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Li D., Christ S.E., Johnson J.D. and Cowan N. (2015) Attention and Memory. In: Arthur W. Toga, editor. Brain Mapping: An Encyclopedic Reference, vol. 3, pp.

275-279. Academic Press: Elsevier.

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Attention and MemoryD Li, Duke University, Durham, NC, USASE Christ, JD Johnson, and N Cowan, University of Missouri, Columbia, MO, USA

ã 2015 Elsevier Inc. All rights reserved.

Attention and memory are both established concepts in psy-

chology and have been extensively studied since the late nine-

teenth century (James, 1890). Attention refers to the process of

preparing for and selecting specific subsets of external stimuli

or internal representations stored in memory (Anderson,

2005). Memory refers to the encoding, storage, and retrieval

of information (Atkinson & Shiffrin, 1968).

Attention and memory are critical for everyday tasks. Ima-

gine the following scenario. You are in the airport to pick up

somebody that you met many years ago and only vaguely

remember his appearance. You were told that he is wearing a

blue jacket today. When the crowd of people comes out of the

exiting gate, you keep the ‘blue jacket’ representation in mind

and selectively attend only to those people wearing blue

jackets. Suddenly, a man wearing a red shirt waves to you,

capturing your attention. After checking other features of his

appearance, you recognize that this is the person you are wait-

ing to pick up. (It turns out that he forgot to put on his blue

jacket.) In this common scenario, attention helps you focus on

certain types of stimuli, such as voluntarily attending to people

wearing blue jackets and involuntarily attending to someone

waving at you. Memory helps you remember information that

is relevant to the current task, such as short-term memory

(STM) of the blue jacket and long-term memory (LTM) of the

appearance of your guest.

Both attention and memory have been conceptualized as

each comprising multiple components (Atkinson & Shiffrin,

1968; Knudsen, 2007; Posner & Petersen, 1990), some of

which are unique to attention or memory, with others inter-

acting across the two. Such interactions have been a particular

focus of research and have been investigated with behavioral,

neuropsychological, electrophysiological, and, more recently,

brain mapping methods (Awh, Vogel, & Oh, 2006; Chun &

Turk-Browne, 2007). This article provides a brief introduction

of these components of attention and memory as well as their

interactions in the context of brain mapping studies in the last

2 decades.

Attention

Posner and Peterson’s model of attention provides an influen-

tial framework for testing the structure and functions of atten-

tion (Petersen & Posner, 2012; Posner & Boies, 1971; Posner &

Petersen, 1990), though there are other perspectives (e.g.,

Knudsen, 2007). In the model of Posner and Peterson, atten-

tion is a cognitive module independent from processing sys-

tems that underlie stimulus processing, decision making, and

output production. Attention is further partitioned into three

distinct components: alerting, orienting, and executive control,

all of which have different functions and activate spatially

distinct brain networks (Posner & Petersen, 1990). These

Brain Mapping: An Encyclopedic Reference http://dx.doi.org/10.1016/B978-0-12-39

Brain Mapping: An Encyclopedic Refere

attentional networks have been extensively studied with brain

mapping methods over the past two decades (Petersen &

Posner, 2012; Raz & Buhle, 2006). Alerting refers to increased

and sustained arousal in preparation for an upcoming stimulus,

and it has not been directly associated with memory. There-

fore, this article focuses primarily on orienting and executive

control. Additional description and discussion of alerting may

be found elsewhere (Petersen & Posner, 2012).

Orienting

Orienting refers to the process of selecting items (or attributes

of an item) for further processing. One distinction that has

been made in the literature is between overt orienting and

covert orienting (Hunt & Kingstone, 2003). Overt orienting

refers to selectively attending to a stimulus by moving the

eyes to the stimulus, whereas covert orienting refers to selec-

tively attending to a stimulus without eye movement. In terms

of neural substrates, as would be anticipated, overt orienting

engages primary motor cortex and midbrain regions directly

responsible for eye movements (Pierrot-Deseilligny, Milea, &

Muri, 2004). Beyond that, however, there appears to be sub-

stantial overlap in the general network of cortical regions sup-

porting overt and covert orienting (Corbetta et al., 1998; Haan,

Morgan, & Rorden, 2008), although recent findings from ani-

mal studies suggest that substructures within these brain

regions in monkeys are differentially recruited during overt

and covert orienting (Schafer & Moore, 2007).

