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Memory changes radically between infancy and extreme old age. Yet in reading the
literature concerned with memory development one is struck by the apparent disconti-
nuity between memory in infancy and memory during the rest of the life span.
Admittedly, this may be simply a consequence of the radically different ways in which
memory is tested in infants, who have no language and limited motor skills as
compared to adults or even young children, in which these capacities are more fully
developed. Yet, despite the attempts of many investigators to account for memory
development in terms of a unitary system that grows or declines in capacity during the
lifespan, it seems that infant memory has characteristics that made it fundamentally
different from that of even very young children. As a student of neuropsychology, 1 was
struck by the similarity between infant memory and organic amnesia. The memory
tests on which infants succeeded were similar to those on which amnesic patients
demonstrated preserved memory abilities, whereas those tests on which infants failed,
amnesic patients also displayed a profound memory impairment.
In an extensive review comparing the memory of infants and organic amnesic
patients, Dan Schacter and I’ suggested that organic amnesia results from damage to a
memory system that develops late in infancy. The preserved memory abilities of
amnesic patients are dependent on the operation of a memory system that develops
early in infancy and accounts for those functions that are characteristic of infant
memory before 8-1 2 months.
In this paper I will review the arguments and evidence Schacter and I presented to
support our hypothesis and compare our approach with that of other developmental
psychologists, particularly Piaget and Inhelder. I will then consider the implications of
our approach to theories of cognitive development, in particular to Piaget’s theory on
the relation between symbolic representation and memory. I will argue that the
capacity for symbolic representation is not sufficient for the development of the late
memory system. I will further suggest that the converse may be true: the full expression
of symbolic representation in cognition and behavior is dependent on the emergence of
the late memory system in infancy. I will then consider briefly the kind of changes that
occur in memory between childhood and old age. Here I will suggest that the changes
in memory performance do not depend on the development of new and different
‘Supported by grants from Medical Research Council of Canada, the Ontario Mental Health
Foundation, and the Connaught Foundation.
78
MOSCOVITCH FROM INFANCY TO OLD AGE 79
memory systems, but rather that the changes result from the maturation and
deterioration of the memory system that is already in place by late infancy and from
the acquisition and deployment of cognitive strategies that serve memory throughout
life.
It is said that children learn more between birth and two years than they do during
any comparable period in their lives. Yet before reaching school-age and certainly
before turning two, a child’s memory for past events is notoriously poor or nonexistent.
Although these two statements may seem paradoxical, they are not. Psychologists have
reconciled them in two ways. One way is to assert that memory functions are similar
throughout life, but that memory performance varies as a function of the tests that are
administered. Given the appropriate tests, even infants can be shown to have a good
memory.’ The other way is to distinguish between different types of memory or forms
of remembering, one of which develops early and the other later. According to the first
approach, which I will call the single memory approach, memory only appears to be
poor in very young children because they lack the means of demonstrating its existence.
Appropriate techniques, such as habituation and conditioning, can reveal quite
startling memory capacities in infants. These techniques rarely, if ever, require the
infant or child to demonstrate that they can consciously recollect a particular episode
by traditional recall or recognition procedures. Instead, they allow the investigator to
infer that previous experience has a powerful and often long-lasting effect on the
child’s subsequent behavior. Despite the difference in testing procedures, some of these
investigators assume that the principles governing memory performance are the same
in infants and in adults. As a result, concepts from the adult memory literature, such as
re~ognition,~ recall, encoding, and retrieval4 are invoked to explain or describe the
infant’s behavior without seriously considering the possibility that these concepts may
take on a very different meaning when applied to such different populations in such
different testing situations.
The alternative way of dealing with the paradox of preserved learning in the face of
poor recollection, the way chosen by Piaget and Inhelder? was to distinguish between
different types of memory, what I will call the multiple memory approach. “Memory in
the wide sense” is observed by noting the effects of any past experience on current or
subsequent behavior. “Memory in the strict sense” is memory for a particular event a t
a particular time and place. According to Piaget and Inhelder, one can speak only of
memory in the wide sense when referring to infants before the age of 1.5 to 2 years.
