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2010 19: 131Current Directions in Psychological ScienceCharan Ranganath

Binding Items and Contexts: The Cognitive Neuroscience of Episodic Memory  

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Binding Items and Contexts: The CognitiveNeuroscience of Episodic Memory

Charan Ranganath1

1Center for Neuroscience and Department of Psychology, University of California at Davis

AbstractIn order to remember a past event, the brain must not only encode the specific aspects of an event but also bind them in a mannerthat can later specify the spatiotemporal context in which event occurred. Here, I describe recent research aimed atcharacterizing the functional organization of two brain regions—the medial temporal lobes and the prefrontal cortex—thatallow us to accomplish this task. Converging evidence indicates that different regions of the medial temporal lobes may formrepresentations of items, contexts, and item-context bindings and that areas in the prefrontal cortex may implement working-memory control processes that allow us to build meaningful relationships between items that are encountered over time. Theresults are compatible with an emerging model that generates novel predictions at both the behavioral and neural levels.

Keywordslearning, memory, fMRI, medial, temporal, brain, recognition, perirhinal, hippocampus, parahippocampal, prefrontal

Episodic memory, the ability to remember a past event, is

central to every aspect of daily life. It allows us to

reexperience the past, stay oriented in the present, and plan for

the future (Tulving, 1985). Tragically, episodic memory is

affected by numerous neurological conditions (e.g, Alzhei-

mer’s Disease, fronto-temporal dementia, epilepsy, traumatic

brain injury) and psychiatric disorders (e.g., schizophrenia,

depression, posttraumatic stress disorder). For this reason,

understanding the functional organization of memory pro-

cesses and their neural substrates will be of importance to both

psychological science and society at large.

One question that is central to understanding episodic mem-

ory is how the brain solves the binding problem in memory. For

instance, I remember the first time I saw Star Wars—I was with

my parents in a drive-in movie theater and I ate Twinkies�.

For my brain to recover and reconstruct this information, I must

have formed a memory that could be distinguished from mem-

ories of other times I saw a movie in a drive-in, times that I ate

Twinkies, and times that I spent with my parents. In other

words, to form a useful episodic memory, one needs to process

the specific aspects of an event and bind them in a manner that

specifies the spatiotemporal context in which they were

encountered. This ability clearly depends on a large network

of brain regions, but here I will focus on progress we have made

in understanding two areas—the medial temporal lobes (MTL)

and the prefrontal cortex (PFC)—that facilitate the successful

formation and retrieval of episodic memories (Moscovitch,

2008; Ranganath, Minzenberg, & Ragland, 2008).

Medial Temporal Lobes and Binding of Itemsand Contexts

It is well established that regions in the MTL play a critical role

in episodic memory, and several researchers have proposed that

different subregions contribute to memory in different ways.

To understand this issue, it is helpful to consider the anatomical

organization of the MTL (Fig. 1). In general, information from

all over the cerebral cortex is conveyed to neocortical regions

that surround the hippocampus, and these projections are not

homogenous. Specifically, the perirhinal cortex, receives input

from neocortical areas that process information about the qua-

lities of objects (i.e., ‘‘what’’ information), whereas the para-

hippocampal cortex additionally receives input from areas

that process spatial (‘‘where’’) information. The perirhinal and

parahippocampal cortices project to the entorhinal cortex and

the ‘‘what’’ and ‘‘where’’ information converges within the

hippocampus (see Eichenbaum, Yonelinas, & Ranganath,

2007, for review). Extrapolating from these aspects of MTL

anatomy, Howard Eichenbaum, Andy Yonelinas, and

I (2007) proposed that the perirhinal cortex may represent

information about specific items (e.g., who and what), the para-

hippocampal cortex may represent information about the

Corresponding Author:

Charan Ranganath, Center for Neuroscience, 1544 Newton Ct., University of

California, Davis, Davis, CA 95618

E-mail: cranganath@ucdavis.edu

Current Directions in PsychologicalScience19(3) 131-137ª The Author(s) 2010Reprints and permission:sagepub.com/journalsPermissions.navDOI: 10.1177/0963721410368805http://cdps.sagepub.com

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context (e.g., where and when) in which these items were

encountered, and the hippocampus may process bound repre-

sentations of items in context (similar ideas have been indepen-

dently proposed by others, including Davachi, 2006, and Eacott

& Gaffan, 2005).

