MEMORY AND THE BRAIN

Morris Moscovitch
Introduction
Memory is central to our lives, from the mundane and trivial, such as
knowing where we put things down, to the social, such as remembering
who we've met and under what circumstances, to the deeply personal,
such as reliving significant experiences that define us. It provides us with
a sense of who we are and where we belong physically, socially, and
historically. It also orients us toward the future. By providing us with a
sense of time past and what transpired, memory allows us to anticipate
the future and plan for it. For these reasons, there are investigators who
believe that this type of personal memory, tied as it is to a sense of a
conscious self, is a uniquely human attribute, which Tulving1 calls
autonoetic consciousness. This latter is specific to humans. Rudiments of
it, however, may exist in non-human species, even insofar as to allow the
individual to reflect on the past and perhaps relive past experiences,
though tests have not yet been designed to allow us to question
non-humans about this aspect of their mental life. What suggests that
humans and non-humans may have certain types of memory in common
is not just our observation of animals whose behaviours resemble our
own, but the knowledge, gained through research, that humans and
non-humans have in common brain mechanisms associated with
memory. By studying memory from the view of brain function we may
gain an appreciation not only of the mechanisms that make memory
possible, but also of its variety. As we will learn, memory is not unitary,
but multifaceted, consisting of many types, each mediated by different
brain structures, concerned with different content, and with its own mode
of operation. Though inter-related, the memory functions mediated by
these different structures can nonetheless be dissociated one from the
other so that some types of memory remain preserved while others are
impaired. By studying neuropsychological disorders following brain
damage we can learn how memory is organized not just at a brain level,
but also at a psychological level and gain some insight into those
processes that make the mental life of each individual unique.

1
E. Tulving, Episodic Memory: from Mind to Brain, Annual Review of
Psychology 53 (2002): 1-25.

Morris Moscovitch

Neuropsychological investigations of memory and the brain began

with the study of amnesia and will serve as the topic of this essay.
Though insights into the neuropsychology of memory have been gained
from recent investigations which use neuroimaging techniques that allow
one to view the brain as it performs its memory functions, it is still the
disorders of memory following brain damage that provide a better sense
of the impact that memory loss has on the individual, and exactly which
aspects of memory can operate independently of one another. I will,
however, refer to some neuroimaging studies briefly as the occasion
demands.
The term amnesia, as a description of a clinical disorder, refers to a
loss of memory for personal experiences, public events, or information,
despite otherwise normal cognitive function. The cause of amnesia can
be either primarily organic, resulting from neurological conditions such as
stroke, tumor, infection, anoxia, and degenerative disorders such as
Alzheimer's disease, which affect brain structures implicated in memory;
or it can be primarily functional or psychogenic, resulting from some
traumatic psychological experience. Although psychogenic disorders are
fascinating and provide insights into the relation between emotion and
memory,2 my attention will focus exclusively on organic amnesia. The
following questions will be addressed: What are the characteristics of
amnesia? What structures are involved in forming memories (and whose
damage causes amnesia) and what function does each serve in the
process? Does amnesia affect recent and remote memories equally, and,
by implication, are memory structures involved only in memory formation
and shortly thereafter, or are they also implicated in retention and
retrieval over long intervals? Are all types of memory impaired in amnesia
or is amnesia selective, affecting only some types of memory and not
others? Finally, what implications does research on amnesia have for
research and theory on normal memory?
Characteristics of organic amnesia
The following are the typical symptoms of organic amnesia: old
memories and the sense of self or identity are preserved but the ability to
acquire new memories is severely impaired. Though capturing an

2
H. J. Markowitsch, Neuropsychology of Memory: System, Organic, and Psychic
Disorders, and Functional Imaging Correlates, in A. Yamadori, R. Kawashima. T.
Fujii, and K. Suzuki, Frontiers of Human Memory (Sendai, Japan: Tohoku
University Press, 2002), 305-315; M.D. Kopelman. Disorders of Memory, Brain 125
(2002): 2152-2190.

Memory and the Brain

essential truth about organic amnesia, this statement needs to be

qualified in important ways in the light of new research.
The scientific investigation of organic amnesia effectively began with
Korsakoff's 18893 description of its symptoms in people with organic brain
disorders at the turn of the century, during what Rozin called the "Golden
Age of Memory Research."4 Likewise, it can be said that the modern era
of neuropsychological research on memory and amnesia was ushered in
by Scoville and Milner's5 publication of a single case: H. M., a man in his
twenties, who became amnesic after his medial temporal lobes were
neuro-surgically removed bilaterally to control epilepsy which was not
responsive to drug treatment. Some aspects of the memory disorder
Korsakoff described are peculiar to a kind of amnesia that now bears his
name (amnesia related to vitaminCthiamineCdeficiency typically
associated with alcoholism), while others are common to all forms of
amnesia, including the one suffered by H.M. The symptoms are best
described by contrasting impaired abilities with preserved ones. They are
as follows:
(1) Memory is impaired for various types of material, which is why
the amnesia is often referred to as global, though as we shall see not all
memories are affected equally. Perception, intelligence, and other
cognitive functions are relatively preserved. Thus, amnesic people can
appear normal in conversation and in solving problems as long as they
do not have to refer to events in the recent past. They can play chess,
solve cross-word and jigsaw puzzles, comprehend complex instructions,
and reason logically. This impression is corroborated by their normal
performance on standard tests of intelligence; on the other hand, they are
impaired on standard tests of memory.
3
S. S. Korsakoff, Etudes mdico psychologique sur une forme du maladie de la
mmoire,. Revue Philosophique (1899) 28: 501-30. Translated and republished by
M. Victor and P. I. Yakovlev, Neurology 5 (1955): 394-406.