Although their behavior can be modified by experience and “primitive recognition” of
previously presented signals is possible, the infants cannot recognize or recall in the
sense that they can bring to mind a previous event that they have experienced. The
infant’s failure to have memory in the strict sense was linked by Piaget and Inhelder to
the absence of an appropriate representational system. For them, true recognition and
recall, what I have called conscious recollection,6.’ depends on symbolic representation
which entails, in part, that objects can be brought to mind in their absence. These
objects must have an existence independent of the actions that are performed on them.
Before the development of symbolic representation, the infant relies on sensorimotor
schemas. In such a representational schema, memory cannot be demonstrated by
consciously recollecting an event, but simply by reactivating the procedures, opera-
tions, or actions performed initially on the object and during the event or by altering
the schema that enables the infant to interact with the object. In short, the infant’s
80 ANNALS NEW YORK ACADEMY OF SCIENCES
behavior may be modified but without any recollection of a previous episode. Memory
in the strict sense must therefore await the development of a symbolic representational
system.
Research on traumatic amnesia in adult humans (and animals) has been concerned
with similar theoretical issues. Human amnesia has a variety of etiologies, ranging
from concussions, ECT, encephalitis, chronic alcoholism and vitamin deficiency, to
neurosurgical excisions. The form that amnesia takes, therefore, may be different
depending on the etiology, the structure of the brain that was damaged, and, perhaps,
even the age and personality of the individual. All amnesias, however, have a variety of
symptoms in common.’ The hallmark symptom is that amnesic patients find it very
difficult, if not impossible, to recollect post-traumatic events. That is, they have a
profound anterograde memory deficit. Amnesic patients are nonetheless capable of
acquiring new information, sometimes normally, despite having no conscious recollec-
tion of having acquired it. At first, it was thought that only perceptuomotor skills are
acquired by amnesic patients whereas true cognitive skills were not.* Recently,
however, it has been demonstrated by a number of investigators that amnesic patients
can use letter fragments to recall words they had seen earlier,g’1° they can solve
anagrams faster the second time than the first,” they can solve the Tower of Hanoi as
quickly as normal people,” and, given sufficient support, they can even show that they
are capable of forming new associations between randomly paired words even after a
single pre~entation.’’*’~
It is important to remember, however, that these demonstrations of relatively intact
memory in the face of profound amnesia occur only when the following three
conditions are satisfied”: the tasks are so highly structured that the goal of the task and
the means to achieve it are apparent, the means to achieve the goal are available to the
subject (i.e., the response and the strategies used to arrive at the goal are already in the
subject’s repertoire), success in achieving the goal can be had without reference to a
particular postmorbid event or episode. With slight modification, these are the same
conditions under which memory can be demonstrated in infants. Likewise, there are
now two approaches to dealing with these paradoxical memory abilities of amnesic
patients that are analogous to the approaches adopted by investigators of infant
memory. The single-memory approach is based on the view that there is a single
memory system whose operation and the memory it reveals varies with the tests used to
probe it. Amnesic patients, like infants, may be incapable of revealing their memories
except on tests such as habituation or dishabituation, conditioning, and priming that
make no demands on conscious recollection. I will illustrate this point with a recent
experiment conducted in collaboration with Mary Rees-Nishio.
A number of infant studies use psychophysiological measures, most typically heart
rate, to gauge the infant’s ability to process different types of information.I6 These
measures are usually used in habituation-dishabituation paradigms in which the trials
are often separated by a few seconds. As a result, studies employing these techniques
necessarily involve a memory component and, in addition to cognitive or perceptual
competence, these studies measure the infant’s memory for previous events, however
short-lived it may be. Rather than heart-rate, Rees-Nishio and I used the skin
conductance response (SCR) as a psychophysiological index of memory and compared
it with the more traditional measures of recognition and recall.