This ‘‘binding of items and contexts’’ (BIC) model (Diana,

Yonelinas, & Ranganath, 2007) was developed in part to

account for findings from studies on the roles of different MTL

subregions in recognition memory. Many theories agree that

one can recognize an item based on its familiarity and by recol-

lecting associated details about the context in which the item

was previously encountered. For example, when encountering

someone on the street, you might recognize the person based

on facial familiarity and by recollecting when and where you

had previously encountered the person. A basic prediction from

BIC and other frameworks (e.g., Aggleton & Brown, 1999;

Cohen & Eichenbaum, 1993) is that the hippocampus dispro-

portionately supports recollection of contextual information

associated with the item and that the perirhinal cortex may

be sufficient to support item recognition based on familiarity.

Consistent with this idea, patients with hippocampal damage

or dysfunction have disproportionate deficits on measures of

recollection, as compared with measures of familiarity (e.g.,

Vann et al., 2009). Converging evidence has come from results

showing that rats with hippocampal lesions have impaired

recollection but generally intact familiarity-based recognition

(Fortin, Wright, & Eichenbaum, 2004).

Results from functional magnetic resonance imaging

(fMRI) studies of recognition memory have been consistent

with lesion studies and have also revealed new insights. For

instance, in two studies (Davachi, Mitchell, & Wagner, 2003;

Ranganath, Yonelinas, et al., 2003), activity in the hippocam-

pus and in the parahippocampal cortex during encoding was

specifically predictive of whether participants could subse-

quently recollect information about the context in which an

item had been studied, but activity did not differentiate

between items recognized on the basis of familiarity and items

that were missed. In contrast, activity in the perirhinal cortex

was correlated with subsequent familiarity-based item recogni-

tion and not sensitive to recollection (see Fig. 2). Of course,

every measure of a memory process relies on specific assump-

tions that can be questioned, so it is important to determine

whether similar results have been observed in other fMRI stud-

ies using different measurement techniques, materials, etc. As

shown in Figure 2b, a recent review revealed that, across stud-

ies, activity in the hippocampus and parahippocampal cortex

during encoding or retrieval is generally increased during

processing of items that are recollected, as compared with

recognized items that are not recollected, and that activity in

these regions is generally insensitive to differences in the

familiarity of an item. In contrast, activity in the perirhinal cor-

tex is rarely observed in contrasts examining recollection of

items but is often related to familiarity. Thus, imaging results

suggest different roles for the perirhinal cortex versus the hip-

pocampus and parahippocampal cortex in item recognition.

In terms of the BIC model, these differences may be

explained in terms of the dynamics of activation of different

MTL subregions. Specifically, activation of a relevant item

representation in the perirhinal cortex may contribute to

familiarity-based recognition. Thus, perirhinal activity should

differ during processing of items that will be recognized

HippocampusItems in Context

Parahippocampal CxContext

Representations

Perirhinal CxItem Representations

VLPFCProcessing

Item-SpecificInformation

DLPFCProcessing

RelationshipsAmong Items

EntorhinalCortex

a

b

Fig. 1. Prefrontal and medial temporal lobe regions that contributeto episodic memory processing. Relative locations of the dorsolateralprefrontal cortex (DLPFC; light blue), ventrolateral prefrontal cortex(VLPFC; peach), perirhinal cortex (blue), parahippocampal cortex(green), and hippocampus (red) are shown on a rendering of a brainwith a cutaway to reveal the medial temporal lobes (a). Our currentmodel of how lateral prefrontal and medial temporal regions maycontribute to episodic memory is shown in the diagram (b). Theanatomical connections between each region are illustrated withblack lines and proposed roles of each region are shown in italicletters. For simplicity, the diagram presents only the most significantanatomical connections between these regions and omits otheranatomically connected regions that also may play a role in episodicmemory formation or retrieval.

132 Binding Items and Contexts: The Cognitive Neuroscience of Episodic Memory

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primarily on the basis of familiarity relative to items that will

be missed. Input to the hippocampus may trigger completion

of the activity pattern that occurred during the learning event

and lead to activation of the associated contextual representa-

tions in parahippocampal cortex networks. Finally, output from

parahippocampal cortex to neocortical regions would elicit the

reinstantiation of contextual information previously associated

with the item, thereby leading to recollection. Thus, hippocam-

pal and parahippocampal cortex activity should be increased

during processing of items that are recollected relative to items

that are recognized primarily on the basis of familiarity.