4
P. Rozin, The Psychobiological Approach to Human Memory, in R. Rozenzweig
and E . L. Bennett, eds., Neural Mechanisms of Learning and Memory
(Cambridge, MA: MIT Press, 1976).

5
W. B. Scoville and B. Milner, Loss of Recent Memory after Bilateral
Hippocampal Lesions, Journal of Neurology, Neurosurgery, and Psychiatry 20
(1957): 11-21.

Morris Moscovitch

(2) The memory function that is impaired is only long-term or

secondary memory, that memory which lasts long after the information
has been received and registered, such as remembering what happened
yesterday or even a few minutes ago; what is not impaired is short-term
or primary memory which is used to hold information briefly in mind, such
as a telephone number or address that one heard for the first time a few
seconds ago. Unaffected also is working memory,6 which is used to
operate on the information held in mind, such as remembering a short list
of groceries and re-ordering them according to produce and canned
goods. As an example, amnesic people have a normal digit span, which
refers to the number of digits one can repeat immediately in sequence,
typically 7 + or 2 (short-term memory), and even to a normal backward
digit span in which the digits must be recalled in reverse order (working
memory). They are impaired, however, at retaining and recalling even a
sub-span list of words after a short interval that is filled with distracting
activity, even if given ample opportunity to rehearse the material
beforehand. The reason for this is that they lack the neural mechanisms
for storing and retaining information in long-term memory. In a more
ordinary life example, amnesic people can remember sentences well
enough to respond to them, but cannot follow a conversation to the end if
reference is made to utterances that occurred at the beginning. The same
dissociation between long-and-short-term memory holds for all material,
including words, stories, complex visual patterns, faces, melodies, and
some aesthetic stimuli.7
(3) Long-term memory loss in amnesia is most noticeable for events
and information acquired after the onset of the disorder and into the
future as well as in the period immediately preceding it, but not for
information acquired long before that. That is, the individual will have an
anterograde amnesia that extends into the future but a retrograde
amnesia limited to the time preceding the onset of the disorder. Thus,
amnesic people have difficulty remembering what they learned or
experienced since the onset of the disorder, even their current address
and neighbourhood if they had moved to a new place, but they can

6
A. Baddeley, "Working Memory: Looking Back and Looking Forward," Nature
Reviews: Neuroscience 4 (2003): 829-839.

7
B. Kolb, I. Q. Whishaw, Fundamentals of Human Neuropscyhology,
4th edition (New York: W. H. Freeman, 1996). See also L. R. Squire and P.
Alvarez, Retrograde Amnesia and Memory Consolidation: A Neurobiological
Perspective, Current Opinion in Neurobiology 5 (1995): 169-77.

Memory and the Brain

remember their old home and neighbourhood, and some old experiences
and events.8 However, as we will see, retention of some types of old
memories, may be more selective and not as well-preserved as had once
been believed, whereas other types follow the general rule. This rule,
first espoused by Ribot (1882)9 holds that the old memories are retained
better than new ones and are more resilient in the face of brain damage
(see below).
(4) A distinction is made in amnesia between memories that are
recollected consciously or explicitly and those that are retrieved implicitly
without conscious awareness. Anterograde long-term memory loss in
amnesia applies only to information that can be recollected consciously,
i.e., to explicit memory. Acquisition, retention, and recovery of memory
without awareness is normal. For example, having studied a set of words
or pictures, amnesic patients perform poorly when their memory is tested
explicitly for recognition (e.g., which of the following items do you
recognize as having been presented to you?) or recall (e.g., tell me the
items you had studied). However, their memory for studied items, is
normal if they are tested implicitly by seeing how performance is altered
by the study experience without making any explicit reference to the
study episode. Thus, though they cannot recall or recognize the items
they studied, amnesic people will perceive them more quickly and
accurately than items they did not study, or complete them better when
they are degraded, such as by filling in the missing letters in a word or
completing the lines in a picture. Performance on these implicit tests of
memory by amnesics indicates that information about the studied items is
held in memory though they are not aware of that.10 My personal
experience in learning to type illustrates the dissociation between implicit
and explicit memory. I learned to type by trial and error instead of taking
lessons. When I began taking lessons, I noticed that although my typing
had improved a great deal, clearly indicating that I had learned where

8
B. Milner, Amnesia Following Operation on the Temporal Lobe, in C. W. M.
Whitty and O. L. Zangwill, eds., Amnesia. (London: Butterworth, 1966).

