Psychological Review
1997, Vol. 104, No. 3, 467-498
Copyright 1997 by the American Psychological Association, Inc.
0033-295X/97/$3.00
Dissociations in Infant Memory: Rethinking the Development
of Implicit and Explicit Memory
Carolyn Rovee-Collier
Rutgers, The State University of New Jersey
Extending the Jacksonian principle of the hierarchical development and dissolution of function to
the development and dissolution of memory, researchers have concluded that implicit (procedural)
memory is a primitive system, functional shortly after birth, that processes information automatically,
whereas explicit (declarative) memory matures late in the 1st year and mediates the conscious
recollection of a prior event. Support for a developmental hierarchy has only been inferred from the
memory performance of adults with amnesia on priming and recognition-recall tests in response to
manipulations of different independent variables. This article reviews evidence that very young
infants exhibit memory dissociations like those exhibited by adults with normal memory on analogous
memory tests in response to manipulations of the same independent variables. These data demonstrate
that implicit and explicit memory follow the same developmental timetable and challenge the utility
of conscious recollection as the defining characteristic of explicit memory.
If empirical dissociations were the criterion for differentiating memory systems, our field of memory might soon become a taxonomic
science resembling botany. - - R . G. Crowder, Varieties of Memory
and Consciousness: Essays in Honour of Endel Tulving
1978), horizontal and vertical associative systems (Wickelgren,
1979), procedural and declarative memory (N. J. Cohen &
Squire, 1980; Squire, 1987), early-developing and late-developing systems (Schacter & Moscovitch, 1984), implicit and
explicit memory (Graf & Schacter, 1985; Schacter, 1987), semantic and cognitive memory (Warrington & Weiskrantz,
1982), and taxon and locale systems (Jacobs & Nadel, 1985;
Nadel, 1992). All of these share the assumption that the memory
system that is spared by amnesia (e.g., implicit or procedural
memory) is primitive and functional very early in the course of
human development, whereas the memory system that is impaired by amnesia (e.g., explicit or declarative memory) is
higher level and becomes functionally mature late in the 1st
postnatal year. Because the implicit and explicit memory systems seem to be the most widely accepted dichotomy, in what
follows, I focus on them.
Contrary to the assumption that the memory system of very
young infants is exclusively implicit, evidence amassed from a
large number of studies that were conducted over the past 25
years reveals that very young infants display experimental dissociations in memory performance that exactly mirror the memory
dissociations displayed by adults with normal memory on analogous tests in response to manipulations of the same independent
variables. This evidence disputes claims that implicit and explicit memory follow different developmental time lines and
challenges the utility of conscious recollection as the defining
Proponents of multiple memory systems argue that two separable and functionally distinct memory systems mature at different rates during the 1st year of life. The core argument of this
article is that even very young infants behave like adults with
normal memory on memory tasks thought to distinguish these
systems.
Support for the popular assumption that two different memory
systems mature at different rates during the 1st postnatal year
is based on the large number of empirical dissociations in the
memory performance of aging adults with amnesia and patients
with Korsakoff's syndrome on various priming and recognition-recall tests in response to manipulations of different independent variables. These dissociations initially led to inferences
about functional dissociations of the cognitive processes and
the neural mechanisms that underlie them which, in turn, led
researchers to propose a number of dichotomous memory systems. ~ The proposed systems include episodic and semantic
memory (Kinsbourne & Wood, 1982; Tulving, 1972, 1983), the
habit system and the memory system (Bachevalier & Mishkin,
1984; Hirsh, 1974), reference and working memory (Honig,
All research from my laboratory and the preparation of this article
were supported by National Institute of Mental Health Grants R37MH32307 and K05-MH00902.
I am endebted to the many students and colleagues, past and present,
who contributed to the research on which this article is based. I also
thank Paula Hertel for providing the material on affect in adults and
George Collier for critical comments.
Correspondence concerning this article should be addressed to Carolyn Rovee-Collier, Department of Psychology, Busch Campus, Rutgers,
The State University of New Jersey, New Brunswick, New Jersey 08903.
Electronic mail may be sent via Internet to [email protected].
Not only has the number of memory systems been debated, but so
has the question of whether multiple memory systems even exist (J. R.
Anderson & Ross, 1980; Baddeley, 1984; Craik, 1983; Hintzman, 1984;
Jacoby, 1984; Johnson, 1992; G. Mandler, 1985, 1989; McKoon, Ratcliff, & Dell, 1986; Olton, 1989; Roediger & Blaxton, 1987; Snodgrass,
1989; Tulving, 1985). One of the best known alternatives to multiple
memory systems holds that memory deficits result from a discrepancy
in the processing operations required at study and at testing; conversely,
evidence of memory is found when these operations match (Roediger,
1990; Roediger & Blaxton, 1987).
467
468
ROVEE-COLLIER
characteristic of explicit memory. It seems unlikely that any
simple dichotomy could adequately characterize a process as
complex as memory, even during the infancy period. Should a
dichotomy eventually prove to be the most satisfactory account,
then at a minimum, both implicit and explicit memory must be
viewed as primitive systems that are simultaneously functional
very early in development.
The Development of Memory Systems: The A r g u m e n t
For many years, preverbal infants were thought to be incapable of retention for longer than a few seconds or minutes at
most (for review, see Werner & Perlmutter, 1979). The capacity
for long-term memory was assumed not to emerge until late
in their 1st year (e.g., Kagan & Hamburg, 1981; Schacter &
Moscovitch, 1984). In retrospect, this assumption is not surprising. It was based on data collected using visual attention measures in a variant of the delayed matching-to-sample paradigm:
the traditional paradigm used to measure short-term memory in
rats (Roberts, 1972b, 1974), pigeons (Grant & Roberts, 1973;
Roberts & Grant, 1976; Shimp & Moffitt, 1974; Zentall, 1973)
and monkeys (D'Amato, 1973; Jarrard & Moise, 1971; Jarvik,
Goldfarb, & Carley, 1969). Recently, however, paradigms using
motivated infants have yielded evidence that even very young
infants can retain information about the events in which they
participated for weeks, months, and sometimes even years
(Hartshorn et al., in press; Hayne, 1990; Hitchcock & RoveeCollier, 1996; Myers, Clifton, & Clarkson, 1987; Myers, Perris, & Speaker, 1994; Perris, Myers, & Clifton, 1990; RoveeCollier, 1990).
Paradoxically, the disparity between these two sets of findings
has not been explained in terms of a paradigm shift but by
attributing the very excellent retention of younger infants to an
early-maturing memory system that is characterized as being
independent of and functionally different from a late-maturing
memory system, which is presumed to become functional near
the end of the 1st year (Schacter & Moscovitch, 1984). The
hypothesis that two separable memory systems mature at different rates during the 1st postnatal year is now widely accepted
as fact (Bachevalier, 1990; Bachevalier & Mishkin, 1984; J. M.
Mandler, 1990; McKee & Squire, 1993; Naito & Komatsu, 1993;
Parkin, 1989; Schacter & Moscovitch, 1984; Tulving, 1983;
Tulving & Schacter, 1990). Most scientists probably believe that
there is empirical evidence for the conclusion that different
systems mediate the retention of different types of acquired
knowledge at different points in development, but there is none.
Instead, the sole evidence for two, functionally distinct memory
systems that follow different developmental timetables has come
from studies of aging individuals with amnesia, patients with
Korsakoff's syndrome, and monkeys with brain lesions, whose
brain damage presumably impairs the late-maturing system but
spares the early one. In a much-cited article entitled, "The
Development of Procedural Memory" (McKee & Squire,
1993), for example, participants ranged from 49 to 77 years of
age, and their mean age was 63 years!
Just as there are obvious differences between human infants
and monkeys with brain lesions, however, there are also vast
differences between infants and the aging adults with amnesia
and patients with Korsakoff's syndrome with whom they have
been compared. Infants, for example, have yet to develop language and the vast networks of associations and experiences
that" adults with amnesia have acquired over the course of a
lifetime. Moreover, infants are not brain-damaged. Although the
attempt to apply the Jacksonian principle of the hierarchical
development and dissolution of function to the hierarchical development and dissolution of memory is intuitively appealing
(Naito & Komatsu, 1993), it is untenable in the absence of
supporting evidence (Campbell, Sananes, & Gaddy, 1984).
Experimental Dissociations in Adult
Memory Performance
Experimental dissociations in adults' memory performance
on direct tests (e.g., recall and recognition tests), which are
thought to require awareness or conscious recollection, and indirect tests (e.g., priming tests), which are not, are the cornerstone
for the assumption that there are two separable memory systems
(e.g., Graf & Schacter, 1985; Squire, 1987; Vriezen, Moscovitch, & Bellos, 1995). Tulving (1983) described the rule of
experimental dissociation as follows:
Dissociation is said to have occurred if it is found that the manipulated variable affects subjects' performance in one of two tasks,
but not in the other, or affects the performancein differentdirections
in the two tasks. Thus, dissociationrefers to the absenceof a positive
association between dependent variables of two different tasks.
(p. 73 )
He suggested that an analogous logic could be applied to studies
of developmental or pathological dissociations, with the performance of groups differing in age or pathology being compared
on two tasks.