The study was concerned with a number of issues regarding the relation of emotion
MOSCOVITCH: FROM INFANCY TO OLD AGE 81
to memory, but I will present only those findings that are directly relevant to this
discussion (for a detailed report see Rees-Ni~hio’~).Subjects studied a set of emotional
and non-emotional words. A week later they were shown the same words mixed with an
equal number of emotional and non-emotional distractors. Their task was simply to say
whether or not they recognized the word as one they had previously studied and
indicate the confidence they had in their answer on a seven-point scale, with one as low
confidence and seven as high confidence. Both of these can be considered traditional
tests of conscious recollection. At the same time, the first skin conductance response
(SCR) within eight seconds of word presentation was measured. The SCR is an
electrophysiological index of habituation and arousal both of which may reflect
“memory in the wide sense” for a previous event in that it tracks changes in neural
FIGURE 1. Differences in reaction time between the first and second presentation of a word in
lexical decision task and recognition tasks. The second word was presented at lags of 0, 7, or 29
items after the first word. MEM. DIS. refers to patients with severe memory disorders.
amnesic patients as in our young and elderly control subjects, demonstrating that the
amnesic patients’ “memory” can appear normal under these testing conditions.
That their memory in the strict sense, namely conscious recollection of particular
events, was severely compromised becomes evident as soon as the repetition priming
paradigm was altered in the following way. Instead of deciding whether each letter
string forms a word or not, the subject had to indicate whether this was the first or
second time that the word appeared on the screen. Here we see that normal
performance deteriorates with lag, although the rate was identical for young and old
people. Many amnesic patients, however, performed at chance level even on the first
presentation of an item. Their data, therefore, do not appear on the graph.
Dan Schacter and I, in a review comparing the literature on memory in infants and
in amnesic patients,’ concluded that the memory system that develops early in infants,
Piaget’s “memory in the wide sense,” is spared in amnesic patients whereas the system
that develops late, “memory in the strict sense,’’ is impaired. Because amnesia is often
associated with bilateral damage to the hippocampus, frontal lobes, and related
structures that typically develop late in mammals,22s23 we felt that we were on safe
ground in referring to the preserved and impaired systems as early and late,
MOSCOVITCH: FROM INFANCY TO OLD AGE 85
respectively. Also, the terms early and late carried very little theoretical baggage. It
enabled us to capture the relevant distinctions between infant and child memory on the
one hand, and amnesic and normal memory on the other, without committing ourselves
to any particular theoretical view of the nature of the memory systems. We speculated
that tests of habituation-dishabituationin infants had qualities similar to tests of
priming in amnesic patients. Similarly, those paradigms that led to successful
conditioning and learning in infants produced normal performance in amnesic patients
and in animals with hippocampal lesions, whereas failure or anomalous performance in
one group was likely to produce similar results in the other.
We may have erred in drawing analogies between the trouble that infants have on
cross-modal matching tasks and the difficulty in obtaining cross-modality effects in
some priming paradigms used with adults (see Schacter & Moscovitch,' pp. 189-191).
First, it is not yet clear whether failures to find evidence for cross-modal matches early
in infancy reflects methodological problems more than the infant's cognitive incompe-
tence. Second, and perhaps more telling, is our own difficulty in demonstrating that all
amnesic patients fail on tests of cross-modality matching. In our study, we had subjects
inspect haptically or visually wire figures that were bent into nonsense shapes. The
subject then had to choose the target item from two items presented in the same or in a
different modality. The first four patients performed worse than control subjects in the
cross-modal but not in the unimodal condition, whereas the next four subjects did not
differ significantly from control subjects in either condition. What was most discon-
certing was that performance did not vary in any obvious way with the severity of the
amnesia. The most amnesic of our patients performed normally in this task!
LAG
FIGURE 2. Differences in reaction time between the first and second presentation of a nonword
in lexical decision and recognition tasks. The second nonword was presented at lags of 0, 7. or 29
items after the first word.
86 ANNALS NEW YORK ACADEMY OF SCIENCES
As a test of our ideas we chose to look at the AB or stage IV error. Piaget2’ observed
that 8-10-month-old infants can search successfully for an object hidden at location A.
After repeatedly finding the object a t A, most infants will continue to search for the
object there even when, in full view, it is moved and hidden at a new location, B.
We decided to test for the presence of similar errors in amnesic patients for a
number of reasons. First, this observation holds a central place in Piaget’s account of
the development of object permanence and, by extension, symbolic representation.
According to Piaget, object permanence is achieved when the object can be called to
mind independently of the perceptuomotor procedures performed on it. During Stage
IV, the infant’s concept of an object is still limited to the previous sensorimotor
operations performed on it and these are elicited when the infant tries to find it. Since
these operations were directed at a particular location in the past, they continue to be
directed at the old location even though the object has been moved to a new one. Only
later, when the capacity for symbolic representation has matured, can infants begin to
search directly at the new location. In fact, it is on the basis of accurate performance on
this task, that the development of symbolic representation is inferred. According to this
interpretation, Stage IV errors should not be committed by individuals who have long
ago developed object permanence.
