteroceptive stimuli, but also from the vestibular system and other proprioceptive systems” (Best et al. 2001, 463). Of course, this highlights the essential experience-dependent nature of place field

formation. Indeed, many of the experiments that study place field activity under varying

conditions require that the organism (the rat) first establish stable place fields distributed

throughout an environment by allowing the rat to explore in pursuit of food (O’Keefe et

al. 2002; Anderson et al. 2006; Wilson and McNaughton 1993; McNaughton et al. 1996).

Thus, to preview an aspect of the discussions to come, even if place cells are regarded as

internal representations that enable sophisticated navigational activity of the organism,

they must also be regarded as themselves enabled by the activity of the organism; the

 

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causation is reciprocal. The implications of this two-way causation will be taken up in

later case studies.

Despite the complementarity between allocentric and egocentric stimuli, much of

the place cell literature is devoted to understanding the isolated contributions of

allocentric and egocentric information on the activity of pre-formed place fields

(O’Keefe 2006; Bures et al. 1997; Burgess et al. 1997). In other words, in artificial

conditions, experimenters are able to selectively manipulate these sources of information

and study how they influence place field activity. Fascinatingly, in different contexts, the

various sources of stimuli (whether allocentric or egocentric) exert different degrees of

control on the stability and activity of place fields. For example, in some instances, a

shift in distal cues in the environment causes place cells to shift their place fields within

the environment so as to retain their relationship to the shifted environmental cue:

“A single visual cue, a white card attached to the inside wall of a cylindrical arena, could exert almost total control over the location of place fields. Rotations of the card were accompanied by equal rotations of the place fields” (Best et al. 2001, 464).

When place fields co-vary with a shift in an environmental cue, it enables the organism

to continue to maintain an awareness of how its movements will alter its position relative

to that cue (how its perspective structure relates to a particular aspect of the invariant

structure in the process of motion). This is significant because certain cues in the

environment may possess learned relationships with locations such as food sources,

enabling them to serve as landmarks for navigation. Thus, maintaining an awareness of

position relative to significant allocentric cues enables the organism to be aware of how

to gain access to a desired location by maintaining coordination between its interior

processes and the exterior world.

 

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The language of relevance and significance with regard to isolated aspects of the

environment resonates with previous assertions that the organism is a process of

selecting features of the physical surroundings that constitute its relevant environment.

Further data with regard to the manipulation of allocentric stimuli and its effect on the

ensuing activity of place cells serves as potent evidence for this assertion. For example,

“in experiments where several distal spatial cues are available, [the] removal of one or

more of these shows that the majority [of place fields] are maintained as long as any two

of the four cues are present” (O’Keefe 2006, 6). Thus, the organism buffers certain stimuli

(Godfrey-Smith 2002). This is significant because it is clear that the organism does not

generate an internal model of the surroundings in their completeness and proceed to

choose relevant features. Nor can we say that the organism perceives those features and

then chooses to model only specific parts. Instead, the organism is itself selectively

sensitive to its environment in varying contexts, as exemplified by the selective sensitivity

of place field stability to various facets of environmental dynamics. In a famous essay

that devises a challenge to the necessity of representation in cognitive processes, Rodney

Brooks, a pioneer in the field of experimental robotics, demonstrates how selective

buffering is essential for the creation of agents that can cope with a dynamic

environment:

“By not trying to have an analogous model of the world, centrally located in the system, we are less likely to have built in dependence on that model being completely accurate. Rather, individual layers extract only those aspects of the world which they find relevant” (Brooks 1991, 144).

Thus, contrary to being a central processor that generates a rich internal representation,

place cell ensembles can be viewed as essential features in a broader embodied system

that is sensitive to the dynamics of movement through the world itself.

 

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The selective influence of allocentric information has led to hypotheses that place

cell ensembles serve primarily as path integrators (McNaughton et al.1996). That is, the

locations of place fields in an environment and the particular pattern of cellular

connectivity are influenced primarily by ideothetic self-motion information. In this

paradigm, the function of allocentric sensory stimuli is to sharpen and heighten the

resolution of place fields in the given environment: “Repeated pairings between these

ideothetically updated place representations and landmark information would

subsequently allow the landmarks […] to correct for drift in the path integrator”

(McNaughton et al. 1996, 175). The shift from viewing hippocampal place cells as

representing allocentric space to integrating self-motion information in relation to

relevant landmarks marks a shift from prioritizing representing an independent world, to

prioritizing staying in touch with the world itself through processes of active perception.

According to Haugeland,

“The trouble with representation is that, to be good enough, it must be relatively complete and relatively up to date, both of which are costly in a dynamic environment. Perception, by contrast, can remain happily ad hoc, dealing with concrete problems only as they arise” (Haugeland 1998, 219).

McNaughton et al., who provided an early and compelling articulation of the path

integration approach to interpreting place cell activity, offer a lucid articulation of

Haugeland’s argument in the context of place cell activity, which is worth quoting at

length:

“An allocentric map of the environment, based on stored relationships among landmarks, would be expected to require considerable time for its acquisition. Moreover […] storing object-centered relationships among n landmarks requires storage of the order n2 items. In contrast, if direction and distance information are available, then a vector-based storage system can, in principle, be constructed, whose storage requirements increase only linearly with the number of landmarks” (McNaughton et al.1996, 174).

 

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In other words, it is much more burdensome to represent how landmarks relate to each

other independently of the organism, than it is for the organism to perceive how

landmarks relate to itself based on direction and distance information that is determined

in relation to the organism’s locomotion. Furthermore, information about the

relationship between landmarks in the environment, which is costly to represent, is made

available once an organism knows how the relative distance/direction of individual

aspects of the environment change in relation to itself in the process of its locomotion.

As the organism enacts this motion, the resolution of place fields (and thus the precision

of the organism’s spatial awareness within the environment) is drastically increased.

Thus, it would appear as though when place cells are regarded as path integrators

whose place fields are based on locomotion, it inextricably implicates the perception of

invariant structures in the environment that are relevant to the organism. In fact, the

perception of invariants is not only implicated in path integration, but rather place cells

as path integrators are themselves dependent upon the perception of invariants insofar

as the path integration system would be imprecise and dysfunctional in the absence of

this perception. Thus, the function of path integration is not merely to track movements

of the isolated organism, but rather to track its situated dynamic relationships to specific

features of the surrounding environment so as to provide a persistent sensitivity to

relevant stimuli.