9
R. Ribot, Diseases of Memory (New York: Appleton, 1882).

10
D. L. Schacter and R.L. Buckner, Priming and the Brain, Neuron 20 (1998),
185-195.

Morris Moscovitch

specific keys were, I nevertheless discovered that I could not explicitly

recount where each (or for that matter any) key was. My implicit memory
of the location of the keys, demonstrated by my typing skills, was good,
but my explicit memory of them was very poor.
These characteristics will serve as the foundation for later discussion
of empirical and theoretical investigations of amnesia, normal memory,
and brain function. Indeed, research on amnesia, fascinating in its own
right, has had a powerful impact on memory research and theory,
especially since the landmark discovery of Scoville and Milner. This
research can be divided into two interacting streams: a functional neuroanatomical one, concerned with identifying the neuro-anatomical
substrates of memory and determining their precise function; and a
(neuro)psychological one, concerned with the implication that amnesia
has for understanding normal memory at a functional level. Each will now
be dealt with in turn.
Neuroanatomy of amnesia
Amnesia is caused by bilateral damage to structures in the limbic
system and to the adjacent cortex in the medial temporal lobes. These
regions, though inter-related, form two subsystems, one centered on the
hippocampus and the other on the peri-rhinal cortex which is adjacent to
the hippocampus. Each of them connects to separate regions in the
thalamus or diencephelon, a mid-line structure beneath the cortex.
The hippocampal formation, in the medial temporal lobes, is the
most prominent of the memory structures. It consists of the hippocampus
proper with its various subfields and regions, plus the dentate gyrus and
the subiculum. Communication between the hippocampus and neocortex
occurs through a series of relays. The hippocampus is connected directly
to the entorhinal cortex which in turn is connected to the
parahippocampal gyrus and peri-rhinal cortex which respectively project
bi-directionally, primarily to the temporal and parietal lobes of the
neocortex. There are also projections from the hippo-campus and
peri-rhinal cortex via the fornix and anterior cingulate to the mammillary
bodies and the dorsomedial nucleus of the thalamus, which are in the
diencephalon. The loop of medial temporal and diencephalic structures
constitutes the limbic system. The hippocampus is thus ideally situated to
collate information about the cognitive (neocortex) as well as the
emotional (limbic) state of the organism and bind that information into a
memory trace that codes for all aspects of a consciously-experienced
event.11
11
For reviews see J. P. Aggleton and M. W. Brown, Episodic Memory, Amnesia,

Memory and the Brain

Functions of the neuroanatomical substrates of memory

There is considerable debate about the role that each of the components
of the memory system have and how they interact with one another.
Korsakoff's amnesia is associated with damage to the diencephalon,
whereas amnesia caused by anoxia, encephalitis, and some
degenerative disorders such as Alzheimer's Disease are associated most
often with medial temporal lobe damage. Although close inspection
reveals differences in memory loss among the various conditions, some
have not been substantiated reliably and others could not be attributed
with certainty to differences associated with diencephalic and medial
temporal lobe damage, as opposed to damage to other structures that
often accompanies the various disorders. For example, it had been
proposed that the medial temporal lobes were necessary for
consolidation and retention of new information whereas the diencephalon
was needed only to register and encode new material. Investigators
claimed that people with amnesia caused by damage to the diencephelon
had difficulty acquiring information, but once acquired, they retained it
normally. Source investigators claim that people with medial temporal
damage, showed abnormally rapid forgetting, though other investigators
found no difference in forgetting rates between amnesic groups, or even
between them and controls.12
However, there is, general agreement that people with Korsakoff's,
but not medial temporal, amnesia showed a number of memory deficits in
addition to loss of memory for the content of an experienced event.
These included confabulation in which the person provides patently false
and often contradictory information without being aware that he or she is

and the Hippocampal-anterior Thalamic Axis, Behavioral and Brain Sciences 22

(1999): 425-89. N. J. Cohen and H. Eichenbaum, Memory, Amnesia and the
Hippocampal System (Cambridge, MA: MIT Press, 1993). N. J. Cohen and H.
Eichenbaum, The Hippocampus and Mechanisms of Declarative Mmemory,
Behavioural Brain Research 103 (1999): 123-33. J. O'Keefe, and L. Nadel, The
Hippocampus as a Cognitive Map (Oxford: Oxford University Press, 1978).

12
M. D. Kopelman, N. Stanhope and D. Kingsley, Retrograde Amnesia in
Patients with Diencephalic, Temporal Lobe, or Frontal Lesions, Neuropsychologia
37 (1999): 939-58. See also D. M. Freed, S. Corkin and N. J. Cohen, Forgetting
in H.M: A Second Look, Neuropsychologia 25 (1987): 461-72.

Morris Moscovitch

doing so, a kind of "honest lying".13 They also have poor memory for the
source and the temporal order of events, susceptibility to interference,
and poor meta-memory (knowledge about memory).14 These deficits, all
of which involve strategic aspects of memory, were shown to be related
more to dysfunction of the frontal lobes of the brain that often
accompanies Korsakoff's amnesia, than to diencepahlic damage per se.15
These studies indicated that there is a need to consider the contribution
of additional structures, such as the frontal lobes, to help organize
memories and to monitor and verify them. Recent functional
neuroimaging studies of memory in normal people have confirmed the
importance of frontal contributions to memory by showing that these
structures are active whenever memory is being used.16
Influenced by research on animal models of memory, investigators
focused on differences among the structures in the medial temporal lobe
itself, and its projections to the diencephalon.17 Memory for single items is
13
M.Moscovitch. Confabulation, in D.L. Schacter, ed., Memory Distortion: How
Mind, Brains, and Societies Reconstruct the Past (Cambridge, MA: Harvard
University Press, 1995) pp. 228-251; A.Gilboa and M. Moscovitch, The Cognitive
Neuroscience of Confabulation: A Review and Model, in A. Baddeley, B. Wilson
and M. Kopelman, eds., Handbook of Memory Disorders, 2nd edition (Chichester,
U.K.: John Wiley and Sons, 2002).