Another important distinction is between top-down

orienting and bottom-up orienting (Corbetta & Shulman,

2002). Top-down orienting is a goal-driven (voluntary) atten-

tional system and is engaged when people purposefully direct

attention to a subset or certain features of stimuli. An example

of top-down orienting in the airport scenario described earlier

would be the purposeful focus of attention on the subset of

people wearing blue jackets. Bottom-up orienting, on the other

hand, is a stimulus-driven (involuntary) system that is engaged

when a salient stimulus automatically captures attention. An

example of bottom-up orienting in the airport scenario would

be the involuntary capture of attention by someone waving at

you, even when that person might not be wearing a blue jacket.

Brain imaging studies have shown that top-down orienting

and bottom-up orienting are associated with two distinct cor-

tical networks, often referred to as the dorsal and ventral

attentional networks (Corbetta & Shulman, 2002). Top-down

orienting recruits a dorsal network consisting of the frontal eye

fields and the superior parietal cortex, extending into the intra-

parietal sulcus. Bottom-up orienting recruits a ventral network

consisting of the ventrolateral frontal cortex and the ventral

parietal cortex (VPC) (in the vicinity of the temporoparietal

junction).

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276 INTRODUCTION TO COGNITIVE NEUROSCIENCE | Attention and Memory

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Executive Control

Generally speaking, executive function refers to a set of higher-

order cognitive processes that allow for the flexible modifica-

tion of thought and behavior in response to changing cognitive

or environmental contexts. Within the context of attention,

executive control is particularly relevant as it relates to top-

down processes such as switching attention from one object

to another and determining which events to attend. Early brain

imaging studies of attention and executive control focused

primarily on the contribution of the anterior cingulate cortex

(Posner & Petersen, 1990), whereas later studies observed

associated effects in more general ‘executive control’ regions

such as the dorsolateral prefrontal cortex and also subcortical

regions such as the basal ganglia (Petersen & Posner, 2012). An

influential model grouped these brain regions into two neural

networks, each subserving a distinct aspect of executive control

(Dosenbach, Fair, Cohen, Schlaggar, & Petersen, 2008). The

‘frontoparietal’ network – including the dorsolateral prefrontal

cortex, posterior parietal cortex (PPC), precuneus, and middle

cingulate cortex – appears to provide control on a moment-by-

moment basis, adapting to slight changes in stimulus input.

This network often shows transient activations during the

onset of attentional tasks and the processing of individual

stimuli and their associated responses. The ‘cingulo-opercular’

network includes the dorsal anterior cingulate cortex, anterior

prefrontal cortex, anterior insula, and thalamus and has been

associated with the adoption of a sustained (stable) cognitive

set over relatively long task periods. Under this framework, the

frontoparietal and cingulo-opercular networks thus form an

integrated executive control system that monitors and regulates

human behavior.

Memory

Memory is usually divided into three types: sensory memory,

short-term (working) memory, and LTM (Atkinson & Shiffrin,

1968). Sensory memory refers to the temporary (usually less

than 1 s) activation of stimulus information immediately after

perception. Due to its seemingly unlimited capacity, sensory

memory is typically not associated with selective attention.

Therefore, this article focuses primarily on STM and LTM.

Additional description and discussion of sensory memory can

be found elsewhere (Bliss, Crane, Mansfield, & Townsend,

1966; Cowan, 1984; Darwin & Turvey, 1972; Sperling, 1960).

Working Memory

Working memory (WM) is the successor of an older concept,

STM, which denotes the temporary storage of a limited amount

of information, which can be used in completion of a cognitive

task (Atkinson & Shiffrin, 1968). WM differs from STM in

that it is said to involve the maintenance and manipulation

of a limited amount of information for a short period using

several separate storage and processing mechanisms together

(Baddeley, 1986; Baddeley & Hitch, 1974). In the airport sce-

nario, information that your guest is wearing a blue jacket must

be kept in WM while the search is ongoing.