In conclusion, it is important to note the complementarity of sensory modalities in

the formation and maintenance of place fields. According to O’Keefe, “place cells use

information from different sensory modalities to identify landmarks or features of the

environment. These cells are not totally dependent on any specific sensory modality”

(O’Keefe 2006, 6). The integral influence of multiple sensory modalities on the activity

 

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of place cells serves two functions. On the one hand, it enables flexibility in place cell

ensemble activity such that the ensemble can shift its dependence upon these various

modalities and maintain stable place fields if certain senses become deprived. It allows

the organism to be an iterative process of both perception and buffering. Conversely, it

enables individual place cells to be sensitive to changes in isolated sensory modalities,

which can promote a process that has been called partial remapping, where individual

place cells alter their place fields within a stable ensemble in response to isolated sensory

stimuli, while the rest of the ensemble retains their place fields (Jeffrey 2011). The

relationship between individual place cells and the ensemble as a whole will be centrally

discussed in an ensuing case study. But for now, the capacities for place cells to either

maintain or alter their place fields in response to dynamic sensory stimuli points toward a

third component of place cells that has hitherto been pre-supposed, but unexplained:

their intrinsic plasticity.

iii) Plasticity: Reuse and Remapping—The fact that place cells are able to form distinct place

fields within different environments is indicative of their intrinsic plasticity. Furthermore,

their sensitivity to changing stimuli (i.e. their ability to re-map within an environment in

response to a shift in a relevant landmark) is a hallmark example of their essential

malleability. Thus, the basic tenets of place cell plasticity have already been at work

throughout the foregoing exposition. However, it is now time to explore this concept

with more precise detail and begin to unfold some of the implications it has for the

framework of ecological embodiment.

The first thing to note, which has already been intimated if not made explicit, is that

the same cell can form place fields in multiple environments. This phenomenon is best

 

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described as the neural reuse of individual cells as they participate in different cell

assemblies underlying the spatial encoding of distinct environments. The neural reuse of

cells that encode for multiple environments exemplifies a type of plasticity in which

redundancy in the underlying neural architecture correlates with divergent qualitative

experiences. Alva Noë and Susan Hurley articulated an inverse type of plasticity when

they observed how a re-wiring of underlying neural architecture (i.e. visual input running

through the auditory cortex) resulted in qualitative experiences that were remarkably

similar (Hurley and Noë 2003). The implications this latter evidence has for embodied or

enactive cognition is that, if

“different neural areas […] can support the same kind of experience […then it is] because the various configurations all come to support the same patterns of interaction with the world, and it is these patterns (not any resultant neural goings-on) that actually constitute […] the experience” (Clark 2012, 758).

Thus, the experience of the organism (or the individual) in an environment is not merely

a product of neural activity, but rather a product of how the neural activity patterns

sensorimotor engagement within the world. It is clear that the same argument can be

made for the kind of plasticity exemplified by place cells. If the same underlying cellular

architecture encodes for multiple environments and provides the organism with a spatial

awareness that is distinct in different environments, then the spatial activity (or

awareness) of the organism must be regarded not as exclusively dependent upon the

neural activity, but rather upon how this neural activity influences and is influenced by

the organism’s sensorimotor behavior.

Since place cells participate in the spatial encoding of multiple environments, it is

important to note that the topographical relationship among the place fields of cells in a

given environment has no correlation to the topographical relationship among the cells

in the brain. In the words of O’Keefe, “neighboring pyramidal cells are as likely to have

 

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fields distant from each other in an environment as to have fields close together”

(O’Keefe 2006, 3). There are clearly benefits to having no pre-given neural topography

for place field relationships, in that it enables the organism to be sensitive to a dynamic

environment as opposed constrained by an internal model possessing a pre-given

structure: “the spatial relationships of the stimuli and features which make up a given

environment cannot be known a priori […] Therefore no predetermined topography can

exist” (O’Keefe 2006, 3). In other words, in order for the organism’s place cell activity to

promote successful navigational behavior, it must let action within the environment

determine the patterns of that activity. Since the environment of an organism and

components within the environment are constantly shifting, expanding, merging, or

shrinking, place cells must be plastic enough to form fields in any point in a given

environment. If proximal place cells always possessed proximal place fields independent

of sensorimotor influence and, furthermore, if these place fields underlay the organism’s

sense of spatial awareness, then different environments would be nearly indistinguishable

due to the persistent homology between the internal models.

Thus, a huge component of the capacity for place cells to completely re-wire in

distinct environments is that cells are never only connected to their immediate

neighbors, but instead have dispersed connections throughout the entire hippocampal

region (and beyond). This introduces a distinction that is worth making explicit: just

because proximal place cells don’t possess proximal place fields, it does not mean that

cells with proximal place fields lack synaptic connectivity. The axons and dendrites of

pyramidal neurons span great lengths, enabling the cells to form synapses with cells that

are anatomically distant. This has huge implications for the amount of information that

can be encoded by the hippocampal network. For example, if there is a network of 100

 

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cells, but each cell has connections with only two other cells, then there is a maximum of

200 available connections that can encode environmental information (i.e. through

mechanisms of Hebbian plasticity). Conversely, if each cell forms a hundred

connections, then there are 10,000 available connections. Thus, this network’s capacity

for encoding information is 50 times greater than the prior one. This capacity increases

exponentially as the number of cells and connections in the network increases, which of

course is the case in a real mammalian brain. Thus, by generating distinct patterns of

place field formation in response to the dynamic environment, these highly integrated

networks better enable the organism to be sensitive to small differences between

environments that are similar. This in turn allows the organism’s action to be more

sensitive to the complexities of the environment that have been discovered and encoded

through the connected processes of organismal action and place field formation. This

once again highlights the co-constitutiveness of action and perception in spatial

awareness and place cell activity.

As an illustration of the processes of reuse and remapping, Lever et al. demonstrated

that repeated exposures to two environments resulted in shifts in the respective place

fields of a given cell in an ensemble. It had been previously asserted that a major

influence on place field location was the distance between two or more walls in a testing

environment, which would thus predict that, in enclosures of similar sizes but slightly

different shapes, the same place cells would exhibit place fields in similar locations. Thus,

the study consisted of two environments of similar size that differed only in their shape:

circular or square. On the initial days of the experiment, the place cells in the sampled

ensemble exhibited firing fields that were in similar locations within both environments.

However, over the course of 21 days in which the organisms were repeatedly exposed to

 

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both environments, the place fields of the individual cells in the network began to

diverge in the respective environments, in some cases moving to different locations and

in other cases falling completely silent. This led the experimenters to conclude “that

environmental experience leads CA1 place cells to discriminate between environments

on the basis of geometrical features […] and to maintain this discrimination for a long

time” (Lever et al. 2002, 93). Thus, the sensitivity of place cell activity to the

environment extends beyond the relative distances between the confines of the testing

environment and into the details of its geometry. In a sense, the organism knows which

environment is circular and which environment is square, despite their similarity in size,

color, odor, etc., because there is a global shift in the ensemble dynamics of the place

cells. And of course, this knowledge is deeply predicated upon the experience and

expectations of active exploration. Thus, the plasticity of highly integrated hippocampal

networks enables the organism to perceive extremely subtle differences in its immediate

environment by means of action-mediated encoding.