One of the earliest reported memory dissociations was, in
fact, of the latter type: Warrington and Weiskrantz (1970) administered free recall and recognition tests as well as two priming tests (word-fragment completion involving degraded letters
and stem-completion tests) to an institutionalized group of
brain-damaged patients with amnesia and a control group of
patients without brain damage. The memory performance of
patients with amnesia was impaired on the recall and recognition
tests but not on the priming tests. Since then, individuals with
amnesia have exhibited preserved learning on a variety of other
indirect tasks, including word-fragment completion, word completion, lexical decision, perceptual decision, spelling of homophones, preference judgments, free association of related information, and word completion with new associates (for review,
see Shimamura, 1986) but not on direct tasks (Jacoby & Witherspoon, 1982; Moscovitch, 1982; Shimamura & Squire, 1984;
for review, see Shimamura, 1986).
Memory dissociations on recall-recognition tasks versus on
various priming tasks were subsequently documented in adults
with normal memory, who performed differently when instructed either to recollect a prior specific episode (usually the
study episode) or to make no reference to a prior episode,
respectively (Graf, Squire, & Mandler, 1984; Jacoby & Dallas,
1981; Schacter, 1987; for review, see Richardson-Klavehn &
Bjork, 1988). These findings gave impetus to the view that
individuals with amnesia were capable of initially encoding information but had difficulty subsequently in gaining awareness
ON THE DEVELOPMENT OF MEMORY SYSTEMS
of it (Crowder, 1988). G. Mandler (1989), for example, referred to the inability of the patient with amnesia " t o use access
routes to information that is not available automatically" (p.
96).
A number of criticisms have been levied at inferences of
different memory systems from differential performance on indirect and direct tasks. For one, the tasks that are used to measure memory performance and the forms (processes) of memory
thought to underlie performance on those tasks are often treated
as equivalent. A measurement per se, however, is neither an
underlying process nor a particular form of memory (Richardson-Klavehn & Bjork, 1988; Roediger & McDermott, 1993). As
Richardson-Klavehn, Gardiner, and Java (1994) noted, "these
dichotomies all obscure important distinctions between different
mental states and processes that may occur in direct and indirect
test performance" (p. 2). In addition, empirical dissociations
on direct and indirect tests of memory reflect only task distinctions, and implicit memory tasks often contain an explicit component and vice versa (e.g., Jacoby, 1991; Rajaram, 1993). As
Jacoby ( 1991 ) observed,
Most past investigations of automatic (unconscious) influences of
memory or perception assumed a one-to-one mapping between processes and tests. The drawing of conclusions, then, requires that
tests be factor- or process-pure with regard to the type of processing
they measure. A difficulty for identifying processes with tasks is
that tasks are probably never process pure . . . . That problem is
not fully solved by finding task dissociations between manipulations
or between subject populations and type of test. (p. 531 )
Common Distinctions Between Implicit
and E x p l i c i t M e m o r y
The characteristics that distinguish implicit from explicit
memory are presented in Table 1.2 Central to the distinction
between these s y s t e m s - - a n d the distinction that is most often
i n v o k e d - - i s the role of consciousness, that is, whether retention
is with conscious awareness or not. Today, conscious recollection is almost universally accepted as the defining characteristic
of explicit memory that distinguishes it from implicit memory.
According to Schacter (1989), "Explicit memory is roughly
equivalent to 'memory with consciousness' or 'memory with
awareness.' Implicit memory, on the other hand, refers to situations in which previous experiences facilitate performance on
tests that do not require intentional or deliberate remembering"
Table 1
Frequently Cited Distinctions Between Implicit
and Explicit Memory
Implicit memory
Explicit memory
Without conscious awareness
Nonepisodic, general
Abstract
Automatic (incidental)
Involuntary
All-or-none retrieval
No capacity demand
Weighted for object form
With conscious awareness
Episodic, particular time or place
Concrete
Deliberate (controlled)
Voluntary
Partial retrieval (decay effects)
Limited capacity
Weighted for object function
469
(p. 356). Likewise, according to J. M. Mandler (1984), " i n all
adult studies the term 'recognition' implies consciousness or
awareness of prior occurrence. It is assumed that the adult is
aware that the item in question has been experienced in his or
her personal past" (p. 77). Subsequently, she wrote, "This
dissociation suggests a dual memory system, one that is automatic in operation and not accessible to conscious report, and
another whose contents can be brought to mind and thought
about" (J. M. Mandler, 1990, p. 487).
Any distinction between memory systems that is based on
evidence of conscious awareness, however, is untenable from
developmental and comparative perspectives. Whether or not a
preverbal infant or an animal is consciously aware of having
previously experienced a previous episode (Schacter & Moscovitch, 1984) or has a sense of "pastness" (J. M. Mandler, 1984;
Tulving, 1983) cannot be directly tested but is solely a matter
of philosophical speculation (see also Shapiro & Olton, 1994).
Yet, this distinction has become the primary basis for concluding
that preverbal infants and animals have an implicit memory
system only (e.g., Bauer, 1996; J . M . Mandler, 1984, 1990;
McDonough, Mandler, McKee, & Squire, 1995; McKee &
Squire, 1993; Naito & Komatsu, 1993; Schacter & Moscovitch,
1984; Tulving & Schacter, 1990). 3
M e m o r y P r o c e d u r e s U s e d W i t h P r e v e r b a l Infants
The majority of studies of long-term memory with preverbal
infants have used the mobile conjugate reinforcement paradigm.
This paradigm overcomes the fact that prelinguistic infants lack
a verbal response to indicate whether or not they recognize
a test stimulus by teaching them a motoric o n e - - a n operant
f o o t k i c k - - t h a t they can subsequently use for this purpose. In
this paradigm, infants learn to kick to move a crib mobile.
The critical to-be-remembered information is either displayed
directly on the sides of the mobile or in the context (e.g., on
cloth panels draped over the sides of the crib or playpen) in
which training occurs. In the standard procedure, 2- and 3month-old infants receive a 15-min training session with a particular mobile on each of 2 consecutive days. Each session
consists of an initial 3-min nonreinforcement period, a 9-min
reinforcement period, and a final 3-min nonreinforcement period. At 6 months, training sessions are one third shorter and
consist of an initial 2-min nonreinforcement period, a 6-min
reinforcement period, and a final 1-min nonreinforcement pe-
2 These are similar to the characteristics originally proposed by G.
Mandler (1985, 1989), although he eschewed the notion of multiple
memory systems.
3 Ironically, hippocampal lesion studies with rats and nonhuman primates are often cited as evidence for distinguishing implicit from explicit
memory (e.g., Zola-Morgan & Squire, 1984; for reviews, see Bachevalier, 1990; Nadel, 1994; Squire, 1987, 1992; and Zola-Morgan & Squire,
1985), and some have developed animal models of human amnesia
using a version of the delayed matching-to-sample task as the test of
recognition (Alvarez, Zola-Morgan, & Squire, 1994; Clower, AlvarezRoyo, Zola-Morgan, & Squire, 1991; Zola-Morgan & Squire, 1990).
Both practices were challenged by Olton (1989). The animal-model
approach commits the fundamental error of identifying a behavioral task
with an underlying process (cf. Jacoby, 1991 ).
470
ROVEE-COLLIER
riod. (The duration of the final nonreinforcement phases at each
age is too brief to permit extinction.) During each reinforcement
period (the acquisition phase), the infant's ankle is connected
to the mobile suspension hook (see Figure 1A), and kicks move
the mobile at a rate that is proportional to their vigor and rate
("conjugate reinforcement"; Rovee & Rovee, 1969). During
the nonreinforcement periods, the ribbon is moved to a second
empty hook while the mobile remains in place. In this arrangement, the infant can view the mobile but cannot activate it by
kicking. The nonreinforcement period at the outset of Session
1 is the baseline phase when the infant's unlearned kick rate
(operant level) is measured; the nonreinforcement period at the
end of Session 2 is the immediate retention test phase, when
the infant's final level of learning (kicks/minute) is measured
after zero delay. Only infants whose kick rate exceeded their
baseline rate by 1.5 times in 2 of 3 consecutive min during an
acquisition phase (the learning criterion) are subsequently tested
for retention.
All infants also receive a long-term retention test that is procedurally identical to the baseline and immediate retention test
phases. The long-term retention test lasts 3 min at 2 and 3
months of age and 2 min at 6 months of age. During the test,
a mobile that is either the same as or different in some way
from the training mobile is simply suspended over the infant
while the ankle ribbon is attached to an empty hook, and the
infant's kick rate is again measured. Following the long-term
test, reinforcement is reintroduced as a control procedure to
insure that infants who performed poorly during the test were
not unmotivated, fatigued, or ill at that particular time.
Infants " t e l l " us whether or not they recognize the test mobile
Figure 1. In A, the experimental arrangement in the mobile conjugate reinforcement paradigm during an
acquisition phase with a 3-month-old. The infant moves the mobile by using the ankle ribbon that is strung
to the hook suspending the mobile. During the delayed-recognition test, the arrangement is identical except
that the ribbon is attached to the "empty" stand. In B, the experimental arrangement during a reactivation
treatment with a 3-month-old. One end of the ribbon is attached to the mobile hook, and the other end is
drawn and released by an experimenter at the side of the crib. The infant seat minimizes incidental activity
during the procedure.
