Thecognitiveneuroscienceofconstructionmemory.pdf

doi: 10.1098/rstb.2007.2087
, 773-786362 2007 Phil. Trans. R. Soc. B

Daniel L Schacter and Donna Rose Addis

remembering the past and imagining the future
The cognitive neuroscience of constructive memory:

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Phil. Trans. R. Soc. B (2007) 362, 773–786

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The cognitive neuroscience of constructive
memory: remembering the past

and imagining the future

Published online 29 March 2007
Daniel L. Schacter
1,2,* and Donna Rose Addis

1,2
One co
processe

* Autho
1
Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA

2
Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital,

149 Thirteenth Street, Suite 2301, Charlestown, MA 02129, USA

Episodic memory is widely conceived as a fundamentally constructive, rather than reproductive,
process that is prone to various kinds of errors and illusions. With a view towards examining the
functions served by a constructive episodic memory system, we consider recent neuropsychological
and neuroimaging studies indicating that some types of memory distortions reflect the operation of
adaptive processes. An important function of a constructive episodic memory is to allow individuals
to simulate or imagine future episodes, happenings and scenarios. Since the future is not an exact
repetition of the past, simulation of future episodes requires a system that can draw on the past in a
manner that flexibly extracts and recombines elements of previous experiences. Consistent with this
constructive episodic simulation hypothesis, we consider cognitive, neuropsychological and neuroima-
ging evidence showing that there is considerable overlap in the psychological and neural processes
involved in remembering the past and imagining the future.

Keywords: constructive memory; false recognition; mental simulation; neuroimaging; amnesia;
Alzheimer’s disease;
1. INTRODUCTION
The analysis of human memory comprises a variety of

approaches, conceptual frameworks, theoretical ideas

and empirical findings. Despite the wealth of contrast-

ing and sometimes conflicting ideas, there are some

basic observations on which memory researchers can

agree. One of the least controversial—but most

important—observations is that memory is not perfect.

Instead, memory is prone to various kinds of errors,

illusions and distortions. For instance, it has been

proposed that memory’s imperfections can be classified

into seven basic categories or ‘sins’ (Schacter 1999,

2001). Each of the memory sins has important

practical implications, ranging from annoying everyday

instances of absent-minded forgetting to misattribu-

tions and suggestibility that can distort eyewitness

identifications. But for memory researchers, such

imperfections are most important because they provide

critical evidence for the fundamental idea that memory

is not a literal reproduction of the past, but rather is a

constructive process in which bits and pieces of

information from various sources are pulled together;

memory errors are thought to reflect the operation of

specific components of this constructive process. This

characterization of memory dates at least to the

pioneering ideas of Bartlett (1932) and has been a

major influence in contemporary cognitive psychology

for nearly 40 years.
ntribution of 14 to a Discussion Meeting Issue ‘Mental
s in the human brain’.

r for correspondence ([email protected]).

773
The situation is rather different when we turn to
cognitive neuroscience approaches, which attempt to
elucidate the neural underpinnings of memory. Here,
sustained interest in constructive aspects of memory has
developed only more recently. Such interest has been
driven mainly by observations concerning the memory
distortion known as confabulation, in which patients with
damage to various regions within prefrontal cortex and
related regions produce vivid but highly inaccurate
‘recollections’ of events that never happened (e.g.
Johnson 1991; Moscovitch 1995; Burgess & Shallice
1996; Dalla Barba et al. 1999; Schnider 2003; Moulin
et al. 2005). During the past decade, investigations of
memory distortions in other patient populations, as well
as neuroimaging studies of accurate versus inaccurate
remembering in healthy individuals, have contributed to
an increase in research on the cognitive neuroscience of
constructive memory (for reviews, see Schacter et al.
1998a; Schacter & Slotnick 2004).