Squire, Wixted, and Clark (2007) objected to the conclusion

that medial temporal subregions differentially contribute to

recollection or familiarity due to the types of information they

receive. Instead, they argued that dissociations between MTL

subregions in fMRI studies could reflect relative differences

in sensitivity to strong versus weak memories. This hypothesis

was falsified, however, in a recent study in which we manipu-

lated the extent to which participants made memory decisions

based on item or context information (Diana, Yonelinas, &

Ranganath, 2009). In this experiment, participants were asked

to learn associations between a word and a background color,

either by encoding color as a feature of the item that they are

encoding (e.g., ‘‘The elephant is red because it is sunburned’’)

or as a contextual association (e.g., ‘‘The elephant stopped at

the red light’’). Behaviorally, we have found that if color was

encoded as a contextual association, then color memory was

supported primarily by recollection, but if color was encoded

as an item feature, memory decisions were also supported by

familiarity (Diana, Yonelinas, & Ranganath, 2008). In an fMRI

study using the same paradigm, we observed a qualitative dif-

ference in the involvement of different MTL subregions during

the retrieval test (Diana et al., 2009). Consistent with results

from previous imaging studies, we found that hippocampal and

parahippocampal activity was enhanced during color memory

decisions when participants indicated that their decisions were

based on recollected contextual details. In the perirhinal cortex,

however, activity was only correlated with successful color

memory if color was encoded as an item feature, and this was

true for recollection-based responses or familiarity-based

responses. Thus, the involvement of different MTL subregions

during memory retrieval relates to the kind of information that

is recovered, and this cannot be explained in terms of differen-

tial relationships between MRI signal and overall memory

strength (see Staresina & Davachi, 2008, for similar findings).

Another potential criticism of BIC and related models is that

some studies have shown that, after hippocampal damage,

memory for associations between items can sometimes be sup-

ported by extrahippocampal regions such as the perirhinal cor-

tex. How can this be reconciled with the idea that the perirhinal

cortex represents item information? One answer may be that

any two items could be processed as a single, larger configura-

tion. For instance, an association between ‘‘house’’ and ‘‘boat’’

could be remembered as the word ‘‘houseboat.’’ Interestingly,

even novel, unrelated pairings (‘‘motor’’ and ‘‘bear’’) can be

unitized into a single item (‘‘motorbear’’) by providing a novel

definition (‘‘a mechanized stuffed animal’’). We have found

that unitizing word pairs is associated with increased activation

in perirhinal cortex during encoding (Haskins, Yonelinas,

Quamme, & Ranganath, 2008) and with increased familiarity

at test (Quamme, Yonelinas, & Norman, 2007). We (Haskins,

et al., 2008) also found that memory for unitized pairings is dis-

rupted by changing the word order between study and test, as is

memory for real compound words (e.g., ‘‘houseboat’’ vs.

0

1

2

3

4

5

6

SourceIncorrect

SourceCorrect

-10

12

34

56

78

Recognition Confidence

BO

LD R

espo

nse

Am

plitu

de

BO

LD R

espo

nse

Am

plitu

de1 2 3 4 5 6

HippocampusPerirhinal Cortex

0

10

20

30

40

50

60

70

80

90

100

Recollection Familiarity

HippocampusPHcPRc

% R

epor

ted

a b

Fig. 2. Dissociable patterns of medial temporal lobe activity related to familiarity and recollection. Results from Ranganath, Yonelinas, et al.(2003; a) showing that activity (BOLD response amplitude) in the left perirhinal cortex during encoding of words was monotonically related tosubsequent familiarity-based recognition (left), whereas activity in the right hippocampus was correlated with subsequent recollection of thecolor (‘‘source’’) that was associated with each word (right). Bar graphs (b) illustrate the proportion of studies that reported neural correlatesof recollection (left) and familiarity (right) in different medial temporal lobe regions (Diana et al., 2007).

Ranganath 133

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‘‘boathouse’’). Our findings suggest that the same kinds of

perirhinal representations that support item recognition may

also be utilized to support recognition of novel associations

based on familiarity.

Although the BIC model makes predictions about the neural

mechanisms of recollection and familiarity, the model does not

necessarily suggest that the functions of any MTL region will

be rigidly tied to any particular state of awareness. Instead, the

model suggests that MTL subregions fundamentally differ in

terms of the types of information they receive and process

(Eichenbaum et al., 2007). Thus, different MTL subregions

may support the recovery of item and context information, but

other regions may be required in order to integrate recovered

information in a manner that can guide conscious behavior.