ON THE DEVELOPMENT OF MEMORY SYSTEMS
471
Figure 2. In A, schematic of the delayed-recognition task, training, and the long-term retention test (i.e.,
the delayed-recognition test). In B, schematic of the reactivation task, showing training, the reactivation
treatment, and the long-term retention test. The only difference between these tasks is the brief reactivation
(priming) treatment prior to the long-term retention test. The memory probe in A serves as the reminder
or memory prime in B, and the final long-term retention test is usually with the original training stimulus.
in terms of their responding during the long-term retention test.
If infants recognize the test mobile, then they say " y e s " by
kicking at a rate higher than their individual baseline rates; if
they do not recognize the test mobile, then they say " n o " by
not kicking above their individual baseline rates.
The Delayed-Recognition Task
In the delayed-recognition procedure, a specified amount of
time (e.g., from 1 min to 42 days at 3 months of age) is allowed
to elapse after the end of training, and then the long-term retention test, described above, is administered (see Figure 2A).
By using different types of retrieval cues as memory probes
after different delays during the delayed~recognition test, it is
possible to ascertain which attributes (e.g., attributes representing specific details or general features, individual features or
feature relations, the focal cue or the context, etc.) are accessible
in the original memory representation and which are not at
different points in time following original encoding. This strategy has revealed that infants forget different kinds of memory
attributes at different rates (Bhatt & Rovee-Collier, 1994, 1996,
in press; Boiler, Rovee-Collier, Gulya, & Prete, 1996; Muzzio &
Rovee-Collier, 1996; Rovee-Collier, Adler, & Borza, 1994;
Rovee-Collier & Sullivan, 1980; see also Riccio, Ackil, &
Burch-Vernon, 1992). Similarly, by using different types of retrieval cues as memory probes at different points in time following a reactivation treatment, we have determined that reminders
also recover different kinds of memory attributes at different
rates (Hayne & Rovee-Collier, 1995; Hitchcock & Rovee-Collier, 1996).
Although infants' operant levels do not change systematically
over the first 18 months of life, operant levels can vary considerably from one infant to another. Therefore, long-term retention
is measured in terms of two relative measures of individual
performance rather than absolute response rate. The primary
measure, the baseline ratio (B/P), indicates whether or not a
particular group exhibited retention. It expresses the extent to
which each infant's kick rate during the long-term retention test
( B ) exceeds that same infant's pretraining response rate during
the baseline phase (P). A mean baseline ratio significantly
greater than a theoretical population baseline ratio of 1.00 (i.e.,
no retention) indicates significant retention. The second measure, the retention ratio (B/A), provides information about the
degree of retention after delays at which retention was significant. This ratio expresses an infant's kick rate during the longterm retention test (B) as a fraction of the same infant's final
level of learning ( A ) , as measured during the immediate retention test at the end of training. A retention ratio of 1.00 or
greater indicates that performance is the same during the longterm test as it was at the end of training (i.e., no forgetting). A
mean retention ratio significantly less than a theoretical population retention ratio of 1.00 indicates significant forgetting.
The Reactivation Task
The reactivation task 4 is interpolated between training and
the long-term retention test (see Figure 2B) and is used to
4 The reactivation procedure was originally developed with animals
(Spear & Parsons, 1976) as a variant of the reinstatement procedure
(Campbell & Jaynes, 1966), and we adapted it for use in the mobile
paradigm (Rovee-Collier et al., 1980; Sullivan, 1982). The term reinstatement refers to the empirical manipulation of experimentally reinstating the external conditions of the original training event at the time of
reminding. (It is misused when a memory or a response is described as
"reinstated," e.g., Bauer, 1996). Reactivation refers to the theoretical
process by which an inactive or inaccessible memory is internally primed
or reactivated (Spear & Parsons, 1976). In the reinstatement procedure,
472
ROVEE-COLLIER
Table 2
Tasks that Produce Implicit-Explicit Memory Dissociations
in Adults and Corresponding Tasks Used With Infants
Memory system
Adult task
Infant task
Implicit
Explicit
Priming
Recognition
Reactivation
Delayed recognition
recover all or part of the original memory that has been forgotten
at the time it is administered. In this task, the infant is briefly
exposed to a memory prime or reminder (see Figure 1B) that
is a component of the original stimulus complex that was present
during training (e.g., the original mobile or the original context). The reminder presumably primes or reactivates the dormant or latent memory attributes, thereby increasing their accessibility. Whether or not the original memory attributes were
reactivated is confirmed later, during the long-term retention
test. If the reactivation procedure was successful, then infants
exhibit excellent retention on the ensuing test; if it was not
successful, then infants exhibit no retention, behaving as if they
had received no reminder at all.
During a reactivation treatment with a mobile reminder, the
infant is placed in a sling seat to minimize movement, and a
mobile that is either the same as or different from the training
mobile is suspended in front of the infant. One end of a ribbon
is then attached to the same hook as the mobile, and the other
end is held by the experimenter, who uses it to move the mobile
for 3 min (2 min at 6 months of age) noncontingently at the
same rate that the infant had previously kicked to move it in
each of his or her final 3 (or 2) min of training. In this way,
movement of the reminder mobile is phenomenologically equivalent to what each infant had witnessed during the final minutes
of acquisition. During a reactivation treatment with a context
reminder, the infant is simply placed in the crib or playpen for
3 (or 2) min in a context that is either the same as or different
from the context that was present during original training. In
both conditions, when the 3 (or 2) min have expired, the infant
is removed from the crib or playpen, and the reactivation treatment is over.
The ensuing long-term retention test is usually conducted
with the original mobile or in the original context. Under these
circumstances, a reminder that is novel differs from both the
training stimulus and the test stimulus; however, only the discrepancy between the reminder and the original training stimulus
is responsible for the infant's memory deficit on the subsequent
long-term retention test. My colleagues and I have repeatedly
shown that this deficit occurs because the novel reminder never
recovered the memory in the first place (Hayne & Rovee-Collier,
1995; Muzzio & Rovee-Collier, 1996; see Rovee-Collier &
Hayne, 1987, for review).
a partial training trial is periodically repeated throughout the retention
interval; in the reactivation procedure, an isolated component of the
original event (e.g., the cue, the context) is presented only once, at the
end of the retention interval.
Infant M e m o r y Tasks T h a t A r e A n a l o g o u s to I m p l i c i t
and E x p l i c i t M e m o r y Tasks U s e d W i t h Adults
The two different memory tasks that have been used with
preverbal infants are analogous to indirect and direct memory
tasks that have been used with adults (see Table 2). Specifically,
the reactivation task is analogous to the priming task that has
been used in studies of implicit memory with adults, where
priming is also thought to reactivate or increase the accessibility
of a memory representation. Likewise, the delayed-recognition
task corresponds to y e s - n o and o l d - n e w recognition tasks that
have been used in studies of explicit memory with adults. Even
though infants are widely believed to have only a single (implicit) memory system, these two infant tasks yield memory
dissociations that exactly parallel the memory dissociations that
are found with adult tasks and that are attributed to two (implicit
and explicit) memory systems.
Comparison of Priming and Reactivation Tasks
In studies with adults, priming tasks are described as implicit
memory tasks on which the effects of prior experiences are
manifested through changes in subsequent task performance
without the need for the conscious recollection of specific prior
episodes (Graf & Schacter, 1985 ). Priming refers to the facilitative effect on retention of the prior presentation of an item
(Tulving & Schacter, 1990). This facilitative effect is presumably mediated by a memory system separate from that involved
in performance on explicit or direct tests such as recall and
recognition. According to Vriezen et al. (1995),
A tacit assumption of a multiple memory systems account of priming is that the mere presentation and processing of an item is sufficient to leave a trace in the perceptual representation system
(Schacter, 1990, 1992; Tulving & Schacter, 1990). It is the reactivation of this trace on subsequent presentations that accounts for the
repetition priming effect" (p. 944).
In Jacoby's ( 1991 ) process-dissociation framework, priming
refers to the automatic or unintentional retrieval of previously
encoded information.
The reactivation task is based on observations that many
memories that are forgotten (i.e., individuals display no evidence of retention during a long-term retention test) can subsequently be recovered. Apparently, these memories remain available in the long-term store long after they can no longer be
accessed by the retrieval cues that are presented at the time of
the long-term retention test. The distinction between the availability and the accessibility of memories was originally made
by Tulving and Pearlstone (1966). Like priming tasks used with
adults, reactivation tasks are used with infants to reveal the
effects of prior experiences that otherwise would not be exhibited. These effects are also manifested through changes in subsequent test performance. In both priming and reactivation tasks,
participants are initially exposed to the target information. Subsequently, they receive a memory prime as a retrieval cue, followed by the retention test (a prior-cuing procedure; Spear,
1978).