In the present paper, we focus on episodic memory,
the system that enables people to recollect past
experiences ( Tulving 1983, 2002). We consider some
recent work concerning the neural basis of memory
construction with a view to addressing a question
concerning its function: why does memory involve a
constructive process of piecing together bits and pieces
of information, rather than something more akin to a
replay of the past? Several researchers have grappled
with this issue and proposed various reasons why
human memory, in contrast to video rec s or
computers, does not store and retrieve exact replicas of
experience (e.g. Bjork & Bjork 1988; Anderson &
Schooler 1991; Schacter 1999, 2001). We focus on one
This journal is q 2007 The Royal Society

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774 D. L. Schacter & D. R. Addis Constructive memory in the human brain

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hypothesis concerning the origins of a constructive
episodic memory: that an important function of this
type of memory is to allow individuals to simulate or
imagine future episodes, happenings and scenarios.
As we discuss later, a number of investigators have
recently articulated a broad view of memory that not
only considers the ability of individuals to re-experience
past events, but also focuses on the capacity to
imagine, simulate or pre-experience episodes in the
future ( Tulving 1983, 2002, 2005; Suddendorf &
Corballis 1997; Atance & O’Neill 2001, 2005;
Klein & Loftus 2002; Suddendorf & Busby 2003,
2005; D’Argembeau & Van der Linden 2004; Dudai &
Carruthers 2005; Hancock 2005; Buckner & Carroll
2007; Schacter & Addis 2007). This latter ability has
been referred to by such terms as prospection (Gilbert
2006; Buckner & Carroll 2007) and episodic future
thinking (Atance & O’Neill 2001, 2005). Since the
future is not an exact repetition of the past, simulation
of future episodes may require a system that can draw
on the past in a manner that flexibly extracts and
recombines elements of previous experiences—a con-
structive rather than a reproductive system. If this idea
has merit, then there should be considerable overlap in
the psychological and neural processes involved in
remembering the past and imagining the future. We
consider some recent cognitive, neuropsychological
and neuroimaging evidence that is consistent with
this hypothesis.
2. CONSTRUCTIVE MEMORY: FROM COGNITIVE
PSYCHOLOGY TO COGNITIVE NEUROSCIENCE
Any discussion of constructive memory must acknowl-
edge the pioneering ideas of Bartlett (1932), who
rejected the notion that memory involves a passive
replay of a past experience via the awakening of a literal
copy of experience. Although Bartlett did not advocate
the extreme position sometimes ascribed to him that
memory is always inaccurate (Ost & Costall 2002), he
clearly rejected the importance of reproductive mem-
ory: ‘the first notion to get rid of is that memory is
primarily or literally reduplicative, or reproductive. In a
world of constantly changing environment, literal
recall is extraordinarily unimportant.if we consider
evidence rather than supposition, memory appears to
be far more decisively an affair of construction rather
than one of mere reproduction’ (Bartlett 1932,
pp. 204–205). Bartlett emphasized the dependence of
remembering on schemas, which he defined as ‘an
active organization of past reactions, or of past
experiences’ (p. 201). Though usually adaptive for
the organism, the fact that remembering relies heavily
on construction via a schema also has a downside:
‘condensation, elaboration and invention are common
features or ordinary remembering, and these all very
often involve the mingling of materials belonging
originally to different ‘schemata’’ (p. 205).

Bartlett’s (1932) ideas have influenced countless
modern attempts to conceive of memory as a
constructive rather than a reproductive process. For
example, Schacter et al. (1998a) described a ‘construc-
tive memory framework’ that links ideas about memory
construction from cognitive psychology with various
Phil. Trans. R. Soc. B (2007)
brain systems. Schacter et al. noted evidence supporting
the idea that representations of new experiences should
be conceptualized as patterns of features in which
different features represent different facets of encoded
experience, including outputs of perceptual systems
that analyse specific physical attributes of incoming
information and interpretation of these attributes by
conceptual or semantic systems analogous to Bartlett’s
schemas. In this view, constituent features of a memory
are distributed widely across different parts of the brain,
such that no single location contains a literal trace or
engram that corresponds to a specific experience (cf.
Squire et al. 2004; Thompson 2005). Retrieval of a past
experience involves a process of pattern completion
( Marr 1971; McClelland et al. 1995; Norman &
O’Reilly 2003), in which the rememberer pieces
together some subset of distributed features that
comprise a particular past experience, including
perceptual and conceptual/interpretive elements.