14
M. Moscovitch and G. Winocur, The Neuropsychology of Memory and Aging,
in F. I. M. Craik, and T. A. Salthouse , eds., The Handbook of Aging and Cognition.
(Hillsdale, NJ: Erlbaum, 1992) 315-372. M. Moscovitch and G. Winocur, The
Frontal Cortex and Working with Memory, in D.T. Stuss and R. T. Knight, eds., The
Frontal Lobes (Oxford: Oxford University Press, 2002).

15
Ibid.

16
Ibid., also P. C. Fletcher and R. N. A. Henson Frontal Lobes and Human
Memory: Insights from Functional Neuroimaging, Brain 124 (2001): 849-881.

17
For reviews see J. P. Aggleton and M. W. Brown, Episodic Memory, Amnesia,
and the Hippocampal-anterior thalamic axis, Behavioral and Brain Sciences 22
(1999): 425-89. N. J. Cohen and H. Eichenbaum, Memory, Amnesia and the
Hippocampal System. (Cambridge, MA: MIT Press, 1993). H. Eichenbaum, The
Hippocampus and Mechanisms of Declarative Memory, Behavioural Brain

Memory and the Brain

dependent on the peri-rhinal system whereas memory for relational

information, i.e. the items and the relations among them, whether it be
among spatial elements, among objects, or among words,18 is dependent
on the hippocampal system. The lesion evidence in humans is roughly
consistent with these proposals based on animal models where
dissociations of function are observed along the lines predicted by the
models.19 Recognition memory for single items, and the sense of
familiarity that accompanies that recognition, is disrupted following
peri-rhinal system lesions but is spared in people with hippocampal
system lesions that do not encroach on the peri-rhinal system. On the
other hand, memory of contextually-rich information, such as that which
accompanies recall and recollection of an experienced event (relational
information), rather than a single item, is disrupted following hippocampal
system lesions but not peri-rhinal system lesions.20
Because amnesic people with circumscribed lesions are rare,
investigators have turned to neuroimaging studies in normal people to
test the hypothesis that different aspects of memory are mediated by
different regions of the medial temporal lobe. In general, the evidence
has been supportive of the hypotheses that have been advanced here,
with greater activation in the right hippocampus on tests of relational
Research 103 (1999), 123-33. J. O'Keefe and L. Nadel, The Hippocampus as a
Cognitive Map (Oxford: Oxford University Press, 1978).

18
N. J. Cohen and H. Eichenbaum, Memory, Amnesia and the Hippo-campal
System (Cambridge, MA: MIT Press, 1993). H. Eichenbaum, The hippocampus
and mechanisms of declarative memory, Behavioural Brain Research 103
(1999):123-33. H. Eichenbaum and N. J. Cohen, From Conditioning to Conscious
Recollection: Memory Sstems of the Brain. (Oxford: Oxford University Press, 2001).

19
D. Moscovitch and M. P. McAndrews, Material-specific Deficits in
Remembering in Patients with Unilateral Temporal Lobe Epilepsy and Excisions,
Neuropsychologia 40 (2002): 1335-1342; A. P. Yonelinas The Nature of
Recollection and Familiarity: A Review of 30 Years of Research, Journal of
Memory and Language 46 (2002): 441B517; A. P. Yonelinas, N. E. A. Kroll, J. R.
Quamme, M. M. Lazzara, M. J. Sauve, K. F. Widaman, and R. T. Knight Effects
of Extensive Temporal Lobe Damage or Mild Hypoxia on Recollection and
Familiarity, Nature Neuroscience 5 (2002): 1236B1241.

20
Yonelinas, Review, 2002.

10

Morris Moscovitch

memory for spatial21 and non-spatial information22 and for recollection,23

and in the region of the peri-rhinal cortex on tests of object and
object-location memory and familiarity.
Whatever the final verdict is regarding the role of the various regions
of the medial temporal lobe and diencephalon, the evidence indicates
that the type, extent, and severity of anterograde amnesia is a function of
the size, side, and location of the lesion. This rule applies as well to the
deficits indicative of retrograde amnesia.
Retrograde amnesia and memory consolidation: where and when are
memories stored?
Whereas studies of anterograde amnesia tell us about memory
acquisition, studies of retrograde amnesia provide clues about the time
course involved in consolidating long-term memories and the
physiological processes and neural substrates which contribute to
consolidation and storage. Until recently, it was widely believed that
retrograde amnesia associated with medial temporal and diencephalic
damage was short-lasting and temporally-graded, such that memory loss
was more severe for information acquired near the time of amnesia onset
21
E. A. Maguire, N. Burgess, J. G. Donnett, R. S. J. Frackowiack, C. D. Frith, and
J. O'Keefe, Knowing Where and Getting There: A Human Navigation Network,
Science 280 (1998): 921-924; N. Burgess, E. A. Maguire, J. OKeefe The Human
Hhippocampus and Spatial and Episodic Memory, Neuron 35 (2002): 625-641.

22
K. Henke, B. Weber, S. Kneife, H. G. Wieser, and A. Buck, The Hippocampus
Associates Information in Memory, Proceedings of the National Academy of
Sciences of the United States of America 96: 5884-5889.

