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This article was originally published in Brain Mapping: An Encyclopedic Reference, published by Elsevier, and the attached copy is provided by
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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.
Author's personal copy
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).
7025-1.00244-X 275nce, (2015), vol. 3, pp. 275-279
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
ce, (2015), vol. 3, pp. 275-279
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).
nce, (2015), vol. 3, pp. 275-279
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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