Brain Mapping: An Encyclopedic Referen

An influential model proposed by Baddeley and colleagues

divided WM into an executive control system and two slave

systems: the ‘phonological loop’ and the ‘visuospatial

sketchpad’ (Baddeley, 1986). The two slave systems maintain

verbal and visuospatial information, respectively, and are

under the control of the executive control system, which can

help to manipulate the information. A fourth component, the

‘episodic buffer,’ was later proposed to bind information from

different domains (Baddeley, 2000). Brain imaging studies

conducted under Baddeley’s framework have dissociated the

neural correlates of WM for different sensory domains (Smith

& Jonides, 1999; Ungerleider, Courtney, & Haxby, 1998).

Baddeley (2003) concluded that verbal and visuospatial WM

is left- and right-lateralized, respectively. Verbal WM appears to

be stored in the left temporoparietal region and be rehearsed in

the left inferior frontal gyrus; visuospatial WM appears to be

stored in the right inferior parietal cortex and be rehearsed in

multiple frontal and parietal regions in the right hemisphere.

The master system, executive control, is closely associated with

the dorsolateral prefrontal cortex.

Cowan (1995) proposed an alternative model of WM that is

less modular than the Baddeley and Hitch model. It includes

two embedded levels. The first level comprises activated LTM

representations, whereas the second level is the focus of atten-

tion that acts on a subset of the activated LTM and has limited

capacity. This model does not assume a distinction between

verbal WM and visuospatial WM. Instead, stimuli from differ-

ent domains are maintained under the same mechanism. To

account for the greater interference between two verbal stimuli

or two spatial stimuli than between two stimuli of different

types, it was proposed that the amount of interference

depended on the amount of feature overlap. This view is sup-

ported by studies showing overlapping activations for visual

and verbal (Cowan et al., 2011; Majerus et al., 2010), verbal

and spatial (Chein, Moore, & Conway, 2011), and verbal and

tonal WM (Koelsch et al., 2009). For each sensory domain,

there appears to be a domain-general frontoparietal network

that directs attention to item-specific information stored in

posterior sensory regions during WM maintenance (Harrison

& Tong, 2009; Lewis-Peacock, Drysdale, Oberauer, & Postle,

2012; Riggall & Postle, 2012). This model too includes the

central executive and it remains to be seen if Cowan’s focus

of attention and Baddeley’s episodic buffer are different.

The neural mechanism of WM is still under extensive inves-

tigation, and experimental results obtained under different

frameworks of WM models need to be reconciled into an

integrated theory of WM.

Long-Term Memory

LTM is a system of vast capacity that comprises permanent

traces. LTM is commonly divided into explicit (declarative)

and implicit (nondeclarative) memory (Schacter & Tulving,

1994). Explicit memory can be further subdivided: episodic

memory refers to personal events that are associated with

specific times and locations, whereas semantic memory corre-

sponds to general facts and knowledge about the world (i.e.,

not tied to a specific time or location; Tulving, 1983). Implicit

memory, on the other hand, encompasses effects of prior

experience that are often not available to consciousness, such

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INTRODUCTION TO COGNITIVE NEUROSCIENCE | Attention and Memory 277

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as priming, habits, and skills (Roediger, 1990). This section

focuses on episodic memory, as it has been investigated most

often with respect to its relationship with both attentional

orienting and WM. An example of episodic memory in the

airport scenario is your memory for your guest’s appearance.

Episodic memory has been shown to recruit a hippocampal–

cortical memory network, which includes the hippocampus,

medial and lateral temporal lobes, lateral parietal cortex, and

ventromedial prefrontal cortex (Squire & Zola, 1998; Vincent

et al., 2006). Themedial temporal lobe cortex and hippocampus

are thought to support distinct functions regarding episodic

memory, although the exact nature of this distinction is a topic

of ongoing debate (Brown & Aggleton, 2001; Squire, Stark, &

Clark, 2004). The role of the hippocampus is widely accepted as

being critical for the encoding of new information into episodic

memory (Corkin, 2002; Scoville & Milner, 1957).