Since a constructive memory system is prone to
error, it must solve many problems to produce
sufficiently accurate representations of past experience.
For example, the disparate features that constitute an
episode must be linked or bound together at encoding;
failure to adequately bind together appropriate features
can result in the common phenomenon of source
memory failure, where people retrieve fragments of an
episode but do not recollect, or misrecollect, how or
when the fragments were acquired, resulting in various
kinds of memory illusions and distortions (e.g. Johnson
et al. 1993; Schacter 1999). Furthermore, bound
episodes must be kept separate from one another in
memory: if episodes overlap extensively with one
another, individuals may recall the general similarities
or gist (Brainerd & Reyna 2005) common to many
episodes, but fail to remember distinctive item-specific
information that distinguishes one episode from
another, resulting in the kinds of gist-based distortions
that Bartlett (1932) and many others have reported.
Similarly, retrieval cues can potentially match stored
experiences other than the sought-after episode, thus
resulting in inaccurate memories that blend elements of
different experiences (McClelland 1995), so retrieval
often involves a preliminary stage in which the
rememberer forms a more refined description of the
characteristics of the episode to be retrieved (Burgess &
Shallice 1996; Norman & Schacter 1996). Breakdowns
in this process of formulating a retrieval description as a
result of damage to the frontal cortex and other regions
can sometimes produce striking memory errors,
including confabulations regarding events that never
happened (e.g. Burgess & Shallice 1996; Dab et al.
1999; Ciaramelli et al. 2006; Gilboa et al. 2006).

During the past decade, research in cognitive
neuroscience has made use of neuroimaging and
neuropsychological approaches to address questions
concerning memory errors and distortions that bear on
constructive aspects of memory (for a review, see
Schacter & Slotnick 2004). We do not attempt an
exhaustive review here, but instead focus on two lines
of research that are most relevant to our broader claims
regarding a possible functional basis for constructive
aspects of memory. First, we will consider research
concerning false recognition in patients with memory

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reduced false recognition in dementia and amnesia

0.7

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0.2

0.1
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pr
op

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recognition accuracy related false alarms

controls
older adults
AD patients
amnesics

Figure 1. Performance of patients with amnesia and Alzheimer’s disease on the Deese–Roediger–McDermott ( DRM) paradigm
( Roediger & McDermott 1995). Participants study lists of words (e.g. tired, bed, awake, rest, dream, night, etc.) that are related to
a non-presented lure word (e.g. sleep). A subsequent old–new recognition test contains studied words (e.g. tired, dream), new
words that are unrelated to the study list items (e.g. butter) and new words that are related to the study list items (e.g. sleep). Both
patient groups show significantly reduced recognition accuracy (i.e. hits—false alarms to new unrelated words) and also make
fewer related false alarms (i.e. false alarms to new related words—false alarms to new unrelated words) relative to age-matched
controls. Note that the ‘controls’ were the age-matched control group for the amnesic patients (data for controls and amnesics
are obtained from Schacter et al. 1996c) and the ‘older adults’ were the age-matched control group for Alzheimer’s patients (data
for older adults and Alzheimer’s patients are obtained from Budson et al. 2000). AD, Alzheimer’s disease.