The similarity between the priming task used with adults and
the reactivation task used with infants has been noted by several
ON THE DEVELOPMENT OF MEMORY SYSTEMS
researchers (J. M: Mandler, 1984; Naito & Komatsu, 1993; Nelson, 19955). Primes used with adults are thought to activate
either a preexisting memory representation (Tulving & Schacter,
1990) or a representation established by a single exposure to a
stimulus (Musen & Treisman, 1990), and they do so as the
result of a sin~gle,brief presentation (Naito & Komatsu, 1993).
The same is true of memory primes used with infants.
In addition, item-specific priming effects occur with adults
whether or not they actually recognize the item. Similarly, in
studies with infants, a reminder is presented only after infants
have forgotten the training memory--they do not recognize the
prime at the time it is presented. G. Mandler (1985, pp. 94-96)
described reminding in adults as a nondeliberate effort to recall
a previously experienced event. This characterization is equally
descriptive of reminding in infants. Not only is a reminder presented only after forgetting is complete, but also evidence that
it has recovered the forgotten memory at 3 months of age does
not surface until at least 8 hr after the reminder presentation,
and all of the memory attributes are not recovered until 72 hr
afterwards (Fagen & Rovee-Collier, 1983 ). At 6 months of age,
evidence that the reminder has recovered the forgotten memory
does not appear until 1 hr after the reminder presentation, and all
of the memory attributes are not recovered until 4 hr afterwards
(Boiler, Rovee-Collier, Borovsky, O'Connor, & Shyi, 1990).
This long recovery latency, even at 6 months, is evidence that
memory reactivation in infants occurs automatically, without an
active search component (BoUer et al., 1990; Fagen & RoveeCollier, 1983).6 That is, memory retrieval in reactivation tasks
cannot involve a motivated search process because infants have
no memory of what they might be searching for at the time they
are reminded.
Finally, for both infants and adults, effective primes are hyperspecific. In reactivation studies, only reminders that strike a
fairly veridical match with the original memory representation
can reactivate i t - - a generalized reminder is not effective (for
review, see Rovee-Collier & Hayne, 1987). Thus, for example,
if the mobile that is used as a reminder contains more than a
single object that was not present on the training mobile, then it
does not recover the memory, which remains forgotten (RoveeCollier, Patterson, & Hayne, 1985). This is one reason that
we view memory reactivation as a relatively pure, perceptual
identification task. Similarly, any change in the physical appearance of an item between study and testing reduces the amount
of priming for adults (Tulving & Schacter, 1990; for review, see
Richardson-Klavehn & Bjork, 1988). This veridicality requirement is consistent with propositions that relate involuntary, automatic processing on priming tests to brain mechanisms that
analyze perceptual information (Jacoby & Dallas, 1981; Musen & Treisman, 1990; Richardson-Klavehn et al., 1994; TuNing & Schacter, 1990; Vriezen et al., 1995).
This absolute veridicality requirement can be overridden by
reminding infants with a mobile on which a unique target item
is embedded in the midst of a number of homogeneous distractors. This type of stimulus array produces a perceptual phenomenon akin to visual pop-out in adults (Julesz, 1984; Treisman & Gelade, 1980; Treisman & Gormican, 1988) in that the
unique item captures the infant's attention. When this occurs,
infants treat the reminder mobile as if it were composed entirely
of items like the unique one, and the perceptual match is made
473
or not solely on the basis of a comparison between the unique
target and the contents of long-term memory (Rovee-Collier,
Bhatt, & Chazin, 1996; Rovee-Collier, Hankins, & Bhatt, 1992).
In adults, visual pop-out is viewed as a preattentive phenomenon
in which perceptual processing occurs automatically and in parallel, without focused attention (Treisman, 1988). The same
may be said of memory reactivation in infants.
Comparison of Recognition and Delayed
Recognition Tasks
Yes-no recognition tests (e.g., Dorfman, Kihlstrom, Cork, &
Misiaszek, 1995) and old-new recognition judgments (e.g.,
Mitchell & Brown, 1988; Musen & Treisman, 1990) are two
of the benchmark tasks used to index explicit memory in studies
with adults. The delayed-recognition task that is used in mobile
studies with young infants is analogous to these standard yesno and old-new recognition tasks. In both tasks, participants
initially study the designated material and then, after a predetermined retention interval has elapsed, are presented with a retrieval cue during the recognition test (a contemporaneous-cuing procedure; Spear, 1978).
McDonough (cited in B. Bower, 1995, p. 86) characterized
infants' memory performance in all mobile studies as "only
procedural" 7 because infants initially learn the recognition response during an operant conditioning procedure (see also
Bauer, 1996; Bauer & Hertsgaard, 1993; J. M. Mandler, 1984,
1990; Schacter & Moscovitch, 1984). The mobile training procedure, however, is used solely as a means of providing preverbal
infants with an alternative way to indicate whether or not they
recognize the test cue. Moreover, because they learn the response prior to the introduction of the different experimental
manipulations that distinguish the memory reactivation task
5 Nelson (1995) described memory performance on delayed-recognition tests in the mobile paradigm as visual recognition but did not
distinguish it from memory performance in a reactivation paradigm.
Although he drew a tentative analogy between responding in the mobile
task and classicallyconditionedleg flexion in studies with cats (Voneida,
Christie, Bogdanski, & Chopko, 1990) and rats (Caldwell & Werboff,
1962; Stehouwer & Campbell, 1978), he acknowledgedthat the analogy
might be inappropriate. Indeed, the mobile paradigm involves purely
voluntary responding rather than elicited or reflexive responding as in
classical conditioning, and infants' memory performance reflects the
informational content of the particular test display rather than a motor
skill, such as how to perform the target response.
The relatively protracted period between priming and recognition
in very young infants may reflect their lack of extensive networks of
associations that facilitate and speed processing in older children and
adults and the immaturity of central integrative pathways (including a
lack of myelinization) that speed memory processing and increase its
efficiency (see also Kesner, 1980). Given the sharp decrease in recognition latency following priming between 3 and 6 months of age, one
would expect recognition to become increasingly faster with age. It is
not surprising, therefore, that priming effects in adults are immediate.
7This description may reflect a misunderstandingof our procedure:
Bauer and Hertsgaard (1993) characterized "procedural memory" as
being evidencedby savings during relearning and cited infants' memory
performance in mobile studies as an example. However, savings are not
measured; the measure of long-term retention in mobile studies is taken
during a nonreinforcementperiod, hence it cannot reflect relearning.
474
ROVEE-COLLIER
from the delayed-recognition task, differential performance in
these two tasks cannot be attributed to how the response got
into the infant's behavioral repertoire in the first place. Even
verbally proficient children and adults at one time had to learn
the labels for the stimuli with which they are subsequently tested
in implicit and explicit memory tasks. Researchers give no
thought to how these verbal labels were initially acquired because that information is irrelevant in accounting for adults'
subsequent performance on implicit versus explicit memory
tasks. Whether the recognition response is verbal or motoric
or was initially acquired by using a conditioning procedure,
observation, or verbal instructions, the memory dissociations
exhibited by preverbal infants, children and adults with normal
memory, and individuals with amnesia on priming and recognition tasks are the same.
Independent Variables That Produce Task Dissociations
in Studies With Adults
Table 3 lists 13 independent variables that produce memory
dissociations on tasks commonly used to distinguish implicit
and explicit memory in studies with individuals with amnesia.
In the following, I present evidence that these same variables
produce the same dissociations in the memory performance of
very young infants, who presumably lack an explicit memory
system, on reactivation (priming) and delayed-recognition
tasks. The bulk of the infant data that are presented in this
section was compiled from numerous, separate studies that were
conducted in my laboratory and the laboratories of my former
students over the last 25 years. Those who would argue that the
evidence of infant memory dissociations that is presented next
reflects only dissociations within a single (implicit) memory
system cannot logically use evidence of these very same dissociations in adults with normal memory and those with amnesia
as support for the existence of two different memory systems.
Age
As Tulving ( 1991 ) put it, "The neural pathways that subserve
episodic remembering, maturing late in childhood and deterioTable 3
Summary of lndependent Variables and Their Effects on Adult
Performance in Implicit and Explicit Memory Tasks
Independent
variable
Effect on
implicit tasks
Effect on
explicit tasks
Age~
Retention interval
Vulnerability (interference)
Number of study trials
Study (exposure) time
Number of items studied
Level of processing
Spacing effects
Affect
Serial position
None
None
Limited
Small
None
None
None
None
Important
Transient or none
Studied size
Memory load
Context dependency
None
None
Less pronounced
Large
Large
Great
Large
Large
Large
Large
Large
Less important
Persistentprimacy
effect
Large
Large
Morepronounced
Subject variable.
rating early in old age, are not necessary for priming" (p. 16).
Proponents of multiple memory systems universally hold that
the order in which memory systems disappear in aging adults
and adults with brain damage predicts the order of their initial
appearance during infancy (Naito & Komatsuk, 1993;
Schacter & Moscovitch, 1984; Tulving & Schacter, 1990). This
hypothesis, originally proposed by John Hughlings Jackson to
describe the hierarchical development and dissolution of sensorimotor functioning (for review, see Rozin, 1976), states that
"the dissolution of mental function due to injury, disease, or
aging first involves those functions which are gained last in
ontogeny, while those functions preserved the longest are those
which appear earliest in childhood" (Campbell et al., 1984, p.