Intrinsic activity in the hippocampal–cortical memory net-

work has been shown to be negatively correlated with that in

the dorsal attentional network, indicating that these two net-

works are involved in complementary processes (Vincent et al.,

2006). Indeed, it has been argued that the hippocampal–

cortical memory network is involved in focusing attention on

internal representations stored in LTM, whereas the dorsal

attentional network is recruited when attention is focused on

external stimuli (Corbetta & Shulman, 2002). Interestingly, the

executive control networks in Posner and Peterson’s frame-

work (Dosenbach et al., 2008) seem to be spatially interposed

between the hippocampal–cortical and the dorsal attentional

networks in the frontal, parietal, and temporal lobes (Vincent,

Kahn, Snyder, Raichle, & Buckner, 2008). This result has led to

the hypothesis that the executive control system receives and

regulates information from these two networks, indicating a

close relationship between attention-based processing and

memory-based processing.

Interactions between Attention and Memory

Attention and memory have close interactions (Awh et al.,

2006; Chun & Turk-Browne, 2007). Brain imaging studies

have been primarily focused on the interactions between atten-

tional orienting and WM/episodic memory.

Orienting and WM

Attentional orienting and WM interact in multiple ways. First,

orienting is thought to act as a ‘gatekeeper’ for encoding infor-

mation into WM by directing attention to task-relevant stimuli

and filtering out distractors. Some studies found that the ability

to filter out irrelevant information is associated with WM capac-

ity (Lee et al., 2010; McNab & Klingberg, 2008). These studies

also suggest that the lateral frontal cortex and basal ganglia

appear to be critical regions in controlling access to WM.

Second, items kept in WM can influence attentional orient-

ing. This interaction is usually investigated with a dual-task

paradigm in which an orienting task accompanies a WMmain-

tenance task. Results have shown that when the target of the

orienting task matches the item held in WM, performance on

the orienting task improves (Downing, 2000), suggesting that

top-down attentional orienting and WM maintenance share

Brain Mapping: An Encyclopedic Refere

some common processes. This postulate is further supported

by brain imaging studies in which top-down attentional and

spatial WM maintenance have been shown to activate a com-

mon set of brain regions, including the intraparietal sulcus and

the frontal eye fields (Awh et al., 2006; Corbetta, Kincade, &

Shulman, 2002). The behavioral and brain imaging results

both suggest that WM maintenance and top-down attentional

orienting may share common cognitive resource, which is

sometimes referred to as ‘the focus of attention’ (Cowan,

1995). It is likely that the focus of attention provides top-

down control over both orienting to external stimuli and

maintenance of internal representations in WM.

Orienting and LTM

The most studied interactions between attention and LTM are

those between attentional orienting and episodic memory

encoding/retrieval, which are reviewed in this section.

Orienting and episodic memory retrieval. Behavioral studies

have shown that a concurrent attentional orienting task

impairs episodic encoding but not retrieval (Baddeley, Lewis,

Eldridge, & Thomson, 1984; Craik, Govoni, Naveh-Benjamin,

& Anderson, 1996; Naveh-Benjamin, Craik, Guez, & Dori,

1998), suggesting that episodic retrieval is a largely automatic

process. However, a concurrent attentional task, although not

affecting accuracy, does impede reaction times at retrieval

(Baddeley et al., 1984). Therefore, the potential interactions

between orienting and episodic memory retrieval cannot be

overlooked.

Neuroimaging results of the interaction between orienting

and episodic retrieval were built on the fact that both tasks

activate dissociable regions in the PPC. Top-down attention

and bottom-up attention appear to recruit the dorsal parietal

cortex (DPC) and the VPC, respectively (Corbetta & Shulman,

2002). In the case of episodic retrieval, DPC is more often

activated in familiarity-based and low-confidence memory

judgments, whereas VPC is more often associated with

recollection-based and high-confidence retrieval (Cabeza,

Ciaramelli, Olson, & Moscovitch, 2008).