Representing or Embedding? Three Case Studies

The exposition thus far has comfortably situated place cell phenomena within the

framework of ecologically embodied cognition. In describing how place fields form and

evolve through environmentally situated action-mediated encoding, I have steered clear

of the language of internal representation so prevalent in the literature itself. The primary

reason for this is that the language of internal representation doesn’t change how we

understand the particular aspects of place cell phenomena outlined in the exposition thus

far. That is, one could still regard the ensemble activity of place cells in a given

environment as an internal representation in the sense that they are brain processes that

 

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co-vary and carry information about the environment, while still embracing them within the

framework of ecologically embodied cognition. Despite their status as covariant internal

processes, place cells violate all the presuppositions endemic to the traditional

framework of internal representation that were outlined in the introduction.

Firstly, place cells do not encode a veridical depiction of a separate environment, but

rather encode how relevant features of the environment relate to the organism and its

action. Secondly, the perceptive processes that enable the formation of place fields are

not passive. Instead, place cells are fundamentally indebted to the embodied action of an

organism situated within its environment. Thus, to conclude, place cell representations

exemplify a fundamental inversion of the traditional approach to cognitive science:

internal place representations are not the condition for the possibility of action, but

rather action is the condition for the possibility of representations, if that is what we are

to call them. These representations must therefore be regarded as indebted to action and

embedded within a broader system that spans across the brain, body, and world (Chiel

and Beer 1997; Clark 1999). In other words, action does not operate on internal

representations, but rather internal representations depend upon and operate on action.

However, I also avoided the language of internal representation because I have not

yet confronted aspects of place cell activity that appear more thoroughly

representational. But by articulating foundational tenets of place cell activity within the

framework of ecological embodiment, I have not shied away from these difficulties, but

rather have paved the way for understanding them more lucidly. It is at this point that I

turn to the particular aspects of place cell phenomena that are more intrinsically

representational, with the ultimate goal of achieving a novel understanding of processes

of internal representation within the system of ecologically embodied action. Thus, the

 

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rest of the analysis of place cells will be devoted to three case studies that attempt to

parse out the role of representations within the framework of ecologically embodied

cognition.

i) Predicting the Path: Does action depend solely upon internal models? ii) Operating on Memory: Place cell projection and simulation iii) Beyond Covariance: Self-organization and predictive processing

i) Predicting the Path: Does action depend solely upon internal models?

In his essay ‘Mind Embodied and Embedded,’ John Haugeland introduces a thought

experiment inspired by the work of Herbert Simon, a leading researcher in the field of

Artificial Intelligence. He wonders, when considering the path of an ant walking along a

beach, whether the details of the ant’s path are determined by the ant’s internal processes

or by the “close interaction between the ant and the concrete details of the beach’s surface”

(Haugeland 1998). If the case is such that the ant’s path is determined exclusively by its

internal representation or model of the beach,

“then the importance of the beach would be reduced or eliminated, [whereas if] there is constant close coupling between the ant and the details of the beach surface, and if this coupling is crucial in determining the actual path, then […] the ant and beach must be regarded more as an integrated unit” (Haugeland 1998, 217).

By arguing for the latter, Haugeland articulates a version of organism-environment

entanglement that I have repeatedly advocated—it is not that there is no boundary

between the organism and its environment, but rather that this boundary is perpetually

re-enacted on the condition of their ongoing integration and intra-action. Thus, the

details that govern an organism’s action must be looked at orthogonally, regarding both

the details of the environment as well as processes internal to the organism.

Place cells offer an interesting contribution to the either-or of Haugeland’s thought

experiment, since the activity of an ensemble of place cells at a given moment carries a

 

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remarkable amount of information with regard to the organism’s position, as well as its

position relative to the particular trajectory of its action. In fact, in a famous experiment

by Wilson and McNaughton, the actual path of a rat through a controlled environment

was reliably reconstructed by observing the activity over time of an ensemble of place

cells with known firing fields. In order to achieve this reconstruction, the study began by

gathering cellular firing data from an ensemble of hippocampal place cells as the

organism explored within the confines of a control environment. After establishing clear

readings from the cells, the study calculated the mean firing rate of all cells at a given

location in space. Finally, after place cell recordings were gathered during a trial in which

the scientists were blind to the rat’s motion (which was recorded by a camera), the study

sought to re-create the path based solely on the firing rate data from the place cell

ensemble: “The actual rate vector over each 1-s epoch was compared with each expected

rate vector, and the site of maximal correspondence was assigned as the estimated

location” (Wilson and McNaughton 1993, 1056). In the cited passage, a ‘rate vector’ is a

snapshot of ensemble activity at a given time. Upon comparing the predicted path with

the actual path, the correlations were striking, and it was found that “1-cm accuracy over

1 second would require about 130 cells” (Wilson and McNaughton 1993, 1056). Thus, in

response to the question, “is the activity of a population of cells over a brief interval a

robust predictor of spatial location?” the study was able to offer a decisive yes (Wilson

and McNaughton 1993, 1056).

Thus, it would seem as though Haugeland’s claim was trumped by a robust set of

data indicating that the details of organismal action are predictably re-created by an

analysis of internal processes alone. But consider how the experimental question can be

framed differently. It would seem to me that another question was answered with equal if

 

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not more force: ‘is the activity of an organism over a brief interval of time a robust

predictor of place cell activity?’ In other words, the experiment did not prove that the

details of organismal action are a result of internal representation, but rather that there is

a constant coupling between the situated action of the organism and the internal processes

of place cell activity. After all, the study required that the organism form stable place

fields through a prolonged process of active exploration in order to establish a consistent

covariance between the location of the organism at a point in space, and the particular rate

vector of the place cell ensemble.

Thus, we return to the question of whether constant covariance between the external

and internal processes is enough to constitute place cell phenomena as representations.

One of the prominent theoretical articulations of the role of representations in cognitive

systems, which was introduced in the introduction and has been implicated throughout

this case study, is that representations carry information about that which is represented

by co-varying with it. Thus, in the foregoing example, place cells carry information about

the animal’s physical location within a specific environment, and thus stand in for them.

But “most theorists recognize, however, that reliable co-variation is not sufficient to

establish something as a representation” (Bechtel 1998, 298). Thus, in order for a

cognitive system to possess a representation, there are “three interrelated components in

a representational story: what is represented, the representation, and the user of the

representation” (Bechtel 1998, 299).