Some evidence for this idea has come from studies in which

eye movements were used to indirectly measure the expression

of relational memory (e.g., Ryan, Althoff, Whitlow, & Cohen,

2000). In one such study (Hannula & Ranganath, 2009),

participants were asked to learn a series of scene–face pairs and

were tested on these pairings while their eye movements were

monitored (Fig. 3a). One of the scenes was shown on each test

trial, and after a delay, a test display consisting of the scene and

three previously studied faces was shown. Participants tended

to disproportionately look at the face that was previously paired

with the scene, suggesting that eye movements were influenced

by the previously learned face–scene association. Hippocampal

activity during initial presentation of the scene was predictive

of the extent to which participants subsequently viewed the

correct face, even when they failed to explicitly recognize it

as the associate (Fig. 3b). Interestingly, activity in the lateral

Time (sec)

Scene Cue 3-Face Display Scene Cue 3-Face Display

Per

cent

Sig

nal C

hang

e

Per

cent

Sig

nal C

hang

e

–2

0.15

Disproportionate Match Trials

Scene Cue

Experimental Paradigm

Hippocampal Activity Predicts Eye-Movement-Based Memory Effects

Test TrialsStudy Trials

6500 ms

Delay

500 ms

+

3-Face Display

Disproportionate Mismatch TrialsIncorrect Trials: High ViewingIncorrect Trials: Low Viewing

0.10

0.05

0.00

–0.05

–0.10

–0.15

0.15

0.10

0.05

0.00

–0.05

–0.10

–0.150 2 4 6 8 10 12 14 16 18 –2 0 2 4 6 8 10 12 14 16 18

Time (sec)

R. Hippocampus

a

b

Fig. 3. Hippocampal activity predicting expression of relational memory through eye movements, even when recollection fails (Hannula &Ranganath, 2009). Participants studied a series of face-scene pairs (a), and on each test trial, they were cued with a previously studied scene(scene cue) and then asked to select the associated face (3-face display). A region in the left hippocampus is shown (b, left), for which activationwas related to expression of memory through eye movements. The middle graph in (b) shows that activation in this region was higher on trialsfor which participants spent more time looking at the associated face (disproportionate match) than on trials for which they spent more timeviewing another face (disproportionate mismatch). The graph to the right shows that, even on trials for which explicit memory decisions wereincorrect, hippocampal activity was higher on trials for which participants spent more time viewing the correct face.

134 Binding Items and Contexts: The Cognitive Neuroscience of Episodic Memory

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PFC was more closely correlated with response accuracy than it

was with eye movement measures of relational memory, and

correlations between activity in the PFC and hippocampus

were higher on correct trials than on incorrect trials. Thus, it

appears that the hippocampus provides a key ingredient for

conscious recollection, but that in order for recollection to

occur, other brain areas such as the PFC (see below) may also

need to be recruited (Moscovitch, 2008).

Prefrontal Cortex, Working Memory, andEpisodic Memory

When we remember a past event, the memory is often selective,

emphasizing certain aspects of the event at the expense of

other, unattended aspects. One reason why this happens is that,

in real-life situations, we actively control the flow of informa-

tion that we process based on our current goals. Numerous

studies have implicated regions of the PFC in the selection,

maintenance, and organization of goal-relevant information,

and neuroimaging studies have implicated the same

regions in episodic-memory encoding and retrieval

(Ranganath, Cohen, & Brozinsky, 2005; Ranganath, Johnson,

& D’Esposito, 2003).

Based on differences in anatomical connectivity and evi-

dence from lesion studies in monkeys, many researchers have

proposed functional distinctions between the dorsolateral

(Brodmann’s areas [BA] 9 and 46) and ventrolateral (BA

44, 45, and 47) PFC (see Fig. 1). In general, neuroimaging

studies of memory encoding have repeatedly shown that ven-

trolateral prefrontal activity is increased during successful, as

vlpfc

dlpfc

High-Confidence Correct

Time (sec) After Onset of Target Word

% S

igna

l Cha

nge

% S

igna

l Cha

nge

% S

igna

l Cha

nge

% S

igna

l Cha

nge

Time (sec) After Onset of Target Word

Time (sec) After Onset of Target Word Time (sec) After Onset of Target Word

RememberFamiliar or NewAll Other Responses

Fig. 4. Dorsolateral prefrontal cortex (DLPFC) activity during encoding as correlated with subsequent memory for associations betweenitems (Murray & Ranganath, 2007). In the left DLPFC (Brodmann’s area [BA] 46; top row), activity during encoding of word pairs was greaterfor pair associations that were subsequently remembered (black trace), as compared with pair associations that were later missed orrecognized with low confidence (gray trace). However, when trials were analyzed as a function of accurate recognition of the words in eachpair (right graph), no significant differences were observed between subsequently remembered items (black trace) and items that were eithersubsequently recognized on the basis of familiarity or missed (gray trace). Activity in ventrolateral PFC (VLPFC; BA 45/47; bottom row) wascorrelated with subsequent memory for pair associations and individual items.