A second reason for testing for Stage IV errors in amnesic patients, is that the
phenomenon lends itself so readily to a memory interpretation. Such an interpretation
had already been proposed by other infant but had been met with
counterproposals that either defended Piaget’s interpretation or advanced new inter-
pretations. The area has a rich experimental and theoretical l i t e r a t ~ r e , ’ * which
~ ~ . ’ ~ is
the third reason we decided to venture into these thoroughly tested waters to see if we
can make our very own waves.
Six severely amnesic patients and six patients with mild cognitive deficits but less
severe memory loss participated in the study. Except for the profound memory deficit
of the amnesic patients that is reflected even in such gross measures as the M Q on the
Wechsler Memory Scale, the two groups did not differ in age, education, or IQ (for the
details of patient population see Schacter and Moscovitch’).
The tests were designed to resemble the infant tests as much as possible. The first
test had two phases. In phase I , the patient had to find an object immediately after the
experimenter hid it behind a set of books located three meters behind the patient a t
location A. Following this immediate test, the experimenter engaged the patient in 2.5
88 ANNALS NEW YORK ACADEMY OF SCIENCES
minutes of conversation after which the patient was again asked to find the missing
object. The cycle of hiding, immediate test, and delayed test was repeated until the
patient found the object at location A on three successive delay trials. A different
object was hidden each time. The same series of events occurred on the next trial,
except the object was hidden at a new location, B, behind a plant or a book on top of a
filing cabinet two meters to the left and a little behind the patient.
The resemblance between the performance of amnesic patients and infants
extended to all phases of the experiment, as FIGURE 3 illustrates. All patients could
locate the object a t A even on the delay trials. On the delayed B trials, four of the six
amnesic patients continued to search for the object at A instead of at B and expressed
surprise when they found nothing there. When queried further, none could recall that
an object had been hidden a t the B location. In contrast, all the control patients
remembered the location of the hidden object on all A and B trials.
Investigators who argue against a memory interpretation of the infant’s failure on
this task cite the observation that infants continue to search for the object at A even
when it is not hidden at a new location but placed there out in the open and in full view
of the infants. Phase 2 served as a further test of the memory interpretation. In phase 2
of the experiment, after two additional successful delayed searches at A, the object was
placed on a desk in full view of the subject at location C. which was directly in front of
location A. The subject could not avoid seeing the visible object a t C when looking or
searching at A. After an immediate test, the subject was engaged in conversation for
two minutes before being asked to find the object that was placed in the room.
As FIGURE 3 illustrates, five of the six amnesic patients failed to locate the object
on the C trial, despite its being directly visible to them. Four subjects looked directly
past the visible object and searched again at A. When told immediately afterwards to
examine the objects on the desk to see if the target object was located there, all the
patients either denied it was there, still maintaining it was placed at A, or chose the
wrong item. All but one of the control patients “found” the object at C, and the patient
who failed corrected himself spontaneously.
The results of phase 2 indicate that failure to “find” visible objects can indeed be
attributed to a poor memory and this, presumably, applies to infants as well. This
interpretation was further supported by the amnesic patients’ failure to recall correctly
A I 1
- AMNESICS
CONTROLS
b
FIGURE 3. Delayed recall of location and object
by amnesic and control patients on consecutive
trials of an object search task conducted in dif-
ferent places in a testing room. Objects were
hidden at an initial location (A) and a second
location (B) and were visible at a third location
(C). A different object was used on each trial.
TRIALS
MOSCOVITCH: FROM INFANCY TO OLD AGE 89
A I
TRIALS
the object for which they were searching. Except for the first A trial, amnesic patients’
delayed object recall was very low in comparison (FIGURE 3) to the control group’s. T o
test for the generalizability of our results, on a different occasion we hid the object in
different drawers (locations A and B) of a small, plastic container. W e found virtually
identical results as in the large room condition (FIGURE 4).