23
N. Burgess, E. A. Maguire, and J. OKeefe, The Human Hippocampus and
Spatial and Episodic Memory, Neuron 35 (2002): 625-641; A. M. Owen, B. Milner,
M. Petrides, and A. C. Evans. A Specific Role for the Right Parahippocampal Gyrus
in the Retrieval of Object-location: A Positron Emission Tomography Study, Journal
of Cognitive Neuroscience 8 (1996): 588- 602; J. P. Aggleton, D. McMackin, K.
Carpenter, J. Hornak, N. Kapur, S. Halpin, C. M Wiles, H. Kamel, P. Brennan, S.
Carton, and D. Gaffan, Differential Cognitive Eeffects of Colloid Cysts in the Third
Ventricle that Spare or Compromise the Fornix, Brain 123 (2000): 800-815; L. L.
Eldridge, B. J. Knowlton, C. S. Furmanski, S. Y. Bookheimer, and S. A. Engel,
Remembering Episodes: A Selective Role for the Hippocampus during Retrieval,
Nature Neuroscience 3 (2002): 1149-1152.

Memory and the Brain

11

than for that which was acquired long before. Accordingly, the medial
temporal lobes, particularly the hippo-campus, and possibly the
diencephalon, were considered to be temporary memory structures,
needed only for memory retention and retrieval until memories were
consolidated in the neocortex and other structures where they were then
permanently stored and from where they could be retrieved directly.
Nadel and Moscovitch and others24 identified a number of problems
with the prevailing view. Though the duration of retrograde amnesia
sometimes is short, it is more often the case that large medial temporal
(or diencephalic) lesions will result in retrograde amnesia for details of
autobiographical events. This may extend for decades, or even a lifetime,
far longer than it would be biologically plausible for the consolidation
process to last. These ideas are consistent with earlier observations
made by Warrington and Sanders, and Kinsbourne and Wood. 25
However, retrograde amnesia for public events and personalities, is less
extensive and often is temporally graded; this is truer still of semantic
memory which includes knowledge of new vocabulary and facts about the
world and ourselves (e.g. our address, the names of our friends, our job),
what some have called personal semantics to distinguish these from
autobiographical episodes.26 The distinction between temporally
24
L. Nadel, A. Samsonovich, L. Ryan, and M. Moscovitch, Multiple Trace Theory
of Human Memory: Computational, Neuroimaging, and Neuro-psychological results,
Hippocampus 10 (2000): 352-368. A. Gilboa, G. Winocur, C. L. Grady, S. J.
Hevenor, and M. Moscovitch, Remembering Our Past: Functional Nneuroanatomy
of Recollection of Recent and Very Remote Personal Events, Cerebral Cortex 14
(2004): 1214-1225. L. Nadel, A. Samsonovich, L. Ryan, and M. Moscovitch,
Multiple Trace Theory of Human Memory: Computational, Neuroimaging, and
Neuropsychological Results, Hippocampus 10 (2000): 352-368.

25
E. K. Warrington and H. I. Sanders, The Fate of Old Memories, The Quarterly
Journal of Experimental Psychology 23 (1971): 432-42. M. Kinsbourne and F.
Wood, Short-term Memory Processes and the Amnesic Syndrome, in D. Deutsch,
and A .J. Deutsch, eds., Short-term Memory. (New York: Academic Press, 1975).

26
T. Fujii, M. Moscovitch and L. Nadel, Consolidation, Retrograde Amnesia, and
the Temporal Lobe, in F. Boller, and J. Grafman, eds., The Handbook of
Neuropsychology, Vol. 4. (L. S. Cermak, section ed.), (Amsterdam: Elsevier, 2000);
Also, M. Moscovitch, R. Westmacott, A. Gilboa, D. R. Addis, R. S. Rosenbaum, et
al, Hippocampal Complex Contribution to Retention and Retrieval of Recent and
Remote Episodic and Semantic Memories: Evidence from Behavioral and
Neuroimaging Studies of Healthy and Brain-damaged People, in N. Ohta, C. M.

12

Morris Moscovitch

extensive and temporally-limited retrograde amnesia also applies to

spatial memory. Schematic cognitive maps of old neighbourhoods that
are adequate for navigation are retained but they lack topographical
details and local environmental features, such as the appearance and
location of particular homes, that would allow the person to have detailed
cognitive maps of their locale. 27
Based on this evidence, Nadel and Moscovitch concluded, contrary
to the traditional consolidation model, that the function of the medial
temporal system is not temporally limited but that it is needed to
represent even old memories, whether autobiographical or spatial, in rich,
multifaceted detail, for as long as the memory exists. Neocortical
structures, on the other hand, are sufficient to form domain-specific and
semantic representations based on regularities extracted from repeated
experiences with words, objects, people, environments, and even of
autobiographical episodes that one recollects repeatedly, creating a gist
of each episode. The medial temporal lobe system may aid in the initial
formation of these neocortical representations, but once formed they can
exist on their own. Recent evidence from studies of children whose
hippocampus was damaged at birth or shortly thereafter supports this
view. Vargha-Khadem et al28 found that the children acquired sufficient
general knowledge (semantic memories) to complete high school even
though their memory for autobiographical episodes was impaired.
Corroborating evidence is also provided by neuroimaging studies of
recent and remote autobiographical and semantic memory. These
studies found that the hippocampus is activated equally during retrieval of
recent and remote autobiographical memories, but not during retrieval of

MacLeod, and B. Uttl, eds., Dynamic Cognitive Processes (Tokyo: SpringerVerlag, 2005), 333-380.