467).
Indeed, most studies of the effect of age on performance in
implicit and explicit memory tasks have found that older adults
are inferior to younger adults on tasks of explicit memory, but
they do not differ from younger adults on tasks of implicit
memory (for reviews, see Graf, 1990; Light & Lavoie, 1993;
and Mitchell, 1993). In all of these studies, age-related deficits
were found on tests of recognition and cued recall, but age
differences were either much smaller or absent altogether on
various single-item priming tests (e.g., Isingrini, Vazoiu, & Leroy, 1995; Java & Gardiner, 1991; Light & Albertson, 1989;
Light & Singh, 1987; Mitchell, Brown, & Murphy, 1990). Not
surprisingly, investigators working with individuals at the other
end of the age continuum have obtained the opposite pattern of
results. On tests of explicit memory with 3- to 11-year-olds and
young adults (Carroll, Byrne, & Kirsner, 1985; Greenbaum &
Graf, 1989; Mitchell, 1993; Naito, 1990), recall and recognition
were found to improve with age, but the amount of priming
was again virtually identical across ages. Finally, Bauer (1996)
reported that 13-, 16-, and 20-month-old infants reproduced an
increasing number of logically ordered events with age on an
immediate cued-recall test of deferred imitation, and Barr, Dowden, and Hayne (1996) reported that 18-month-olds produced
higher levels of deferred imitation after 24 hr than 12-montholds. Taken together, these studies suggest a pattern of memory
performance over the life span that is described by an inverted
U-shaped function for explicit memory tasks and a flat function
for implicit memory tasks (Mitchell, 1993).
As was the case with children and young adults, the memory
performance of preverbal infants studied in the mobile paradigm
also improves with increasing age on the delayed-recognition
task but not on the memory reactivation (priming) task. Figure
3 shows that the magnitude of infants' retention in a delayedrecognition test 1 week after training increased as a function of
age despite the fact that the final levels of acquisition were
equivalent at all ages (Hayne, 1990; Hill, Borovsky, & RoveeCollier, 1988; Rovee-Collier, 1984; Sullivan, Rovee-Collier, &
Tynes, 1979). The same figure also shows that the magnitude
of retention following a reactivation treatment that was administered 3 weeks after training was not affected by age (Davis &
Rovee-Collier, 1983; Hayne, 1990; Hill et al., 1988; RoveeCollier, 1984; Rovee-Collier, Sullivan, Enright, Lucas, & Fagen,
1980; Vander Linde, Morrongiello, & Rovee-Collier, 1985).
The dissociations in infants' memory performance in delayedrecognition and reactivation tasks are not unique to the mobile
conjugate reinforcement paradigm. Hartshorn and Rovee-Collier
475
ON THE DEVELOPMENT OF MEMORY SYSTEMS
.
[ ] Recognition
• Reactivation
.
.
1.C
0.c
0.~
.o
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0.E
¢D
n-
0..'
0.'~
Rovee-Collier, 1997; Hartshorn et al., in press). The combined
data from the mobile and train tasks show that the duration
of infants' retention in the delayed-recognition task increases
monotonically over the first 18 postnatal months (see Figure
4). There is no suggestion in these data that long-term memory
is suddenly enhanced at 8 - 9 months of age (Kagan & Hamburg,
1981 ), changes abruptly at the end of the 1st year when the
late-maturing memory system is thought to become functionally
mature (Schacter & Moscovitch, 1984), or differs during the
period of transition from receptive to productive language early
in the 2nd year. In contrast, the magnitude of retention following
a reactivation treatment remains the same over this same developmental period, irrespective of the particular task in which
the priming occurs (Hartshorn & Rovee-Collier, 1997; RoveeCollier et al., 1980; Sheffield & Hudson, 1994).
Retention Interval
0."
2
3
Age (Months)
6
Figure 3. Memory performance of 2-, 3-, and 6-month-olds on a delayed-recognition test (striped columns) 1 week after training and on a
reactivation test (filled columns) 3 weeks after training. (A retention
ratio of 1.00 or greater indicates no forgetting from the immediate to
the long-term test.) Asterisks mark groups that displayed retention (baseline ratio > 1.00). Data are from Borovsky & Rovee-Collier, 1990;
Davis & Rovee-Collier, 1983; Hill, Borovsky, & Rovee-Collier, 1988;
Rovee-Collier, 1984; Rovee-Collier, Griesler, & Earley, 1985; RoveeCollier, Sullivan, Enright, Lucas, & Fagen, 1980.
A basic observation o f human memory is that retention on
standard recognition, cued-recall, and free-recall tests declines
with the passage of time (Wickelgren, 1972; Woodworth,
1938). In contrast, priming effects are long-lasting in adults
and children with normal memory (Komatsu & Ohta, 1984;
Mitchell & Brown, 1988; Naito, 1990; Roediger & Blaxton,
1987; Tulving, Schacter, & Stark, 1982) and individuals with
amnesia (Schacter, Chiu, & Ochsner, 1993; Tulving, Hayman, &
Macdonald, 1991 ). q'hlving et al. (1982), for example, primed
adults with words and found that their memory performance on
a word-fragment completion test was stable over a period of 1
13
(1997) taught 6-month-olds how to move a miniature train
around a circular track by lever-pressing and obtained identical
delayed-recognition and reactivation data after the same test and
reminder delays described earlier (Figure 3) for 6-month-olds
who were studied in the mobile paradigm. Likewise, Sheffield
and Hudson (1994) obtained a parallel dissociation on cuedrecall and reactivation tests with 14- and 18-month-olds who
had been trained to perform six distinct activities during a single
visit to a laboratory playroom. On the cued-recall tests, 14month-olds forgot the initial training event sooner (after 8
weeks) than 18-month-olds (after 10 weeks). Once forgetting
was complete, all infants received a reactivation treatment during which the experimenter modeled three of the original six
activities. During the standard cued-recall test 24 hr later, infants
were tested for retention of the remaining (unmodeled) three
activities. This time, the magnitude of retention was equivalent
in the two age groups. Note that the latter dissociation on the
cued-recall and reactivation tests was identical to the dissociation that was obtained in mobile studies with younger infants,
despite the fact that the younger infants had learned to produce
the target response by means of a conditioning procedure,
whereas the toddlers were shown how to find and use the materials for each activity and then enacted those target responses.
Delayed recognition has now been tested in the train task
with independent groups of infants ranging from 6 through 18
months of age at the time of original encoding (Hartshorn &
12
..--t,0
11
10
9
cO
C
8
~
7
E
•-,
E
5
"~
4
~
3
C ~
2 3
M°bile?a?k,
6
. /
9
. . . . . . .
12
15
18
Age (Months)
Figure 4. The maximum duration, in weeks, of delayed recognition
(baseline ratio > 1.00) from 2 to 18 months of age. Independent groups
of infants were studied in the mobile ( 2 - 6 months) and the train ( 6 18 months) tasks. At 6 months of age, long-term retention was the same
irrespective of task. Data are from Hartshorn & Rovee-Collier, 1997;
Hartshorn et al., in press.
476
ROVEE-COLLIER
week, whereas their performance on a y e s - n o recognition test
declined over the same delay. Similarly, Musen and Treisman
(1990) found a perceptual priming effect that remained constant
across delays ranging from a few hours to 1 week, whereas
recognition declined significantly across the same period of
time. In the perceptual priming task, adults were briefly exposed
to a series of visual patterns that they had previously studied or
that were novel. After each exposure, they attempted to draw
the pattern just seen. The difference in accuracy between their
reproductions of previously studied and novel patterns was the
measure of implicit memory. Explicit memory was measured
by asking them to select which pattern of four alternatives they
remembered having studied. Finally, Mitchell and Brown
(1988) obtained a robust priming effect that remained stable
across delays ranging from 1 to 6 weeks on a picture-naming
task, whereas performance on an o l d - n e w picture-recognition
task declined over the same period.
The same pattern was obtained in two studies of deferred
imitation with toddlers. Bauer, Hertsgaard, and Wewerka (1995)
reported that the number of correctly ordered events produced
by 14-month-olds immediately following a verbal reminder (a
priming task) was approximately equivalent whether children
were tested after 1 week or after 1 month, but children's imitation performance on a cued-recall test decreased as the retention
interval increased from 1 week to 1 month. Hayne, MacDonald,
and Barr (in press) likewise reported that 12-month-olds exhibited significant deferred imitation after a 2-day delay but none
after a 2-week delay; they did not use a priming task.
In mobile studies with infants ranging in age from 2 through
6 months, performance in a delayed-recognition task is also
affected by the length of the retention interval, but performance
in a reactivation (priming) task is not. Figure 5, for example,
shows that the memory performance of 3-month-olds on a delayed-recognition test declined steadily with increases in the
training-test delay (Hayne, 1990; Rovee-Coilier et al., 1980;
Sullivan et al., 1979), but the magnitude of their retention 24 hr
after a reactivation treatment was the same whether the interval
between training and reminding was 2, 3, or 4 weeks (Hayne,
1990; Rovee-Collier et al., 1980). An identical result was obtained whether infants received one, two, or three reminders
(Hayne, 1990). Following a reactivation treatment, memory recovery appears to be an all-or-none phenomenon (see also Table
1, "Implicit m e m o r y " ) . Of the 9 infants reminded 5 weeks
after training, 4 exhibited perfect retention on the ensuing test,
whereas 5 exhibited none. The value of the 35-day test point in
Figure 5, which was not significantly above baseline, reflects
the averaging of these all-or-none data.