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dis s that provides evidence indicating that false
recognition – rather than reflecting the operation of a
malfunctioning or flawed memory system – is some-
times a marker of a healthy memory system, such that
damage to the system can reduce, rather than increase,
the incidence of this memory error. Second, we
consider neuroimaging studies that provide insight
into the extent to which accurate and inaccurate
memories depend on the same underlying brain
regions. A growing body of evidence indicates that
there is indeed extensive overlap in the brain regions
that support true and false memories, at least when
false memories are based on what we refer to as general
similarity or gist information.
3. FALSE RECOGNITION IN AMNESIA
AND DEMENTIA
As noted earlier, patients with damage to regions of
prefrontal cortex and related brain areas sometimes
exhibit the memory distortion known as confabulation.
Such patients also sometimes show pathological levels
of false recognition, claiming incorrectly that novel
information is familiar (e.g. Delbecq-Derouesné et al.
1990; Schacter et al. 1996a; Ward et al. 1999). The fact
that brain damage can increase the incidence of memory
distortion leads naturally to the view that recollective
errors reflect the operation of a diseased or malfunction-
ing system. By contrast, however, two related lines of
research that have emerged during the past decade
indicate that some types of memory distortion reflect the
adaptive operation of a healthy memory system. These
studies of amnesic and demented patients have
examined the incidence of robust false recognition
effects, in which healthy people exhibit high levels of
false alarms after studying a series of semantically
or perceptually related words or pictures. For example,
in the Deese–Roediger–McDermott (DRM) paradigm
(Deese 1959; Roediger & McDermott 1995), parti-
cipants study lists of words (e.g. tired, bed, awake, rest,
dream, night, blanket, doze, slumber, snore, pillow, peace,
yawn and drowsy) that are related to a non-presented lure
Phil. Trans. R. Soc. B (2007)
word (e.g. sleep). On a subsequent old–new recognition
test containing studied words (e.g. tired and dream), new
words that are unrelated to the study list items (e.g.
butter) and new words that are related to the study list
items (e.g. sleep), participants frequently claim that they
previously studied the related lure words. In many
instances, false recognition of the related lure words is
indistinguishable from the true recognition rate of
studied words (for review of numerous DRM studies,
see Gallo 2006).

A number of studies have consistently revealed that
amnesic patients with damage to the hippocampus and
related structures in the medial temporal lobe (MTL)
show significantly reduced false recognition of non-
studied lure words that are either semantically or
perceptually related to previously studied words
(figure 1; Schacter et al. 1996c, 1997, 1998b; Melo
et al. 1999; Ciaramelli et al. 2006). This false
recognition ‘deficit’ roughly parallels patients’ true
recognition deficit and occurs even though amnesics
typically show similar or even increased levels of false
recognition to unrelated lure words. Amnesics also
show reduced false recognition of non-studied visual
shapes that are perceptually similar to previously
presented shapes ( Koutstaal et al. 1999). Parallel
studies have been reported in patients with Alzheimer’s
disease (AD), who typically have neuropathology that
includes, but is not limited to, MTL regions. Like
amnesics, AD patients show reduced false recognition
of lure items that are either semantically or perceptually
related to previously studied items (Balota et al. 1999;
Budson et al. 2000, 2001, 2003).

One interpretation of this pattern of results is that
healthy controls form and retain a well-organized
representation of the semantic or perceptual gist of a
list of related study items. Related lures that match
semantic or perceptual features of this representation
are likely to be falsely recognized, while unrelated
words that do not match it are likely to be correctly
rejected. As a result of MTL damage, amnesic and AD
patients may form and retain only a weak or degraded
gist representation and thus make fewer false alarms to

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776 D. L. Schacter & D. R. Addis Constructive memory in the human brain

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semantic associates or perceptually similar items than
do controls. Support for this interpretation comes from
a study that used a modified version of the DRM
semantic associates procedure ( Verfaellie et al. 2002).
Participants were instructed to call ‘old’ any item that is
semantically related to the theme or gist of a previously
studied list, even if the item itself had not appeared on
the list. Evidence from the healthy controls suggests
that such a task provides a more direct probe of gist
information than a standard old/new recognition task
(Brainerd & Reyna 1998; Schacter et al. 2001).
Verfaellie et al. (2002) reported that even in this
meaning test, amnesic patients provided fewer ‘old’
responses to semantically related lure words than do
controls, thereby supporting the idea of a degraded gist
representation. Budson et al. (2006) reported similar
results in patients with AD, using a paradigm in which
participants studied categorized pictures and were
given a version of a ‘meaning test’ in which they were
instructed to respond ‘yes’, when either a studied or
non-studied picture came from a studied category.