In the place cell study discussed here, there are only two components present in the

cognitive system: the organism’s action within the environment and the place cell activity

that encodes this environmentally situated action. In other words, in the case of place

cell ensembles, what is represented and the user of the representation blur into a single

 

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entity. Thus, it can just as easily be said that the place cell ensemble operates on

organismal activity as it can be said that organismal activity operates on the place cell

ensemble. As a result, in order for place cell ensembles to serve as representations, we

would have to embrace the familiar traditional model of organismal activity that has been

thoroughly disproven, one in which “perceptual modules deliver a symbolic description

of the world and the action modules take a symbolic description of desired actions and

make sure they happen” (Brooks 1991, 143). Forgive me if my prose becomes trite for

once again indicating that in the case of place cell ensembles, action and perception

appear as one process, not two, such that embodied action and place cell activity form a

constitutive feedback loop, removing the causal intermediary that would be reputed as

the cognitive representation.

It thus appears as though Haugeland’s hypothesis holds its ground—the

particularities of an organism’s path are dependent upon an intimately coupled

interaction between the details of the environment and the internal processes of place

cell ensembles. The Wilson and McNaughton study was successful because of this

coupling, not in spite of it. By predicting spatial location based on place cell ensemble

activity, the study demonstrated first and foremost that this ensemble activity is

indicative of organismal action inasmuch as it is derived from it. However, if this

conclusion feels incomplete for the reader, that’s because it is. After all, contrary to

disproving the status of place cells as representations, “co-variation is often a primary

tool in discovering what serves as a representation” (Bechtel 1998, 298). In other words,

by carrying information about the environment within which the organism is embedded,

place cells do indeed meet a foundational criterion for status as representations. Within

this study in particular, however, all that was demonstrated was the reliable covariance

 

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between organismal action and place cell activity and, as Bechtel pointed out, this falls

short of confirming the status of place cells as representations. The ensuing cases studies

will thus look more deeply into how the organism’s brain uses the reliability of this

covariance in the sense of operating on it. In doing so, I hope to confirm their status as

representations of a novel kind by demonstrating how these representations emerge

from and are thus dependent upon embodied action and not vice versa. In doing so, I

hope to overcome the homuncular problem of the traditional approach to cognitive

science.

ii) Operating on memory: Place cell projection and simulation In my initial description of what constitutes a representation, I introduced a

foundational conception: representations as brain states or processes that stand in for

that which is absent or covert. In other words, when certain aspects of the environment

are not directly available, internal representations are the means by which an organism

relates to these absent aspects. Think back to my example—as I sit here writing in

Middletown, the only way to count the pictures on the wall in my living room in

Berkeley is by use of an internal representation, or in other words, a memory. Thus far, we

have come to see how place cell phenomena does not qualify as representational in the

processes of the organism’s action within the immediate environment, insofar as the

covariance of place cell activity with organismal location and trajectory is sensitive to the

action the organism, embedding place cell activity in the broader system of brain-body-

world.

However, it is irrevocably clear that a (if not the) central component of place cell

activity (and the hippocampus more broadly) is the role it plays in encoding memory,

 

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whether spatial, episodic, or semantic (Eichenbaum 2013; Buzáki and Moser 2013).

Memory in this context can be regarded as the brain’s capacity to endogenously conjure

internal states or processes in the absence of the stimuli with which they were covariant

and, as such, memories constitute representations. Indeed, the primary logic for

describing place cells as internal representations is the function they serve as memory

encoders. During and after the process of forming place fields through active

locomotion, the connections between co-active or consecutively active place cells can

strengthen or weaken (by means of Hebbian plasticity) such that ensemble activity can

become coordinated, both with respect to the environmental context as a whole, as well as

the possible trajectories within that context (Wills et al. 2005; Jeffrey 2011). These

precisely encoded memories enable place cell ensembles to “self-generate temporally

evolving cell assembly sequences” that are rooted in prior experience, but occur in the

absence of exterior stimuli (Buzáki and Moser 2013, 130).

Thus, despite the fact that place cell firing fields are thoroughly dependent upon the

active exploration of the organism, the formation of clear firing fields provides the

organism with a memory-embellished spatial awareness that opens more precise and

efficient means of planning and taking action within the environment, as well as enabling

the organism to remember an environment in the absence of exterior stimuli. In other

words, to invoke a now-familiar conceptual apparatus, the relationship between action

and place cells is cyclical, or non-linear—action enables the formation of stable place

fields (perception), which in turn orients and enables the organism’s further action with

regard to where it has been and where it can continue to move and act. The co-

implication of action and perception is, as we have come to seen, a central pillar of the

 

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framework of ecological embodiment, and it is clear that place cell phenomena helps to

strengthen this pillar.

However, it is time to focus on the various ways that place cell ensembles do more

than simply help elucidate the organism’s immediate context by remaining sensitive to its

action. They can also enable the organism to deal with what is absent or covert, a

process that, as Andy Clark would put it, is “representation-hungry” (Clark 1999, 347).

In the context of place cells, this ability is most clearly manifest in the phenomena of

spatial navigation, or the ability to plan novel routes to previously experienced locations. In

the words of Godfrey-Smith, “the hypothesis that an animal has a ‘cognitive map’

requires, at a minimum, a capacity to devise novel detours and shortcuts in response to

obstruction of more familiar paths” (Godfrey-Smith 2002, 243). Historically, it has been

a fierce debate as to whether cognitive maps are deployed in the process of spatial

navigation. For example, some behaviorists have argued that the ability to find novel

shortcuts does not require a cognitive map, but rather can arise through mechanisms of

landmark-recognition and/or path integration (Bennett 1996).

Based on what has been described thus far, it is clear that place cells are candidates

for these latter methods for navigation, but this does not necessarily preclude the

capacity for place cells to serve further functions, and there is in fact experimental

evidence in which place cells do indeed operate on their established memories in the

processes of planning future paths (Pfeiffer et al. 2013). As a result, I hope to avoid the

debate between advocates of a behaviorist approach and advocates of internal

representation for fear of being tacked on to either party. Instead, I will focus on

essential aspects of place cell phenomena that move beyond the confines of behaviorism

while remaining within the framework of ecologically embodied cognition in order to

 

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elucidate processes of internal representation that are distinct from traditional accounts.

As a result, the rest of this section will describe two examples in which the organism

operates on memories encoded in place cells. Through these examples, place cells will

come to meet Bechtel’s tripartite criteria for representation while simultaneously

remaining within the framework of ecologically embodied cognition.