A similar dissociation was also found when 14- and 18month-olds were subsequently tested for their retention of six
different activities that they had originally performed during a
single session in a laboratory playroom. Their magnitude of
cued-recall progressively declined as the retention interval between the original enactment and testing increased (Hudson,
1994), but their magnitude of retention following a reactivation
treatment was the same whether the delay between training and
reminding was 8 weeks or 10 weeks (Sheffield & Hudson,
1994). It is noteworthy that the retention interval after which
toddlers remembered the original play activities in the cuedrecall test was virtually identical to the duration of delayed
1.4
Recognition
1.2
O
Reactivation
1.o
o~
n"
tO
0.8
t(9
(9
IT
0.6
0.4
0
1
I
4
8
=
J
12
•
i
.
16
T i m e Since
i
20
,
i
24
,
i
28
.
i
i
32
36
Training(Days)
Figure 5. Magnitude of delayed recognition or reactivation as a function of the retention interval for independent groups of 3-month-olds.
(A retention ratio of 1.00 indicates no forgetting from the immediate to
the long-term test.) Asterisks mark groups that displayed no retention
(baseline ratio not > 1.00). Data are from Hayne, 1990; Rovee-Collier,
Sullivan, Enright, Lucas, & Fagen, 1980.
recognition that we obtained for same-age infants in the train
task (see Figure 4), despite the fact that only in the latter task
was the target response originally learned through operant
conditioning.
Vulnerability
Although there is a rich tradition of research documenting
that adults' performance on explicit memory tasks is vulnerable
to interference (Barnes & Underwood, 1959; Postman & Underwood, 1973 ), evidence that performance on implicit memory
tasks is relatively insensitive to interference is more recent
(Graf & Schacter, 1987; Sloman, Hayman, Ohta, Law, & Tulving, 1988; Tulving, 1983). Priming on word-fragment (Sloman
et al., 1988), word-completion (Graf & Schacter, 1987), and
lexical decision (Bentin & Moscovitch, 1988) tasks, for example, is unaffected by the same interference manipulations that
produce memory impairment on recognition, cued-recall, and
free-recall tests.
A similar dissociation has been observed infants' memory
performance on delayed-recognition and reactivation tasks.
When 3-month-olds were trained with one mobile in Session 1
and with a different mobile in Session 2, they failed to recognize
the Session 1 mobile in a delayed-recognition test 24 hr l a t e r - a classic example of retroactive interference (Fagen, Morrongiello, Rovee-Collier, & Gekoski, 1984). This retroactive interference effect occurred even when infants were trained with a
particular mobile for a total of 30 min over 2 successive days
and then, immediately after training was over, they merely
v i e w e d - - f o r only 3 m i n - - a novel mobile that was being moved
by the experimenter. These infants, like those in the Fagen et al.
(1984) study, also failed to recognize the original mobile during
ON THE DEVELOPMENT OF MEMORY SYSTEMS
a delayed-recognition test 24 hr later (Rovee-Collier, Borza,
Adler, & Boiler, 1993). At 6 months of age, infants were trained
with one mobile for two sessions and then were passively shown
the novel mobile for only 2 min after delays ranging from 1 to
13 days following the second training session. Even after the
longest exposure delay, infants were still unable to recognize
the original mobile on the ensuing delayed-recognition test. In
contrast, infants with no interpolated exposure exhibited nearperfect retention on the long-term test after the same retention
interval (Muzzio & Rovee-Collier, 1996).
The retroactive interference exhibited by infants in the delayed-recognition task is not limited to instances in which they
are exposed to a different mobile between training and testing.
A similar result was obtained when infants were trained with
the same mobile in a different context in each of two sessions
and were then tested for recognition of the mobile in the original
(Session 1 ) context. At both 3 months (Rovee-Collier & DuFault, 1991 ) and 6 months (Amabile & Rovee-Collier, 1991 ),
training in a second context impaired infants' ability to recognize the original mobile in the original training context during
a delayed-recognition test 24 hr after Session 2. Retroactive
interference also occurred when 3-month-olds (A. RossiGeorge, unpublished observations, April 8, 1996) and 6-montholds (Boiler & Rovee-Collier, 1992) were trained in the same
context for 2 days and then were simply exposed to a novel
context immediately after training was over. Infants again could
no longer recognize the training mobile in the original context
during the 24-hr test (see Figure 6, left panel); instead, they
now recognized the original mobile only in the briefly exposed
context.
In contrast to the susceptibility of infants' delayed recognition
to retroactive interference, a reactivated memory is relatively
impervious to retroactive interference by new information that
is interpolated between the reactivation treatment and testing.
Using the same exposure condition that impaired 6-month-olds'
recognition of the original mobile in the original context (Figure
6, left panel), we were unable to impair their reactivated memory by exposing them to a new context after a reactivation
treatment (Boiler & Rovee-Collier, 1994). Whether infants were
exposed to the novel context immediately after a reactivation
treatment or after delays that ranged from 15 rain to 24 hr, they
continued to recognize the mobile only in the original context
(see Figure 6, right panel) and never recognized it in the exposed one.
Number of Study Trials
In studies with adults, recognition improves as the number
of study trials or stimulus presentations increases, but the number of study trials has little or no effect on priming. Musen and
Treisman (1990), for example, gave adults visual patterns to
study for 3 s each; after each pattern was removed, they were
allowed to rehearse it for 7 s before the next pattern was presented. After this initial study period, some participants were
again exposed to the sequence of patterns four times (each
pattern was reexposed for only 1 s), whereas others received
only the initial study trial. Explicit memory was measured in a
fixed-choice recognition test in which participants indicated
which one of the four test stimuli they had previously studied.
1.3
Recognition
*
477
Reactivation
1.2
1.1
~k
._o
nr
t--
0.9
o
t"
0.8
I'r
"'"
0.7
%x\
0.6
~
~,.,\
\N\
0.5
x~
None
Interference
None
Exposure Groups
Interference
Figure 6. Magnitude of delayed recognition (left panel) i day after
training and magnitude of reactivation (right panel) 3 weeks after training at 6 months of age. Groups either were exposed to a novel context
between training or reminding and testing (Interference) or were not
(None) and were tested in the original training context. (A retention
ratio of 1.00 indicates no forgetting from the immediate to the longterm retention test.) Asterisks mark groups that displayed retention
(baseline ratio > 1.00). Data are from Amabile & Rovee-Collier, 1991;
Boiler & Rovee-Collier, 1994.
Implicit memory was measured in a perception test in which
studied patterns and distractor patterns were presented singly,
followed by a mask, and participants were instructed to draw
what they had just seen; the priming effect was determined
by comparing performance on the old and the new patterns.
Individuals in both the repeated- and the single-trial conditions
were tested immediately after the first session and 8 days later.
In addition, some individuals in the repeated-trials condition
were tested in a second session 1 to 3 hours after their first.
Musen and Treisman found that the number of study trials had
a negligible effect on priming whether testing occurred later on
the same day or after an 8-day delay. In contrast, the decline in
recognition accuracy was almost three times greater in the single-trial group than in the repeated-trials group after the 8-day
delay.
Studies using more conventional verbal materials with adults
similarly found that increasing the number of massed repetitions
beyond a single presentation had little or no effect on priming in
implicit tests (e.g., word-fragment completion) but significantly
improved performance on recall and recognition tests (Challis &
Sidhu, 1993). In a study of deferred imitation with 14-montholds, Bauer et al. (1995) similarly found that performance on
an explicit memory test was dramatically improved by additional trials. Infants received either one or three trials, and their
ability to reproduce ordered events was assessed either 1 week
or (for the three-trial group only) 1 month later. After a single
trial, toddlers exhibited excellent cued recall after 1 week but
478
ROVEE-COLLIER
poor cued recall after 1 month; after three trials, toddlers performed as well after 1 month as those with only one trial had
performed after l week.
In mobile studies, the number of training trials also has a
differential effect on memory performance on delayed-recognition and reactivation tests. At 3 months, each additional training
trial (session) prolonged delayed recognition by 1 week (see
Figure 7, left panel; Ohr, Fagen, Rovee-Collier, Hayne, & Vander
Linde, 1989) but did not affect the magnitude of reactivation 3
weeks after training was over (see Figure 7, right panel; Greco,
Hayne, & Rovee-Collier, 1990; Rovee-Collier et al., 1980). The
same effect was found at 6 months of age; increasing the number
of training sessions from one to two prolonged delayed recognition from 1 week (K. Boller, unpublished observations, June 2,
1996) to 2 weeks (Hill et al., 1988), but the magnitude of
reactivation 3 weeks later was unaffected by whether infants
were trained for two sessions (Borovsky & Rovee-Collier,
1990), three sessions (Gulya & Rovee-Collier, 1996), or four
sessions (Timmons, 1994). The magnitude of reactivation was
also not affected by the number of reactivation treatments.