Ranganath 135

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compared with unsuccessful, memory formation. This is gen-

erally consistent with the idea that ventrolateral prefrontal

regions implement control processes that select the relevant

features of items, thereby resulting in a distinctive memory

trace that will be more robust to interference (Paller &

Wagner, 2002).

In contrast, activity in dorsolateral prefrontal regions is not

usually correlated with successful encoding of specific items.

Instead, we believe that dorsolateral PFC activity may be

related to the processing of relationships between items. Con-

sistent with this idea, we and others have shown that dorsolat-

eral prefrontal activity during encoding predicts subsequent

memory specifically if participants are given encoding tasks

that encourage relational processing or retrieval tests that are

sensitive to memory for associations among items (see

Blumenfeld & Ranganath, 2007, for review). For instance,

Murray and Ranganath (2007) found that dorsolateral prefron-

tal activity was increased during relational encoding of word

pairs and that activity was correlated with subsequent recogni-

tion of the word-pair associations but not with recollection of

individual items (Fig. 4). More recent data from our lab (Blu-

menfeld, Parks, Yonelinas, & Ranganath, in press) has con-

firmed that dorsolateral prefrontal activity during encoding is

not simply reflective of effort, task difficulty, or elaborative

encoding, but rather is more specifically tied to the demand

to build relationships between items. This research might have

important implications for the understanding of memory defi-

cits in aging. Recent findings have suggested that aging is asso-

ciated with decreases in white-matter integrity and that these

changes are negatively correlated with the ability to activate the

dorsolateral PFC during both working- and episodic-memory

tasks (Nordahl et al., 2006).

Outstanding Questions and Areas for FutureResearch

Obviously, the processes that support episodic memory are

complex, and the ideas presented here represent a relatively

simple starting point for understanding the underlying neural

mechanisms of these processes. Nonetheless, we are moving

toward experimental investigations of the more complex

aspects of human episodic memory. For instance, a central

aspect of episodic memories is that they are tied to a specific

temporal context, and we are currently investigating how inter-

actions between the PFC and MTL might facilitate memory for

temporal context (see also Polyn & Kahana, 2008). In other

work, we are investigating whether what we have learned about

the PFC might be used to develop techniques to improve episo-

dic memory. Specifically, we are testing whether processes

supported by the dorsolateral PFC can be trained in order to

improve episodic memory (particularly in children or the

elderly). Given the importance of episodic memory for so many

of our daily activities, the answers to these questions might turn

out to be not only of theoretical interest but also of immense

practical significance.

Declaration of Conflicting Interests

The author declared that he has no conflicts of interest with respect to

their authorship or the publication of this article.

Funding

Our research is supported by National Institutes of Health Grants

R01MH067821 and R01MH83734.

Acknowledgments

The ideas presented here reflect a collaborative effort and I am

indebted to the contributions of Andy Yonelinas and to the former and

current students and postdocs whose research is presented here. In

addition, Howard Eichenbaum contributed significantly to the ideas

presented on the organization of the medial temporal lobes. Special

thanks to Elizabeth Chua for her helpful comments and suggestions

on an earlier draft of this manuscript. I apologize to my colleagues

whose work could not be cited here due to reference limits.

Recommended Reading

Davachi, L. (2006). (See References). A thoughtful review of human

fMRI studies of episodic memory encoding for readers who want

to learn more about the functional organization of the MTL.

Eichenbaum, H., Yonelinas, A.P., & Ranganath, C. (2007). (See

References). A synthesis of behavioral, fMRI, neurophysiological,

and lesion studies of recognition memory in humans, rodents, and

monkeys.

Mitchell, K.J., & Johnson, M.K. (2009). Source monitoring 15 years

later: What have we learned from fMRI about the neural mechan-

isms of source memory? Psychological Bulletin, 135, 638–677.

A beautifully written review of results from fMRI studies that have

revealed important insights into both the binding of item and con-

text information and the processes that act on this information in

order to make attributions about past experiences.

Rosler, F., Ranganath, C., Roder, B., & Kluwe, R.H. (Eds.). (2009).

Neuroimaging of Human Memory: Linking Cognitive Processes

to Neural Systems. Oxford, England: Oxford University Press. A

good introduction to functional imaging studies of human memory;

each chapter reviews a specific topic and discusses how the find-

ings pertain to theoretical questions in psychological science.

Polyn, S.M., & Kahana, M.J. (2008). (See References). An innovative

and highly accessible review of the neural mechanisms that support

memory for temporal context, integrating work from mathematical

models of temporal context memory and data from electrophysio-

logical recordings and FMRI studies.

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