The dissociation between DPC and VPC in both attentional

orienting and episodic retrieval has spawned several interpre-

tations accounting for the role of PPC in both domains. One

influential model, the ‘attention to memory’ (AtoM) model

(Cabeza et al., 2008; Ciaramelli, Grady, & Moscovitch, 2008),

is based on a ‘dual attentional processes’ account in which DPC

and VPC have distinct functions not only on external stimuli as

stated in the attentional orienting literature (Corbetta & Shul-

man, 2002) but also on internal representations retrieved from

memory (Cabeza, 2008). In the AtoM model, DPC is involved

in the top-down allocation of attention to memory retrieval,

whereas VPC is involved in bottom-up capture of attention by

retrieved information. Thus, memory associated with few

details and low confidence requires greater top-down attention

and activates DPC, whereas memory with abundant details

and high confidence automatically captures attention and acti-

vates VPC.

One assumption of the AtoM model is that the DPC and

VPC regions overlap across attention and episodic retrieval

tasks. This assumption, however, is not supported by a recent

meta-analysis (Hutchinson, Uncapher, & Wagner, 2009).

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278 INTRODUCTION TO COGNITIVE NEUROSCIENCE | Attention and Memory

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Several other theories have been proposed to account for the role

of PPC in episodic retrieval (for review, see Wagner, Shannon,

Kahn, & Buckner, 2005). One popular account considers the

contribution of VPC to maintaining retrieved information in

WM (i.e., in the episodic buffer; Baddeley, 2000), which is

particularly relevant when memory decisions require the eval-

uation of information in service of responding (Vilberg &

Rugg, 2008).

Orienting and episodic memory encoding. Compared to episodic

retrieval, episodic encodingperformance seems tobemuchmore

affectedby a secondary attentional orienting task (Baddeley et al.,

1984; Naveh-Benjamin et al., 1998), which clearly suggests a

close interaction between orienting and episodic encoding. This

interaction has been investigated most often using the subse-

quentmemory paradigm, inwhich brain activity during episodic

encoding is classified (back-sorted) based on later retrieval per-

formance. The contrast of brain activity between successful

retrieval and forgetting is used to identify brain regions that are

involved in successful episodic encoding.

Brain imaging studies of subsequent memory effects have

revealed that successful encoding is associated with DPC acti-

vation as well as VPC deactivation (Uncapher, Hutchinson, &

Wagner, 2011; Uncapher & Wagner, 2009). These results are

consistent with the distinct roles of DPC and VPC in atten-

tional orienting: increased activation in DPC reflects stronger

top-down attention to task-relevant information at encoding,

whereas decreased activity in VPC reflects weaker involuntary

capture of attention by information that is salient, but not

beneficial to later retrieval success.

Open Questions

A number of questions remain unanswered in the fields of

attention and memory. In this section, we list a few of these

questions that can potentially benefit from brain imaging

research:

1. What is the unit of attentional orienting? In our initial

example, is the unit an object such as a jacket, a feature

such as the color blue, or the combination of both? Are the

units of WM and LTM the same as those of attentional

orienting?

2. What are the limits on WM capacity? Do individuals have a

limited number of slots to store items or, alternatively, an

unlimited number of slots but limited resources?

3. How are WM and LTM representations ‘stored’ in the cortex?

Are these representations localized to particular brain regions,

or are they distributed across multiple cortical regions?

4. Is attentional orienting domain-general, such that the same

cortical network may be used across sensory domains, or

domain-specific whereby distinct networks correspond to

different sensory domains? Do the same principles apply to

WM and LTM?

Summary

In the earlier text, we covered some of the most acknowledged

results in attention and memory, as well as their interactions,

Brain Mapping: An Encyclopedic Referen

although some other important findings are not included due

to the limited length of this article. For a long time period,

attention and memory have been investigated in independent

frameworks. The gap between these frameworks, however, is

becoming smaller and smaller thanks to results obtained from

brain imaging studies. As brain imaging techniques evolve, we

look forward to a more integrated conceptual framework of

attention and memory.

See also: INTRODUCTION TO COGNITIVE NEUROSCIENCE:Attentional Capacity and Limitations; Memory Attribution and CognitiveControl; Salience/Bottom-Up Attention; Short-Term Memory; TheMedial Temporal Lobe and Episodic Memory; WorkingMemory–Attention Interplay; INTRODUCTION TO SYSTEMS:Memory; Working Memory.

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