The resemblance between the performance of amnesic pgtients and infants on the
search task is striking. We called this analogue of the AB, or Stage IV, an error
in amnesic patients the “mnemonic precedence effect.” There is little doubt that the
effect occurs in amnesic patients because of poor memory rather than a poorly
developed object concept. At first glance, what is surprising is not their poor
performance on the B and C trials, but their relatively normal performance on the A
trials. If we consider the A trials as unique events that require little effortful processing
to remember,” it becomes easier to understand how even amnesic patients do well on
the A trials at relatively short delays. On the B and C trials, however, not only must the
patients remember that event, but she must distinguish it from the previously repeated
trials. Since it is established that amnesic patients are highly susceptible to proactive
interference, their failure in the B and C trials and their intrusion of A trial responses is
not only understandable but consistent with their performance on verbal analogues of
this search task.”
To rule out a pure response perseveration interpretation of the mnemonic prece-
dence effect, we administered the task to three patients with documented bilateral
frontal lesions who exhibit the classical perseverative cognitive deficits associated with
frontal lesions. All of these patients performed normally on the task.
The striking similarity between amnesic and infant performance on the search task
suggests, but does not prove, that the underlying causeof the Stage IV error is the same
for both groups-an impaired late memory system not a poorly developed symbolic
representational system. This interpretation is supported by other research showing
that memory is a significant factor in infant search tasks” and by other similarities in
memory performance between the two groups.’ Accepting this interpretation implies
that the infant may have developed the concept of object permanence, that is a form of
90 ANNALS NEW YORK ACADEMY OF SCIENCES
symbolic representation in a conceptual sense, but may not be able to evoke the object
to mind voluntarily because this latter act requires the late memory system. This view
predicts that so long as tests do not invoke the late memory system, object permanence
can be shown to develop much earlier than Piaget claimed. A recent study by
Baillargeon er supports this prediction. By using a habituation-dishabituation
paradigm, which by my criteria is associated with the early memory system, she found
that 5-month-old infants who expect to see a solid object behind a screen increased
their looking time when the screen tilted all the way backwards-an impossible feat if
a solid object were already there. She interpreted her finding as evidence for the
existence of a form of object permanence, and by inference symbolic representation,
even in a 5-month-old infant.
The third major implication that follows from these considerations is that it is
premature, if not altogether wrong, to link the early and late memory system
exclusively with sensorimotor and symbolic representations, respectively. I have
already argued that the capacity for symbolic representation is not sufficient either for
the development or the continued operation of the late memory system. That symbolic
representation is necessary for conscious recollection, however, seems likely, but is not
proven.
With regard to the early memory system, there are strong indications from the
amnesia literature that it can operate on symbolic or declarative representations,
although typically its functions are associated with sensorimotor or procedural
operations. Thus, in addition to learning mirror drawing and ~nirror-reading,~*~**’~ and
solving jigsaw puzzles” and the Tower-of-Hanoi (somewhat stretching the concept of
procedural or sensorimotor kn wledge),” amnesic patients have also learned new facts
5c
about individual^,^^ formed ass iations between randomly paired and even
learned to redefine old words for use on a computer”-all this without any conscious
recollection of having learned the material at all.3s
Again, an experiment from my laboratory will illustrate this phenomenon.
Amnesic patients and normal young and elderly subjects were presented with a list of
40 pairs of randomly associated words. After studying each of these pairs for three
seconds, the subjects were required to read as quickly as possible a list of the original
pairs, a list of recombined pairs in which a stimulus item from one pair was recombined
with a response item from another pair, and a list of new pairs they had never seen
FIGURE 5. Reading time in seconds to old, recombined (REC), and new word pairs. The right
panel shows the reading time when the old and new words are presented individually rather than
as pairs. MEM. DIS.refers to patients with severe memory disorders.
MOSCOVITCH FROM INFANCY TO OLD AGE 91
100 -
80 -
80 -
m-
60 -
50 -
40 -
30 -
20 -
10 -
I I I
0 LO REC NEW
FIGURE 6. Proportion of positive “yes” responses to old, recombined (REC).and new items on a
recognition test.
before. As FIGURE5 indicates, amnesic patients like old and young control subjects,
read the old pairs faster than either the recombined or new pairs indicating that they
had formed novel associations. Unlike the normal control subjects, however, the
amnesic patients performed very poorly on a subsequent recognition test (FIGURE6).