27
E. Teng, and L. R. Squire, Memory for Places Learned Long Ago is Intact after
Hippocampal Damage, Science 400 (1999): 675-77. See also R. S. Rosenbaum,
S. Priselac, S. Kohler, S. E. Black, F. Gao, L. Nadel, and M. Moscovitch, Remote
Spatial Memory in an Amnesic Person with Extensive Bilateral Hippocampal
Lesions, Nature Neuroscience 3 (2000): 1044-1048.

28
F. Vargha-Khadem, D. G. Gadian, K. E. Watkins, A. Conneley, W. Van
Paesschen, and M. Mishkin, Differential Effects of Early Hippocampal Pathology on
Episodic and Semantic Memory, Science 277: 376-380.

Memory and the Brain

13

memory for public events or personal semantics; see Maguire for

autobiographical event memory, and Haist et al for famous faces. 29
To account for this evidence, in 1977 Nadel and Moscovitch
proposed a Multiple Trace Theory (MTT) according to which a memory
trace of an episode consists of a bound ensemble of neocortical and
hippocampal/medial temporal lobe (and possibly diencephalic) neurons
which represent a memory of the consciously-experienced event.
Formation and consolidation of these traces, or cohesion, is relatively
rapid, lasting on the order of seconds or at most days. Each time an old
memory is retrieved, a new hippocampally-mediated trace is created so
that old memories are represented by more or stronger traces than are
new ones, and therefore are less susceptible to disruption from brain
damage than more recent ones. With respect to autobiographical
episodes, the extent and severity of retrograde amnesia and perhaps the
slope of the gradient are related to the amount and location of damage to
the extended hippocampal complex in the neocortical temporal lobes.
Remote memories for the gist of events, and for personal and public
semantics, are not similarly dependent on the continuing function of the
hippocampal complex.
Proponents of the standard consolidation model, however, argue
that severe and temporally-extensive retrograde amnesia is observed
only when the lesion extends beyond the hippocampus to include
neocortical structures where remote memories, both auto-biographical
and semantic, are represented. It remains to be determined what specific
contributions the different regions of the medial temporal lobes and
diencephalon make, and how they act in concert with the neocortex and
29
L. Ryan, L. Nadel, K. Keil, K. Putnam, D. Schnyer, T. Trouard, and M.
Moscovitch, The Hippocampal Complex and Retrieval of Recent and Very Remote
Autobiographical Memories: Evidence from Functional Magnetic Resonance
Imaging in Neurologically Intact People, Hippocampus, 2001, 11, 707-714; A.
Gilboa, G. Winocur, C. L. Grady, S. J. Hevenor and M. Moscovitch, Remembering
Our Past: Functional Neuroanatomy of Recollection of Recent and Very Remote
Personal Events, Cerebral Cortex 14 (2004): 1214-1225. F. Haist, J. Bowden
Gore, and H. Mao, Consolidation of Human Memory over Decades Revealed by
Functional Magnetic Resonance Imaging, Nature Neuroscience, 4 (2001): 11391145. L. Nadel, and M. Moscovitch, Memory Consolidation, Retrograde Amnesia
and the Hippocampal Complex, Current Opinion in Neurobiology 7 (1997):
217-227. M. Moscovitch, Recovered Consciousness: A Hypothesis concerning
Modularity and Episodic Memory, Journal of Clinical and Experimental
Neuropsychology 17 (1995): 276-291.

14

Morris Moscovitch

other brain areas to form and retain both detailed, contextually-rich

representations and context- independent knowledge.
Amnesia and neuropsychological theories of normal memory: which
types of memory are affected?
Research on amnesia and other memory disorders has influenced
theories of normal memory at least since the end of the nineteenth
century but at no time has this been more apparent than in the last
quarter of the twentieth century.30 Because amnesia is selective, affecting
some memories and not others, research on amnesia has been used to
promote the view that memory is not unitary, but rather consists of
dissociable components, each governed by its own principles and
mediated by different structures.
For example, evidence showing that retrograde amnesia affects detailed
autobiographical memory more than semantic memory supports to the
idea that episodic and semantic memory are functionally and
neurologically distinct.31
One of the characteristics of amnesia is that it affects long-term or
secondary memory more than short-term or primary memory. This
observation was one of the crucial pieces of evidence used in the 1960s
and early 1970s to argue for a functional separation of memory into at
least these two major components. The idea has since become almost
universally accepted and opened the field to investigation of the
functional differences between the two major components, to
development of the concept of working memory,32 and to identification of
the mechanisms supporting working and primary memory in the frontal
and posterior neocortex.
30
P. Rozin, The Psychobiological Approach to Human Memory, in R. Rozenzweig
and E. L. Bennett, eds., Neural Mechanisms of Learning and Memory (Cambridge,
MA: MIT Press, 1976).

31
E. Tulving, Elements of Episodic Memory (Oxford: Clarendon Press, 1983). M.
Kinsbourne and F. Wood, Short-term Memory Processes and the Amnesic
Syndrome, in D. Deutsch and A. J. Deutsch, eds., Short-term Memory (New York:
Academic Press, 1975).