One way in which place cell memories support and enhance organismal action and

navigation is by helping to further embed the organism in its spatiotemporal context. Place

cells achieve this by timing their firing in relation to an oscillating frequency in the

hippocampus termed the theta rhythm. Large-scale brain synchronizations such as the

theta rhythm are rooted in the network activity of the neurons in a given brain region,

whose emergent field potential (the sum of the membrane potentials of individual cells)

graphed over time appears on an EEG graph as a sinuous oscillation occurring at a given

frequency (Hz). The synchronization of the hippocampal neuronal population in the

form of the theta rhythm enables the clustering or coordination of more localized

neuronal assemblies within the hippocampus, such as place cell ensembles. This

clustering occurs within individual cycles or ‘rotations’ of the theta wave (i.e., one

complete period of the theta oscillation), enabling the theta wave to serve as an

organizational ‘background’ for these smaller-scale assemblies: “the dual function of the

theta oscillation mechanism is to bring together and link cell assemblies into the

temporal range where they can be modified by synaptic plasticity, and at the same time

segregate them within the available phase space” (Buzsáki and Moser 2013, 134). In

other words, the cells in an assembly that fire within one cycle of the theta oscillation are

able to change and differentiate the strength of their connections based upon the

background field potential of the theta rhythm. This enables the cells to encode the

 

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specificities of the organism’s trajectory within an environment by allowing them to form

reliable patterns of sequential firing. The formation of these patterns of firing enables the

brain to plan ahead in the midst of the organism’s movement within its known

environment.

In order to fully comprehend this mechanism, it is necessary to understand that one

cycle of the theta oscillation is as brief as an instant. Thus, many of the cells that fire

within a theta cycle correlate not only with the organism’s current position, but also with

the organism’s past and future positions. In other words, place cell ensemble activity

within a theta cycle at a given spatiotemporal position and in the midst of a particular

trajectory relates the organism to where it has been, where it currently is, and the

possibilities for where it can continue to move: “the firing sequences of neurons on the

descending phase, trough, an ascending phase of the theta waves represent the sequences

of the past, current an future positions of the animal’s journey” (Buzsáki and Moser

2013, 134). Thus, the organism is embedded in place by remembering its past position

and projecting ahead of itself to those positions that are available within the

environment. This holistic awareness in each spatiotemporal position is perpetually re-

enacted within each cycle of the theta oscillation, such that the organism is always

already in the midst of an environment disclosed by its action and oriented prospectively

towards the continuation of this action in the context of the environment in which it is

navigating. Indeed, “during theta, place-cell activity seems to ‘sweep’ ahead of an animal

located at a choice point, leading to the hypothesis that such activity could support the

evaluation of alternatives during decision making” (Pfeiffer and Foster 2013, 74). Thus,

the experience-encoded place fields of the hippocampus enable the organism to be

constantly prospectively oriented with regard to its current position.

 

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Back in part one I put forth a refutation of Shapiro’s critique of Noë’s theory of

enactment, arguing that the perceptual sense of details within the environment depends

neither upon memory (Shapiro’s weak interpretation of Noë) nor the actual enactment

of sensorimotor contingencies (Shapiro’s strong interpretation of Noë). Instead, the

perceptual sense of details in the world comes from implicit knowledge about how past

actions have disclosed the world, as well as an expectation about the prospective

availability of the environment, or how it will continue to change in response to

sensorimotor activity. Notwithstanding the question of whether organisms such as rats

possess a ‘perceptual sense’ of objects (I have argued that they do not in the semantic

sense), the resonance between this phenomenological account and the firing of place

cells within a given theta cycle is striking, and, at the very least, offers a compelling

example of the neural-embodied underpinnings of such perceptual capacities. After all, if

in each phase of the theta cycle place cell activity correlates with where the organism has

and will continue to move within a known environment, it constantly maintains its

capacity to bind its action to landmarks within this environment. In short, this ensemble

activity allows for the coordination between the organism’s internal processes, its

locomotion, and the world.

Thus, it is clear that the memories encoded in place fields and the particular

sequences of firing within one theta cycle are constantly sensitive to action, but they also

broaden the organism’s spatial awareness beyond its immediate position enabling it to

plan ahead and navigate within the environment. Thus, while on the one hand these

temporally evolving place cell assemblies operate on the trajectory of the organism, on

the other hand, the organism’s trajectory operates on these theta-mediated cell

assemblies, particularly to the extent that they can reliably predict its future locations. It

 

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now seems place cells are beginning to look more like representations inasmuch as the

brain uses the reliable covariance of place fields with location semi-endogenously in order

to generate cell-assemblies that in turn influence action. However, the persistent

feedback or coupling between organismal action and assembly activity further highlights

the fundamental embeddedness of the semi-autonomous place cell networks within an

active organism, pointing towards a broader system in which the dynamics of brain,

body, and world are in constant interaction (Chiel and Beer 1997).

However, there are indeed cases when place cell networks become more thoroughly

autonomous and self-organizing. It has been observed in many cases that, when body

and environmental cues are held constant, self-generated place cell assembly activity

depicts possible paths that an organism can take within the environment, usually back to

a known location such as the organism’s home (Pfeiffer and Foster 2013). Thus, place

cell assemblies plan an organism’s future path in the absence of body-derived cues:

“During many candidate events [which are events of place cell assembly activity in the absence of motion], decoded position revealed temporally compressed, two-dimensional trajectories across the environment […] Events depict the future trajectory to Home, indicative of a planning mechanism to guide behavior” (Pfeiffer and Foster 2013, 75).

The use of place cells in navigational planning exemplifies the capacity for an organism

to negotiate with what is not immediately present (i.e. is absent or covert). In other

words, the phenomenon of navigational planning meets the tripartite criteria for

representation.

And yet, the particular quality of these internal representations is thoroughly

indebted to the organism’s embodied activity. This is because the navigational planning

exhibited by place cells is fundamentally an example of simulated acting, and is thus a

phenomenon that is dependent upon the experience of actual action for its existence and

 

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efficacy. One of the primary critiques of embodied approaches to cognitive science is

that it is unable to account for ‘off-line’ reasoning, or coping with the absent, because

one of the central tenets of the framework, as we have seen, is the constant coupling

between internal processes and the world itself. However, as Andy Clark observes,

“One promising advance is the suggestion that embodied cognitive science might treat off-line reason as something like simulated sensing and acting, thus preserving the special flavor of embodied problem solving alongside a high degree of ability to decouple from the environment” (Clark 1999, 347).