In a later modification of this experiment, Graf and S ~ h a c t e r ’had
~ subjects
complete a word given its first three letters. They showed that both amnesic patients
and normal control subjects performed much better if the word fragment was
presented along with the stimulus item that was associated with it a t study rather than
with a new word or with another word taken from the list. If the subjects were asked to
recall the response words, rather than merely complete them, amnesic performance
dropped dramatically whereas normal performance actually improved (see Schacter,
this volume). Both these tasks satisfy the conditions stated earlier that are associated
with preserved functioning of the early memory system in amnesia, yet it would be
difficult to argue that the formation of new word associations is based simply on
procedural or sensorimotor knowledge, or even on the activation of old memories,
without seriously distorting currently held views of these concepts. A more parsimo-
nious explanation is that the early memory system can operate on symbolic representa-
tions. It is important to note, however, that the domain over which this newly acquired
92 ANNALS NEW YORK ACADEMY OF SCIENCES
infant is like the amnesic patient in this way. Because he has virtually no past from
which to draw his knowledge and is prevented from evoking any new symbolic
representations until the late memory system is in place, the infant’s cognitive
development may appear more impoverished than it really is.
I do not wish to leave the impression that once the late memory system becomes
functional in late infancy no other interesting changes occur. There is no doubt that
memory improves dramatically from late infancy through childhood and adolescence
and declines again in old age,’- though what accounts for these changes is
unresolved. What I wish to emphasize is that the emergence of the late memory system
in infancy marks an important transition in memory development and to suggest that it
might also underlie or make possible important changes in cognitive d e ~ e l o p m e n t , ’ ~ . ~
particularly with regard to symbolic representation.
Are there, however, other significant transitions that can account for the changes
that occur in memory during the rest of the life span? From a psychological and
neuropsychological perspective, the safe answer would be “yes.” It is commonplace to
note that memory and cognition are linked. Whatever cognitive skill is acquired, be it
language, number concept, or seriation, it is likely to influence some aspects of memory
for information associated with that skill (see J. Moscovitch4’for a thorough discussion
and some very interesting experiments on this issue with special emphasis on the
relation between memory and seriations’). If we accept the neuropsychological premise
that cognitive skills are dependent on the development of neural structures that
mediate that skill, then again, one would be forced to conclude that significant
transitions in the development of memory coincide with the period during which these
structures become functional. This is especially true for structures such as the frontal
lobes that develop late and whose damage leads not only to cognitive but to
specific memory deficits as well.4’.”
Despite this evidence, I wish to propose that after the late memory system becomes
functional, the major changes that occur in memory during the lifespan can be
explained best, not by postulating many additional fundamental changes, but by the
further maturation and later deterioration of the early and late system, and by the
acquisition and loss of cognitive strategies that affect memory p e r f ~ r m a n c e . ” ~ .I~n ’
short, in terms of memory function per se, the major changes that occur are changes in
capacity and efficiency, not changes in fundamental memory processes. In addition,
the child acquires knowledge both about the world and about how some aspects of
memory and cognition work.45That knowledge can then be used either directly to help
encode and retrieve information or indirectly to create strategies that can serve
memory. By contrast, in normal aging there is a mild deterioration of the structures
associated with the late memory as well as a reduction in working memory4’ or
mental energy and attentional resources.48 As a result, the normal elderly person’s
memory performance is impaired primarily on those tasks of conscious recollection
that are effortfu13’ and rely primarily on internal generation rather than external
environmental support for successful p e r f ~ r m a n c e Because
.~~ the late memory system
is not severely compromised, forcing the elderly person to adopt appropriate strategies
and providing her with external support either in the form of a simple, easily organized
task structure or cues, or both, can often raise her performance to the level of the
y o ~ n g . ~Once
~ . ~ the
’ late memory system is severely impaired, as in pathological forms
94 ANNALS NEW YORK ACADEMY OF SCIENCES
ACKNOWLEDGMENTS
I thank Meredyth Daneman, Howard Gardner, Jill Moscovitch, Dan Schacter, and
Sandra Trehub for their very helpful comments. Don McLachlan kindly referred most
of the patients to us and acted as a neurological consultant on the projects.
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