32
A. Baddeley, Working Memory (Oxford: Oxford University Press, 1986); and
Baddeley, 2003, see footnote 6.

Memory and the Brain

15

Beginning in the late 1960s, research on animal models and humans

indicated that the formation and retention of some types of long-term
memory are spared in amnesia, but there is continuing debate on how
best to characterize them. It is generally accepted that only conscious
recollection is affected by amnesia. Memory retrieval without awareness
seems to be intact. For example, it was noted that people with bilateral
medial temporal-lobe lesions, such as the patient H.M., could learn and
retain motor skills for months or years, though he had no memory of the
learning episode minutes after it was over. The same was true of
perceptual skills involved in reading mirror-reversed words or in
identifying degraded or fragmented pictures and words. That more than
just a skill was involved became apparent when patients could complete
or identify items to which they had been exposed more accurately and
more quickly than new items, which suggests that they stored information
peculiar to that item even though at a conscious level they could not
recall or recognize that they had studied it. At the same time, similar
phenomena were reported in normal people for material they could not
consciously recollect, which suggests that the dissociation between
memory with and without awareness was not peculiar to amnesia but was
indicative of something fundamental about the organization of memory.33
These observations not only had a major impact on our understanding of
normal memory, but were also instrumental in re-vitalizing research on
unconscious processes in cognition and emotion, an area of investigation
that had been abjured by mainstream experimental psychology for almost
a century.
A number of terms have been used to refer to memory with and
without awareness, including declarative and non-declarative (or
procedural) memory, direct and indirect memory, memory and habit,
controlled and automatic memory. I prefer the terms explicit and implicit
memory because they are descriptively accurate, refer to the types of
tests used to assess memory, and are close to theoretically neutral as to
the processes and mechanisms involved. In the last twenty years,
research on normal people and on people with amnesia has identified a

33
L.S. Cermak, ed., Human Memory and Amnesia. (Hillsdale, NJ: Erlbaum, 1982);
N. J. Cohen and H. Eichenbaum. Memory, Amnesia and the Hippocampal System
(Cambridge, MA: MIT Press, 1993); B. Kolb, and I. Q. Whishaw, Fundamentals of
Human Neuropscyhology 4th edition (W. H. Freeman: New York, 1996); M.
Moscovitch, E. Vriezen, and Y. Goshen-Gottstein, Implicit Tests of Memory in
Patients with Focal Lesions or Degenerative Brain Disorders, in F. Boller and H.
Spinnler, eds., The Handbook of Neuropsychology, Vol. 8. (Amsterdam: Elsevier
Press, 1993), 133-173; D. L. Schacter, and R. L. Buckner, Priming and the Brain,
Neuron 20 (1998), 185-195; L. R. Squire, and S. M. Zola, Episodic Memory,
Semantic Memory, and Amnesia, Hippocampus 8 (1998): 205-211.

16

Morris Moscovitch

number of characteristics of implicit memory. The structures implicated in

amnesia, the medial temporal lobes and diencephalon, are not needed
for normal implicit memory. Instead, performance is mediated by a variety
of structures, depending on the type of implicit memory that is being
tested. Like explicit memory, implicit memory is not unitary and consists
of a variety of different subtypes. Although a detailed description of all
them is not possible, three types of which we know a great deal have
been identified: perceptual implicit memory or priming, conceptual implicit
memory, and procedural memory.
On tests of perceptual implicit memory, the test stimulus resembles
the studied target perceptually (e.g., a perceptually de-graded version of
it, or even an identical repetition of it) whereas on tests of conceptual
implicit memory, the test stimulus resembles the target semantically (e.g.,
having studied the word "horse", the participant may be asked to make a
semantic decision to the word during tests, or asked to produce it in
response to the word "animal".) Performance is measured by speed or
accuracy of the response to the test stimulus, without explicit reference to
the studied items, and the implicit nature of the test is corroborated if the
person is not aware that the response or test item refers to a studied
stimulus. Increases in accuracy or decreases in response latency to old
studied items as compared to new ones are indicative of implicit memory
for the studied items.
Research on perceptual implicit memory suggests that performance
is mediated by the same perceptual modules or representation systems
of the posterior neocortex that are involved in perceiving the stimuli.
These modules are modified by the act of processing some given
material, leaving behind a record of that process. As a result, processing
is faster and more accurate when the system is re-exposed to that
material as compared to new material.34 The modules are domain
specific, in that separate ones exist for objects, faces, words, and
possibly places. They are also pre-semantic in that they do not represent
the meaning of the item but only its structure. Thus, performance on
perceptual implicit tests is sensitive to changes in perceptual or structural
aspects of the stimulus but not to changes in semantic aspects.
The opposite holds for performance on conceptual implicit tests,
which is mediated by conceptual systems in the lateral temporal lobe and

34
M. Moscovitch, Memory and Working with Memory: A Component Process
Model Based on Modules and Central Systems, Journal of Cognitive Neuroscience
4 (1992): 257-267; C. L. Wiggs, and A. Martin, Properties and Mechanisms of
Perceptual Priming, Current Opinion in Neurobiology 8 (1998): 227-233.