In the foregoing studies, involving meaning tests,
participants were asked to remember explicitly aspects
of previously presented materials; it is well known that
both amnesic and AD patients exhibit deficits on
explicit memory tasks. Thus, it is conceivable that
patients do form and retain a normal gist represen-
tation, but do not express this information on explicit
tests. Since amnesic patients can show intact priming
effects on various implicit or indirect memory tasks (for
review, see Schacter et al. 2004), Verfaellie et al. (2005)
examined whether use of an implicit task might reveal
intact retention of gist information in amnesics. They
did so by having patients and controls study lists of
semantic associates (e.g. resort, sun, beach, parties, etc.)
that were all associated to a non-presented related lure
word (e.g. vacation). On the subsequent stem com-
pletion test, participants were provided three-letter
word beginnings that had multiple possible com-
pletions; some could be completed with previously
studied words (e.g. bea___) and some with related lures
(e.g. vac___). Previous research using a similar
paradigm with healthy subjects revealed the existence
of a ‘false priming’ effect: compared with a baseline
condition, participants were more likely to complete
stems of related lures with the lure item following study
of a list of semantic associates (not surprisingly,
priming was also observed for previously studied
words, e.g. McDermott 1997; McKone & Murphy
2000). Verfaellie et al. reported that amnesic patients
showed intact priming for previously studied words,
replicating earlier results, but showed no priming for
related lures. By contrast, controls showed significant
priming for both studied words and related lure words.

These results further strengthen the idea that
impaired false recognition of similar words and objects
in amnesic and AD patients reflects an impoverished or
diminished gist representation, while suggesting that
the deficit extends beyond the strict confines of
episodic memory. They also support the idea that this
type of memory error in control populations reflects the
normal operation of healthy adaptive memory pro-
cesses. This latter conclusion is also supported by the
results of functional neuroimaging studies.
Phil. Trans. R. Soc. B (2007)
4. NEUROIMAGING STUDIES OF TRUE
AND FALSE RECOGNITION
In a number of studies using positron emission
tomography (PET) and functional magnetic resonance
imaging (fMRI), subjects studied lists of DRM
semantic associates and were later scanned while
making judgements about old words, related lures
and unrelated lures. Consistent with the results from
amnesic and AD patients, these studies have revealed
significant and comparable levels of activation in the
MTL, including the hippocampus, during both true
and false recognition of related lures (e.g. Schacter et al.
1996b; Cabeza et al. 2001; for more detailed review, see
Schacter & Slotnick 2004).

More recent neuroimaging studies of gist-based
false recognition using paradigms other than the
DRM procedure have replicated and extended these
results. Slotnick & Schacter (2004) used a prototype
recognition paradigm in which the critical materials
were abstract, unfamiliar shapes; all shapes in the study
list were visually similar to a non-presented prototype
(figure 2). Participants made significantly more ‘old’
responses to studied shapes than to new related shapes
and also made significantly more ‘old’ responses to new
related shapes (i.e. prototypes) than to new unrelated
shapes. This latter result confirms the presence of a
false recognition effect that was presumably driven by
memory for the ‘perceptual gist’ of the studied
exemplars that resembled the prototype. Slotnick &
Schacter documented that a number of regions
previously implicated in true recognition, including
MTL, fusiform cortex, lateral parietal cortex and
multiple regions in dorsolateral and inferior prefrontal
cortex, showed significant and comparable levels of
activity during false recognition of new related shapes
and true recognition of studied shapes (figure 2).