Hayne (1990), for example, found that the magnitude of reactivation 3 weeks after training was identical whether 3-montholds received one, two, or three reminders.
The retention advantage of a greater number of trials was
observed even when the total amount of training time was held
constant over trials. Vander Linde et al. ( 1985 ) trained 2-montholds in the mobile task for either one 18-min trial or three
6-min trials that were separated by 24 hr. During a delayedrecognition test 3 weeks later, infants whose training time was
distributed across three trials exhibited near-perfect retention,
whereas infants whose training time occurred within a single
session exhibited none after the same delay.
Spacing Effects
In studies with adults, superior performance on tests of recall
and recognition is a common result when study trials are distributed instead of massed (for reviews, see R. L. Cohen, 1985;
Figure 7. The effect of number of training sessions at 3 months on
the magnitude of delayed recognition (left panel) after different delays
and the magnitude of reactivation (right panel) 3 weeks after training.
Asterisks mark groups that exhibited retention (baseline ratio > 1.00).
Data are from Greco, Hayne, & Rovee-Collier, 1990; Ohr, Fagen, RoveeCollier, Hayne, & Vander Linde, 1989; Rovee-Collier, Sullivan, Enright,
Lucas, & Fagen, 1980.
Crowder, 1976). In contrast, spacing effects on priming tests
are inconsistent and small (e.g., Challis & Sidhu, 1993; Jacoby & Dallas, 1981; Perruchet, 1989). Although Greene
(1990) found a spacing effect on a perceptual identification test
under intentional learning instructions, the effect disappeared
when leaming was incidental or when the spacing was manipulated between study lists. Jacoby ( 1978; Cuddy & Jacoby, 1982)
attributed the retention advantage of spaced study on explicit
tests to the greater processing that is required for successful
retrieval when successive repetitions are further apart. Assuming
that each trial or presentation of an item initiated retrieval of
the memory of its prior presentation, he proposed that when
trials were massed, retrieval was trivial and required little processing; when the interval between successive trials was greater,
retrieval was more difficult, and more processing was involved.
Bjork and his colleagues (M. C. Anderson, Bjork, & Bjork,
1994; Bjork, 1975; Schmidt & Bjork, 1992) similarly attributed
the retention advantage of spaced study trials to the greater
retrieval difficulty associated with the greater amount of time
since the last retrieval. In a classic study (Landauer & Bjork,
1978), adults learned a number of names or name-picture associations during a single study session in which each item was
presented once. They then received three or four cued-recall
tests, and the intervals between succeeding tests were filled with
different numbers of names. Retention was poorest when test
items were massed (no intervening names), better when four
or five items intervened between successive tests, and best when
the number of items between successive tests increased progressively. They concluded that the expanding series of interitem
intervals permitted adults to practice retrieval under increasingly
difficult conditions. Rea and Modigliani ( 1985 ) similarly found
that children's recall of multiplication facts and spelling lists
was significantly enhanced by an expanding series of practice
tests.
In mobile studies, at both 2 months (Vander Linde et al.,
1985) and 3 months (Rovee-Collier, Evancio, & Earley, 1995),
the magnitude of delayed recognition 8 days after Session 1 was
significantly greater when the interval between two successive
sessions was 2 days than when it was 1 day. At 3 months, when
the intersession interval was 4 days, however, infants exhibited
no recognition at all on the 8-day test. This result was interpreted
in terms of the time window construct (Rovee-Collier, 1995),
which holds that there is a limited period of time following an
initial event (Session 1 ) within which subsequent information
(Session 2) can be integrated with the memory representation
of the initial event. Information that is encountered after the
time window has shut is not integrated with the initial event but
is treated as unique, that is, as if it had been encountered for
the first time. In the study with 3-month-olds, the time window
for integrating two successive training sessions apparently shut
after 3 days (see Figure 8, left panel). The magnitude of reactivation 15 days after Session 1, however, was the same whether
the two training sessions were spaced by 1 day or 2 days. When
the two sessions were spaced by 4 days (i.e., Session 2 was
outside of the time window), however, the reactivation treatment
was not effective (see Figure 8, right panel).
Muller and Rovee-Collier (1996) trained 3-month-olds for
three sessions but programmed them such that successive intersession intervals (ISis) were in an expanding series (Days 0 -
ON THE DEVELOPMENT OF MEMORY SYSTEMS
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Figure 8. The effect of spacing between successive training sessions
(Session 1 = Day 0; Session 2 = Day 1, 2, or 4) on the magnitude of
delayed recognition (left panel) 8 days after Session 1 and the magnitude
of reactivation(right panel) 15 days after Session 1 at 3 months of age.
Asterisks mark groups that displayed retention (baseline ratio > 1.00).
Data are from Rovee-Collier & DuFault, 1991; Rovee-Collier, Evancio, & Earley, 1995.
2 - 8 ) or in a constant series (Days 0 - 4 - 8 ) . Although the mean
ISI was the same (4 days) for both groups, the second training
session was again either inside (Day 2) or outside (Day 4) the
time window for the integration of two training sessions. As in
studies with adults and children, training infants with an expanding series of ISis prolonged retention on the explicit test.
Although 3-month-olds who were trained on 3 successive days
(Days 0 - 1 - 2 ) exhibited significant recognition 2 weeks after
their final session but not 3 weeks afterward (Ohr et al., 1989),
infants who were trained for three sessions in an expanding
series exhibited significant recognition 3 weeks after their final
session (i.e., 29 days after Session 1 ) but not 4 weeks afterward.
In contrast, the constant-series training group failed to recognize
the training mobile 1 week after its final session, even though
this group had received three training sessions.
In another study (Rovee-Collier, Greco-Vigorito, & Hayne,
1993), 3-month-olds were trained for three sessions and then
were shown a novel moving object either immediately after
training was over (when the time window opened) or 4 days
later (at the end of the time window, which closes after 4 days
with three training sessions). Infants who were exposed to the
object at the beginning of the time window recognized it for
only 4 days, but infants who were exposed to the object at the
end of the time window recognized it for 10 additional days.
Although the delay between training and exposure to the novel
object affected infants' magnitude of delayed recognition after
a retention interval of 1 day, it had no effect on their magnitude
of reactivation after a retention interval of 3 weeks (see Figure
The total time hypothesis is a widely accepted principle in
human memory. It states that the degree to which an item is
recalled is a direct function of its total study time, irrespective
of the manner in which that time is distributed (R. L. Cohen,
1985; Cooper & Pantie, 1967; for review, see Crowder, 1976).
The amount of perceptual processing that can be completed at
the time of encoding is also constrained by the length of time
a stimulus is physically available to the perceiver; as its exposure
time increases, the perceiver should be able to extract more
perceptual information from the stimulus. In studies with adults,
neither study time nor stimulus exposure time affects measures
of implicit memory, but both affect measures of explicit memory. For example, Von Hippel and Hawkins (1994, Experiment
1 ) measured retention in three implicit tasks (word-fragment
completion, perceptual identification, and general knowledge)
and found that increasing stimulus exposure time had no effect
on implicit conceptual memory performance when the encoding
task focused on the perceptual features of the stimulus. Other
researchers have also reported that increasing stimulus exposure
time has no effect on performance in either a perceptual identification task (Jacoby & Dallas, 1981 ) or a word-fragment completion task (Neill, Beck, Bottalico, & Molloy, 1990) but improves performance in explicit memory tasks (Debner & Jacoby,
1994; Jacoby & Dallas, 1981; Neill et al., 1990), including the
free recall of word lists (Roberts, 1972a).
Figure 9. The effect of the timing of a brief posttraining exposure to
a novel object on the magnitude of delayed recognition of that object
(left panel) 1 day after the exposure and on the magnitudeof reactivation
(right panel) 3 weeks after training at 3 months of age. (A retention
ratio of 1.00 indicates no forgetting.) Asterisks indicate that all groups
displayed retention (baseline ratio > 1.00). Data are from Greco,
Hayne, & Rovee-Collier,1990; Rovee-Collier,Greco-Vigorito,& Hayne,
1993.
480
ROVEE-COLLIER
Using nonverbal stimulus materials, Schacter, Cooper, Delaney, Peterson, and Tharan ( 1991 ) exposed adults to either single
or multiple presentations of visual objects and measured their
memory performance in an object decision task (a test of implicit memory). When the exposure duration was 5 s, a single
exposure was as effective as multiple exposures in facilitating
priming. When the exposure duration was reduced to 1 s, however, multiple exposures led to significant priming, but a single
exposure did not. When Musen (1991) increased the duration
of a single exposure of a novel visual figure from 1 s to 10 s,
however, she found that performance on a priming task was
not affected, but recognition performance was significantly
enhanced.
In a deferred-imitation study with preverbal infants, Barr et
al. (1996) exposed 6-month-olds to a demonstrator modeling a
sequence of three actions on a hand puppet for 30 s. They found
no evidence of deferred imitation after a 24-hr delay, but infants'
deferred imitation immediately after training was excellent.