Memory and the Brain

17

inferior frontal cortex.35 As with perceptual modules, improvement in

performance results from modifications in the conceptual systems
themselves.
Tests of procedural implicit memory involve learning rules, motor
sequences, conditioned responses, and subjective probabilities of
stimulus-response associations without explicit memory for any of them.
The structures that have been identified as crucial for procedural learning
are the cerebellum for classical conditioning, and the basal ganglia, which
are subcortical structures concerned, in part, with motor function. There is
some indication of pre-frontal involvement if learning rules or motor
sequences involves strategic, sequential, or inhibitory components.36
Changes in these structures during execution of procedures underlies the
changes in performance observed on implicit tests of procedural memory.
In studying implicit memory, great care must be taken to insure that
performance on tests of memory that are ostensibly implicit are not
contaminated by explicit components, such as might occur when asking
participants to identify degraded stimuli they had studied earlier. It is for
this reason that studies of amnesic patients are so useful. Because their
explicit memory is so poor, equivalent performance between amnesic and
normal people on an implicit test is taken as evidence that the test in
question was not contaminated by explicit memory.
Amnesia and beyond: a neuropsychological, component process model
of memory
Studies of memory in amnesia have indicated that memory is not
unitary but rather consists of a variety of different forms, each mediated
by different component processes which in turn are subserved by
different neural mechanisms. Because neither short-term or working
memory, nor implicit memory is impaired in amnesia, we might conclude

35
For reviews on implicit memory see Moscovitch, Dobbins L. Schacter, Vriezen
and Goshen Gottstein, Schacter and Buckner. M. Moscovitch, E. Vriezen, and Y.
Goshen-Gottstein, Implicit Tests of Memory in Patients with Focal Lesions or
Degenerative Brain Disorders, in F. Boller and H. Spinnler, eds., The Handbook of
Neuropsychology, Vol. 8 (Amsterdam: Elsevier Press, 1993), 133-173.

36
M. Moscovitch, E. Vriezen, and Y. Goshen-Gottstein, Implicit Tests of Memory
in Patients with Focal Lesions or Degenerative Brain Disorder, in F. Boller and H.
Spinnler, eds., The Handbook of Neuropsychology Vol. 8. (Amsterdam: Elsevier
Press, 1993), 133-173.

18

Morris Moscovitch

that these types of memory are not dependent on the medial temporal
lobes and diencephalic structures which are damaged in amnesia. These
structures, however, are necessary for conscious recollection of
long-term, episodic memories. It has been proposed that any information
that is consciously experienced is picked up obligatorily and automatically
by the hippo-campus and related structures in the medial temporal lobes
and diencephalon. However, these structures bind into a memory trace
those neural elements in the neocortex and elsewhere that mediate the
conscious experience of an event. The episodic memory trace thus
consists of an ensemble of hippocampal and neocortical neurons. The
hippocampal component of the trace acts as an index or file entry
pointing to the neural elements in the neocortex, which represent both the
content of the event and the conscious experience of it. "Consciousness"
is therefore part of the memory trace. Retrieval occurs when an external
or internally generated cue triggers the hippocampal index, which in turn
activates the entire neocortical ensemble associated with it. In this way,
we recover not only the content of an event but the consciousness that
accompanied our experience of it. In short, when we recover episodic
memories, we recover conscious experiences.37
According to this model, both encoding and retrieval of
consciously-apprehended information via the hippocampus and related
structures is obligatory and automatic, yet we know from experience and
from experimental investigation that we have a measure of control over
what we encode and what we retrieve from memory. Moreover, if
encoding is automatic and obligatory, the information cannot be
organized, yet memory appears to have some temporal and thematic
organization. How can we reconcile this model of memory with what we
know about how memory works? One solution is that other structures,
particularly those in the frontal lobes, control the information delivered to
the medial temporal and diencephalic system to encode, initiate and
guide retrieval, monitor, and help interpret and organize the information
that is retrieved. By operating on the medial temporal and diencephalic
system, the frontal lobes act as working-with-memory structures that
control the more reflexive medial temporal and diencepahlic system and
confer a measure of intelligence and direction to it. Such a

37
M. Moscovitch, Recovered Consciousness: A Hypothesis concerning
Modularity and Episodic
Memory, Journal of Clinical and Experimental
Neuropsychology 17 (1995): 276-291. M. Moscovitch, Memory and Working with
Memory: A Component Process Model Based on Modules and Central Systems,
Journal of Cognitive Neuroscience 4 (1992): 257-267.

Memory and the Brain

19

complementary system is needed if memory is to serve functions other

than mere retention and retrieval of past experiences.38
As invaluable as studies of amnesia have been to our understanding
of memory, in order to have a full appreciation of how memory works
those studies need to be supplemented by investigations of memory in
people with other types of disorders, particularly those implicating the
frontal lobes. The realization that the frontal lobes play a crucial role in
memory was slow in coming, but once it did, there was a burgeoning of
research on the frontal lobes, fueled by developments in functional
neuroimaging, that rivaled, and in recent years surpassed, research on
the medial temporal lobes. As a result, investigators have identified a
number of crucial regions of the pre-frontal cortex that are implicated in
encoding, retrieval, monitoring and verification, and have begun mapping
their interaction with the medial temporal lobes and posterior neocortex.
Though the precise function of each region is still uncertain and being
debated vigorously,39 it is becoming increasingly clear that memory relies
on a network of structures, of which the medial temporal lobes and prefrontal cortex are important parts.40 The interaction among these
structures accounts for the formation, retention, and retrieval of durable
memories which can be used flexibly in the service of ones goals and
aspirations, and which con-tribute to ones sense of a personal past and
future, and possibly ones identity.

38
M. Moscovitch, Memory and Working with Memory: A Component Process
Model Based on Modules and Central Systems, Journal of Cognitive Neuroscience
4 (1992): 257-267. M. Moscovitch and G. Winocur. The Frontal Cortex and Working
with Memory, in D.T. Stuss and R.T. Knight, eds., The Frontal Lobes. (Oxford:
Oxford University Press, 2002).

39
See Fletcher and Henson, footnote 16.

40
See Winocur and Moscovitch, footnotes 14, 24, 30, 44.