Garoff-Eaton et al. (2006) also used abstract shapes
as target items in a slightly different experimental
paradigm that focused on the relationship between
processes underlying related and unrelated false recog-
nition. In both types of false recognition, subjects
respond ‘old’ to new items. However, in related false
recognition, semantic or perceptual overlap between the
new item and a previously studied item drives the false
recognition response, whereas the basis for ‘old’
response to unrelated items is unclear. Standard signal
detection models of memory typically do not distinguish
between related and unrelated false alarms: both are
seen to result from a single underlying process that
supports familiarity or memory strength sufficient to
surpass a subject’s criterion for saying ‘old’ (e.g. Miller &
Wolford 1999; Slotnick & Dodson 2005; but see,
Wixted & Stretch 2000). However, data from studies of
false recognition in amnesic patients reviewed earlier
point towards different mechanisms underlying related
and unrelated false recognition, because amnesics
typically show reduced related false recognition
compared with controls, together with either increased
or unchanged unrelated false recognition.

In the experiment by Garoff-Eaton et al. (2006),
subjects studied abstract shapes drawn from the same
set as those developed by Slotnick & Schacter (2004).
On a subsequent recognition test, they were presented
either with the same shape from the study list, a related

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BA 39/40

dorsal view coronal view

hippocampal responses

true recognition

false recognition

parietal
BA 7/39/40

prefrontal
BA 45/46/47
BA 8/9

true recognition (old hits > new CRs)
false recognition (related FAs > new CRs)
new CRs
conjunction of true and false recognition
((old hits and related FAs) > new CRs)

time

time

test phase

related

old

old

new

0 4 8 12 16

pe
rc

en
ta

ge
o

f
si

gn
al

c
ha

ng
e

0.2
0.1

0
– 0.1

regions active during both true and false recognition

paradigm
study

cortical responses

Figure 2. Neural regions engaged during both true and false recognition (adapted from Slotnick & Schacter 2004). A prototype
recognition paradigm was employed; all stimuli presented during study were abstract, unfamiliar shapes. During recognition
testing, participants made recognition judgements about old studied shapes, new prototypical shapes visually related to studied
shapes and new shapes unrelated to studied shapes. A number of regions previously implicated in true recognition, including
hippocampus, lateral parietal cortex, and dorsolateral and inferior prefrontal cortex, showed significant and comparable levels of
activity during false recognition of new related shapes (i.e. prototypes) and true recognition of studied shapes compared with
correct rejections of new unrelated shapes. The percentage of signal changed extracted from the left lateral parietal cortex is also
shown. BA, Brodmann area; CR, correct rejection; FA, false alarm.

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shape that was visually similar to one of the studied
shapes or a new unrelated shape. Participants were
instructed to respond ‘same’ when a test shape was
identical to a previously studied shape, ‘similar’ when a
new shape was visually similar to a previously studied
one and ‘new’ to unrelated novel shapes. Behavioural
data revealed significantly more ‘same’ responses (0.59)
to same shapes than to either new related or new
unrelated shapes, and significantly more ‘same’
responses to related (0.31) than to unrelated (0.20)
shapes. A conjunction analysis of the fMRI data that
assessed common neural activity during true recog-
nition (i.e. ‘same’/same) and related false recognition
(i.e. ‘same’/related new) compared with unrelated false
recognition (i.e. ‘same’/new) indicated significant
activity in a network of regions previously associated
with episodic remembering, including hippocampus/
MTL, several regions within prefrontal cortex, medial
and inferior parietal lobes and ventral temporal/
occipital regions. In striking contrast, a conjunction
analysis that assessed common activity during related
and unrelated false recognition, in comparison with true
recognition, showed no significant activity in any region.
When contrasting unrelated false recognition with true
recognition and related false recognition, significant
activity was observed in regions of left superior and
middle temporal gyri (BA 22/38), regions previously
associated with language processing. Unrelated false
recognition may have occurred when subjects mis-
takenly applied a verbal label generated …