In order to demonstrate precisely what this means, Clark draws from an example in

AI from the lab of Lynn Stein. In order to negotiate the immediate environment, Stein’s

robot, TOTO, uses sonar technology (think back to the echolocation example) to detect

physical properties of an environment and generate a map of the environment. Much

like place cells then, these

“inner mechanisms […] record landmarks as a combination of robotic motion and sonar readings, so that a corridor might be encoded as a combination of forward motion and a sequence of short, lateral sonar readings” (Clark 1999, 347).

In other words, the inner map of the environment is a type of path integrator that

encodes how movements of the robot correlate with the aspects of the surrounding

environment. TOTO is thus highly capable of acting within its known environment, but

incapable of navigating to novel places.

In order to achieve this next level of cognitive capacity, Stein constructed another

robot, METATOTO, which builds on the fundamental architecture of TOTO in order

to navigate to novel locations. The importance of METATOTO is that it uses the same

systems of TOTO in order to simulate action in an environment it has not experienced:

“METATOTO works by simulating both sensors and actuator […These] simulation

runs create the kinds of feedback that would be received from the actual world” (Clark

1999, 347). Representation-hungry behaviors such as coping with the covert are thus

 

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secondary properties that evolve out of the mechanisms of embodied action, which is

made evident by the example of place cells. Place cell assemblies that are active when the

organism is active possess a capacity to resonate and re-activate endogenously, as well as

form into novel sequences of firing in the process of navigational planning:

“Assembly sequences in the hippocampus can be generated by two different but possibly interacting mechanisms, driven, respectively by external inputs and internal self-organization. Self-organized cell assembly sequences disengaged from the environment or body-derived inputs, may support mental travel” (Buzsáki and Moser 2013, 134).

This clarifies that it is not only representational processes such as navigational

planning, but also memory more broadly that is rooted in embodied action. This is

because memory itself often occurs as a re-simulation of experience by means of the

sequential firing of neurons that were covariant with experience. To give an example,

let’s return to the firing of cell assemblies within phases of the theta oscillation. One

byproduct of this process, indeed one of its essential functions, is to encode and

establish linear sequences of cellular firing by modifying the strength of synaptic

connections in a spatiotemporally contingent mater. This causes the relationship between

proximal cells in the firing sequence to be asymmetrical, such that “forward associations

are stronger than backward associations” (Buzsáki and Moser 2013, 133). Thus, when

memories that are dependent upon the connections that were formed during experience

are recalled internally, they tend to occur in the linear direction, if not the precise

sequence, with which they were encoded. As children, we all learned our ABCs by singing

a song, and placing letter blocks in a particular sequence. Have you ever tried to say the

ABCs backwards? Or, to use another example, in order to remember song lyrics in the

middle of a chorus that happen to be slipping our mind, we tend to start at the beginning

of the chorus and sing (whether literal or simulated singing) in order to cue our memory

 

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of the lyrics by placing them in the sequence within which they belong. It is clear that

our memories, which enable us to deal with the absent, are dependent upon our re-

simulation or re-enactment of past experience, not a static internal model of that

experience.

There is one final detail to note with regard to memory and representation as the

neuronal (re)-simulation of embodied experience. Pfeiffer and Foster, whose experiment

demonstrated the mechanism of navigational planning by neuronal simulation, take

caution to note that “theta power, which is high during exploration, was significantly

decreased immediately before and after [navigational simulation]” (Pfeiffer and Foster

2013, 75). Other experiments have observed that theta oscillation is active only during

exploration, but not during recall or simulation (Buzsáki and Draguhn 2004; Buzsáki and

Moser 2013). Thus, although simulation events possess a vague qualitative similarity to

actual action, the neurons through which simulations are enacted do not benefit from

the precise modulations of connectivity enabled by the theta oscillation. Of course, these

simulation and recall events do alter the connectivity between the neural substrates to

some extent, but it is important to note that they are not encoded as experiences.

Instead, they modify specific sequential connections that have already been formed

through theta-mediated encoding and thus serve to consolidate actual experiences and

tentatively plan possibilities for action by utilizing action-encoded connectivity to self-

generate sequences of firing. This further indicates the primacy of action in the

functioning of higher-level representations.

Thus, to conclude, this section has made significant modifications to the framework

of ecological embodiment. As opposed to expressing hostility to representation or an

inability to account for cognitive behaviors that necessitate internal processes of

 

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representation, place cells have enabled the framework of ecologically embodied

cognition to confer a transformation of the concept of representation. If neurons are

indeed the substrate for higher level cognitive functions and yet they evolved first to

coordinate organismal embodied action, then the higher level cognitive functions such as

internal representation that are exhibited by organisms must have evolved out of and be

dependent upon the processes of embodied action: “The neuronal mechanisms that

evolved to define spatial relationships among landmarks can also serve to embody

associations among objects, events, and other types of factual information” (Buzsáki and

Moser 2013, 131). For example, when you recall a concept from a book you’ve read and

want to return to the particular passage that articulates the concept, your foundational

memory is of the location of the passage on a particular page. Other evidence for

representations and memory as (re)-simulations of embodied experience within an

environment offers a deeply compelling testament to the logic of Buzsáki and Moser.

iii) Beyond Covariance: Self-organization and predictive processing The previous section introduced the concept of self-organized or endogenous brain

activity, exhibiting two examples—the semi-endogenous activity of cellular firing with

respect to the theta-cycle of an organism in a known environment, and the wholly

endogenous sequential firing of cells in the process of navigational planning. The

conclusion made was that while these (semi)-autonomous neural processes meet many of

the criteria for status as representations, they more deeply point towards the

indebtedness of representations to action, both in terms of their sensitivity to position

and trajectory on the one hand, and their simulation of the neural processes covariant

with action on the other.

 

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During endogenous neural activity, there are two reciprocal processes at work:

upward and downward causation (Thompson and Varela 2001). Upward causation refers

to the way in which the individual cells shape the activity of the emergent network, they

have a local to global effect, while downward causation refers to the way in which

network level events constrain the possibilities for activity at the level of individual

neurons (Thompson and Varela 2001; Jeffrey 2011; Varela et al., 2001). These emergent

networks “constrain or prescribe the behavior of the individual components, ‘enslaving’

them, as it were, so that they no longer have the same behavioral alternatives open to

them” (Thompson and Varela 2010, 421). To connect this concept to a previous point in

the exposition, this description of upward and downward causation account should

remind you of my description of part-whole relationships in symphonies.

It is at this point that I want to turn to a more focused account of downward

causation in place cell networks and its location within the framework of ecological

embodiment. Downward causation is significant because it enters into a reciprocal

relationship with the mechanisms of covariance, in which the organism’s action exerts a

bottom-up influence on the network activity of cells. By understanding how the brain

functions beyond covariance through mechanisms of downward causation, we will once

again come to achieve a more nuanced grasp of the role of the brain in ecological

embodiment:

“Given that the coupled dynamics of brain, body and environment exhibit self-organization and emergent processes at multiple levels, and that emergence involves both upward and downward causation, it seems legitimate to conjecture that downward causation occurs at multiple levels in these systems” (Thompson and Varela 2001, 421).

The brain is an energy-expensive organ. Thus, efficiency in its ability to learn

environments is paramount. We are already familiar with two ways in which this occurs:

 

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through embodied action and the neural reuse of place cells in the ensemble encoding of

multiple environments. Indeed, much time has been spent focusing on how action

influences shifting ensemble behavior. But another way the brain can maximize the

efficiency of learning is by predicting the activity that will emerge through the bottom-up

stimulation of embodied activity, allowing it to form powerful connections when

predictions match, learn from mistakes or false predictions, and finally, embrace

particular discrepancies as insignificant (the organism is a process of selecting relevant

stimuli): “Prediction-driven processing is processing that is driven by an imperative to

reduce error in the brain’s own predictions concerning its current and future states”

(Clark 2012, 759).

One of the prominent testimonies to predictive processing in place cells is the

existence of ‘attractor networks’ (Jeffrey 2011; Wills et al. 2005; Jezek et al. 2011). An

attractor network can be regarded as a global profile of ensemble activity, where the state

of the network determines the possibilities of activity for individual cells within the

network (i.e. a cell possesses a particular place field only as part of a broader attractor

network). One of the main supports for this hypotheses is that “experiments have

shown that place representations in [the hippocampus] tolerate small changes in the

configuration of the environment but switch to uncorrelated representations when

dissimilarities become larger” (Jezek et al. 2011, 246). The language of ‘representation’

here is synonymous with ensemble activity. Thus, this passage is describing experiments

in which there is a sudden and global shift in the place field locations of an ensemble of

place cells at a particular point during a gradual shift in environmental shape (Wills et al.

2005). Such a process indicates a lack of distinction between environments that are

sufficiently similar to match the top-down expectations of the attractor network. It is

 

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therefore hypothesized that attractor networks are the “existence of stable states […]

towards which the system gravitates when it is sufficiently close” (Jeffrey 2011, 1). Thus,

an attractor network integrates bottom-up activity with its top-down prediction in order to

configure a stable profile of ensemble activity that co-varies with an organism’s specific

environment (Varela et al. 2001; Jeffrey 2011).

It is important to note that there are two classes of attractor networks that can be

observed in hippocampal ensemble activity. The first is of the type just mentioned—a

‘discrete’ ensemble profile whose global activity equates with a particular environment

(Jeffrey 2011). The second type, a ‘continuous’ attractor, is the pattern of ensemble

activity at a given spatiotemporal position within an environment (Jeffrey 2011). This

type of attractor is most thoroughly exhibited by ensemble firing with respect to the

theta rhythm. Thus, while the former refers to the global pattern of cells whose activity is

possible within a given environment, the latter refers to the actual pattern activity at a given

moment. The latter is thus nested within the former. Some of the benefits of continuous

attractors have already been outlined in the context of theta-oscillations, but it is

important to demonstrate how their predictive processing increases the efficiency of

learning. By predicting the place fields that will be active in future positions, theta-cycle

ensemble activity is in a sense predicting the activity of the neurons in the populations

below it in ensuing moments (i.e. cells that input onto place cells based on body-derived

cues). When matches are made between these top-down and bottom-up expectations,

the synaptic modification (the learning) that occurs is more potent than would occur

from bottom-up stimulation alone: “to perceive the world […] is to meet incoming

driving sensory signals with matching top-down expectations” (Clark 2012, 762).

 

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But of course, the successful matching of top-down expectations with incoming

stimuli in continuous attractors depend upon the existence of stable place fields in the

discrete attractor network. That is, the neurons that are active within a single theta have

place fields that are determined by the discrete attractor that is active in the given

moment. Thus, it is now necessary understand how discrete attractors enable the rapid

learning of novel environments. Various experiments have demonstrated how global

ensembles of cells with stable place fields form in novel environments at rates that are so

rapid as to perhaps suggest a partial pre-configuring (O’Keefe 2006; Wilson and

McNaughton 1993). For example, “suppose that, rather than forming through the

storage of arbitrary events, the synaptic weight matrix was preconfigured in a manner

that implicitly defined a large-set of two-dimensional relationships” (McNaughton et

al.1996, 179). By possessing a vast bank of partially pre-configured cellular connectivity,

the hippocampus can depend upon pre-existing ‘reference frames’ that exist at the level

of a discrete attractor so as to expedite the process of learning in novel environments

(McNaughton et al. 1996).

This is beneficial for two connected reasons. When transitioning from a known

environment to a novel one, the organism can, on the one hand, switch reference frames

(discrete attractors) so as to decrease interference in the ensemble activity between the

two environments and thus increase distinction between the two environments. On the

other hand, by using a pre-existing reference frame, the brain expedites learning by

means of the top-down, bottom-up integration mechanisms in which the body plays a

central role. Now, while this prediction-based learning may appear to equate with some

form of a priori cognitive structure, it is important to note the ways that it is not.

 

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Contrary to serving as an alternative to embodied cognition, this prediction based, top-

down learning mechanism actually amplifies its efficacy:

“Embodiment and action fit very naturally within such a framework. Embodiment matters because embodied agents alter their own sensory input streams in ways that can drive faster and more successful prediction-based learning” (Clark 2012, 760).

Furthermore, it is posited that the particular discrete attractor (reference frame) that

is active in a given moment is itself constituted by the organism’s motion; that is, both

the cellular content of the reference frame as well as which reference frame is active in an

environment derives primarily from ideothetic information, which is to say, from bodily

cues (McNaughton et al. 1996). Thus, upon entering a novel environment, the existence

of a pre-existing reference frame derived from mechanisms of path integration

(embodied activity) enables landmarks to be efficiently encoded through the integration

of incoming stimuli and pre-configured patterns of connectivity, resulting in a stable

discrete attractor network that is bound to that specific environment. Upon re-entering

this same environment, this particular discrete attractor becomes active and equips the

organism with a memory of this past location and promotes precise and efficient

learning to occur at the level of the continuous attractor. It does so by enabling

established place fields that fire with respect to the theta rhythm in the process of

embodied activity to potently alter their connections:

“Transient neural assemblies mediate the coordination of sensory and motor surfaces, and sensorimotor coupling with the environment constrains and modulates neural dynamics. It is this cycle that enables the organism to be a situated agent” (Thompson and Varela 2001, 424).

Neuronal assembly self-organization is indispensible to the efficacy of body in the

processes of learning, while simultaneously deriving from embodied activity, once again

pointing towards two-way causation occurs at many levels within the brain-body-world

system.

 

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By moving beyond covariance, this section has created a more nuanced

understanding of the brain as an independent subsystem while simultaneously observing

its fundamental embeddedness within the ecological agent, once again pointing towards

the system of brain-body-world as the relevant unit for understanding cognition. Gibson,

who was repeatedly criticized as providing an account of nothing more glorified

behaviorism, somewhat famously responded by arguing that the organism does not

simply respond to stimuli, but rather its brain ‘resonates’ with information in the process

of ecological exploration (Shapiro 2010). While ‘resonance’ is largely a metaphorical

term, I believe that these latter two case studies have offered a couple of relative

concretizations to this concept.

First of all, the stability of place fields and the encoding of particular paths of

locomotion in the organism’s memory are largely dependent on the capacity of place

cells to ‘re-play’ firing sequences during rest or sleep: “In replay, simultaneously recorded

populations of place cells show reactivation of temporal sequences reflecting prior

behavioral trajectories” (Pfeiffer and Foster 2013, 74). Thus, quite literally, the

information encoded in experience resonates in the brain; the brain is constantly echoing

the activity of its experience. Second of all, the predictive processing of the hippocampus

can be articulated as a self-tuning mechanism. By constantly seeking to match its

attractor activity to the flow of incoming stimuli, the brain is striving to minimize

dissonance between its predictive models and the incoming stimuli. In doing so, the

brain appears to be tuning itself to the resonant frequency of the environment. Thus,

“equipped with brains like ours we become porous to the world. Its structure and

statistical regularities flow through us in as real a way as do food and water” (Clark 2012,

 

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767). To me, it would appear as though resonance and porousness are deeply

homologous metaphors.

Concluding Remarks

I began this thesis with a negation of internal representations á la traditional

cognitive science and yet I concluded with an exposition of the centrality of the brain’s

internal processes for the organism’s ecologically embodied cognition. Thus, I want to

conclude by providing two overarching claims that vindicate this peculiar arc while at the

same time synthesizing some of the central tenets of my particular account of

ecologically embodied cognition.

1. At bottom, it’s the body

Traditional accounts of the mind posit internal representations as a starting point for

explaining cognition. The question that is asked is as follows: how does the mind (or

brain) use internal models to perform various cognitive acts, such as successfully

engaging with the exterior world? By framing the question this way, however, these

accounts are forced into explanations that ultimately depend upon the existence of internal

representations for their coherence. Thus, I sought to re-frame the question and ask the

following: how does the body provide the condition for the possibility of the mind, and

how does it determine and constrain its contents? In other words, I sought to

demonstrate how the environment that is perceived and the various possibilities and

concretizations of action within that environment could only be understood through the

particularities of the organism’s active body.

By showing how the enactment and perception of an environment is dependent

upon the locomotion of the organism, the particularities of the body were re-centered

 

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and shown to play a constitutive role in determining the particular way the environment

is disclosed. The discussion of affordances helped elucidate the unique couplings that the

organism’s body forms with the surrounding environment. Such couplings made it clear

that the organism is a process of ‘cutting together-apart’—the organism becomes

individuated in the context of the specific environment with which it is integrated

(Barad, personal communication). Furthermore, such couplings demonstrated the extent

to which it is impossible for action within the environment to derive from output signals

generated from a central processor. Instead, action is in need of constant sensitivity to

the organism’s body and a perpetual coordination between the organism’s internal

processes and the exterior world. Thus, in short, by reframing the question and using the

body as the foundation for understanding cognition, I sought to overcome the

‘homuncular problem,’ which is the practice of using later-evolved capacities in the

process of explaining the biological processes from which they evolved. Internal

representations do indeed exist, especially in human organisms, but using them as the

foundation for explaining action within an environment serves as a hollow foundation

because, at bottom, it’s the body that acts, and action emerged in evolution long before

internal representations.

2. Moving Upwards and Peering Back Down: A novel heuristic for neural processes

By indicating the body as the relevant unit for explaining various facets of cognition,

the brain was not forgotten. Instead, I sought to provide a novel entry point into

understanding neural processes. As a result, I began my exposition of place cell activity

by demonstrating the myriad ways that place cell phenomena are thoroughly indebted to

the organism’s embodied action and the details of the environment within which it is

situated. In other words, place cells and their respective place fields, which are rather

 

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ubiquitously regarded as internal representations, were demonstrated to emerge through

action inasmuch as they are covariant with the organism’s action within a particular

environment.

After establishing this entry point into understanding the foundations of place cell

activity, it became necessary to complicate and broaden the picture. Ultimately, the

extent to which the endogenous activity of place cells can serve as representations that

feedback on the action of the organism and enhance its ability to learn, discriminate

between, and navigate within environments offered a novel conception for how to

understand representations within the framework of ecologically embodied cognition. In

order to enable the organism to perform the cognitive acts of spatial navigation and

spatial learning, place cells represent the environment by simulating action, or

endogenously generating the sequences of cell activity that have and would co-vary with

the organism’s embodied action. And secondly, place cells enable the rapid learning of

environments by endogenously generating patterns of activity that intend to predict the

way in which the organism’s action will continue to alter this activity. This ultimately

provided another example of reciprocal coupling—between the brain’s internal network

processes and the incoming stimuli from the action of the organism’s body.

Ultimately, this re-instated the central claim that to thoroughly understand the mind,

it is necessary to embrace non-linear processes that are happening at many levels. And of

course, non-linearity does not equate with cycles of input and output through the brain

regarded as a central processor. This approach is endemic to the computational

assumptions of traditional cognitive science. Instead, the non-linearity exemplified by the

brain’s internal processes in the context of embodied action is such that respective poles

of the linear oppositions presupposed by traditional cognitive science come to carry

 

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within themselves the contents of their opposites—action is perception, perception is

action; mind is body, and body is mind. It was only through the body that the brain’s

internal processes of representation could be grasped as both indebted to action and

indispensible to it.

After repeatedly invoking the empty observation that the first neurons evolved to

coordinate action, it is my hope that this observation has been given substance in the

process of my exposition. Ultimately, the focus of this project has not been to offer an

exhaustive account of the bodily and neural contributions phenomena such as thought

or reflection, features we often equate with our ‘mind.’ Instead, by showing the centrality

of the body in cognitive action within an environment and, furthermore, the way in

which endogenous brain activity ultimately emerges from and is related two this

embodied activity, I hope to have pointed towards a valuable heuristic for inquiring into

the neural activity that underpins such phenomena. In short, I hope to have pushed the

field of cognitive science towards a more unified naturalism of mind.

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