When they increased the stimulus exposure period from 30 to 60
s, however, infants' 24-hr deferred imitation was also excellent.
In mobile studies with infants, increasing the study time similarly enhances performance on a delayed-recognition test. Twomonth-olds who were trained for 12 min in a single session, for
example, failed to recognize the mobile after 1 week, but their
recognition was excellent after that delay when they were
trained for 18 min (Rovee-Collier, 1984; Vander Linde et al.,
1985). At 3 months, infants trained for a single session lasting
6 or 9 rain failed to recognize the original mobile 1 week later,
but with a 12-rain session, they recognized it for 1 week, and
with an 18-min session, they recognized it for 2 weeks (see
Figure 10; Ohr et al., 1989).
Figure 10. The effect of study time (session duration) on the magnitude of delayedrecognitionof independentgroups of 3-month-oldstested
7, 14, or 21 days later. Asterisks mark groups that displayed retention
(baseline ratio > 1.00). Data are from Ohr, Fagen, Rovee-CoUier,
Hayne, & Vander Linde, 1989.
In another manipulation of stimulus exposure time, 3-montholds were trained with a particular mobile for two sessions and
then were merely exposed to a novel mobile for either 120 s or
10 s immediately after training was over. On a delayed-recognition test 24 hr later, the 120-s exposure interfered with infants'
ability to recognize the original mobile and led them to treat
the briefly exposed mobile as if they had been trained with it
instead (Rovee-Collier, Borza, et al., 1993); the 10-s exposure
produced the same interference effect after 1 hr but not after 24
hr (Bhatt, 1997). No reactivation (priming) data pertaining to
exposure duration are available.
Number of Studied Items
G. Mandler (1985) characterized nonautomatic memories as
capacity demanding and distinguished them from automatic
memories with no capacity demand. Although he rejected the
explicit-implicit memory distinction, similar differences in capacity demand have been found to affect performance in explicit
and implicit memory tasks, respectively. In studies with adults,
increasing the number of studied items decreases performance
on explicit memory tasks but does not affect performance on
implicit memory tasks. Adding new items to a study list impairs
adults' retention in free-recall, cued-recall, and recognition tasks
(Atkinson & Joula, 1973; Ratcliff & Murdock, 1976; see
Crowder, 1976~ for review). Reinitz and Demb (1994), for
example, had college students study a list of compound words
and then tested them on either an old-new recognition test or a
perceptual identification test with old words, recombined words,
compound words in which either the first or second parts were
new, and completely new words. On the recognition test, the
number of false recognitions increased with the number of studied components. On the perceptual identification task, however,
priming occurred only for old words; identification of the other
test items was poor, irrespective of the number of previously
studied components. Mitchell and Brown (1988) similarly
found that the magnitude of repetition priming was not affected
by the number of studied items, or list size.
In a mobile study with 2- and 3-month-old infants, the number
of studied items was defined in terms of the number of different
types of blocks on the training mobile; all five mobile blocks
were identical, or each was different (Rovee-Collier, Earley, &
Stafford, 1989). At both ages, performance on a 24-hr delayedrecognition test was better when the list was shorter (i,e., when
the five objects were identical; see Figure 11, left panel), but
the magnitude of reactivation 3 weeks after training was unaffected by the number of studied items at 3 months of age (see
Figure 11, right panel). Reactivation data for 2-month-olds are
not available.
Likewise, Merriman, Rovee-Collier, and Wilk (in press)
trained 6-month-olds with an ordered "list" of three mobiles
for three successive sessions. T~venty-four hours after their final
training session, infants recognized the test mobile from Serial
Position 1, but they did not recognize the mobiles from Serial
Positions 2 and 3 - - a classic primacy effect. They also discriminated a novel mobile as not on the study list. Because independent groups were tested with only a single mobile from a given
serial position (a serial-probe recognition procedure), we hypothesized that infants might have learned both item and order
ON THE DEVELOPMENT OF MEMORY SYSTEMS
481
reactivation task, 24 hr after priming (Bhatt & Rovee-Collier,
in press).
Level o f Processing
Figure 11. The effect of the number of different objects (studied items)
on the training mobile on the magnitude of delayed recognition 1 day
after training (left panel) and the magnitude of reactivation (right panel )
3 weeks after training at 2 and 3 months of age. (A retention ratio of 1.00
indicates no forgetting.) Asterisks mark groups that displayed retention
(baseline ratio > 1.00). Data are from Davis & Rovee-Collier, 1983;
Greco, Hayne, & Rovee-Collier, 1990; Hayne, 1990; Rovee-Collier,
Earley, & Stafford, 1989; Rovee-Collier, Hankins, & Bhatt, 1992.
information during training but failed to recognize the test mobiles from Serial Positions 2 and 3 because the single test stimulus provided no order information. In a follow-up study (Gulya & Rovee-Collier, 1996), when the number of mobiles on
the list was increased from three to five, the primacy effect
disappeared. Instead, infants now recognized mobiles from all
serial positions on the study list during a delayed-recognition
test 24-hr later (see Figure 12) and again discriminated a novel
mobile as not on the study list. Presumably, infants failed to
learn order information when the list was longer, and therefore
it no longer interfered with their recognition of the items from
the middle and last serial positions. This result again demonstrates that infants' memory performance on a delayed-recognition test is affected by the number of items on the study list.
Finally, infants' delayed recognition was also impaired when
the number of studied features and feature relations on the training mobiles was increased. Three-month-olds were trained with
a six-block mobile displaying either two feature sets with three
feature combinations each (three blocks per set) or three feature
sets with three feature combinations each (two blocks per set).
In the two-set condition, three training blocks displayed red As
on a black ground and three blocks displayed green 2s on a
yellow ground; in the three-set condition, two training blocks
each displayed the preceding combinations as well as brown Xs
on a blue ground. During the 24-hr delayed-recognition test,
two features from the original combinations (figure, figure color,
or ground color) were exchanged between the sets (e.g., a figure-color recombination would yield green As on a black ground
and red 2s on a yellow ground). Infants discriminated recombinations of all features when trained with two feature sets but
not with three feature sets (Bhatt & Rovee-Collier, 1994, in
press). Thus, they remembered "what went with what" 24
hours later only when the number of features and feature relations was smaller. Even though infants had failed to discriminate
feature recombinations from the three-feature set in the 24hour delayed-recognition task, they did discriminate all feature
recombinations from the three-feature set 3 weeks later in the
Level of processing (LOP) is an encoding variable that is
widely thought to affect performance differently on implicit and
explicit memory tasks. In their original exposition, Craik and
Lockhart (1972) suggested that the duration of a memory was
determined by the level or depth at which the perceptual input
for that memory was processed. Thus, the shallower processing
of phonemic and orthographic features (e.g., searching for specific letters in a word) should lead to a shorter duration of
retention, whereas the deeper processing required by the generation of a verbal associate or a semantic-orienting task (e.g.,
rating the pleasantness of words on a study list) should lead to
a longer duration of retention. Over time, other accounts of
observed retention differences as a function of encoding difficulty were advanced. Craik and Tulving (1975), for example,
attributed retention differences to the degree of stimulus elaboration instead of to differences in processing depth during encoding, retaining the term depth to refer to the degree of semantic
involvement. Others introduced terms such as meaningfulness,
differentiation, integration, distinctiveness, and so forth (for
review, see Tulving, 1983) in attempts to explain encoding difficulty in terms of a single factor.
In memory studies with adults, manipulations of LOP produce strong effects on explicit tests but no effects on implicit
tests (Graf, Mandler, & Haden, 1982; Graf, Squire, & Mandler,
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Figure 12. The 24-hr delayed-recognition performance of independent
groups of 6-month-olds tested with mobiles from the first, middle, and
last serial positions of a three-mobile list (left panel) and a five-mobile
list (right panel). Infants trained with both lists failed to recognize (i.e.,
they discriminated) a novel test mobile. Asterisks mark groups that
displayed retention (baseline ratio > 1.00). Data are from Gulya &
Rovee-Collier, 1996; Merriman, Rovee-Collier, & W i l l in press.
482
ROVEE-COLLIER
1984; Moscovitch, 1994; Roediger, Weldon, Stadler, & Riegler,
1992). One of the earliest demonstrations of this dissociation
was reported by Jacoby and Dallas ( 1981 ). They asked college
students to answer three yes-no questions about each word on
a long list and then assessed their retention on either a perceptual
identification task or a recognition task. The shallow-encoding
condition included questions about the letters in the word and
a rhyme question; the deep-encoding condition questions concerned the meaning of the word. Initially, each question appeared
briefly on a screen and then was replaced by the target word,
which remained on the screen until the question was answered.
During the recognition test, students responded "yes" to words
that had been presented in the first phase and " n o " to those
that were new. During the perceptual identification test, words
were simply flashed on the screen, and students reported each
word immediately. Jacoby and Dallas found that the semantic
question had longer reaction times than the other two questions,
and " n o " responses took longer than "yes" responses. On
the recognition memory test, the probability of a correct word
identification was significantly higher for semantic questions
and questions requiring a "yes" response; on the perceptual
identification test, however, neither the type of question nor
whether it required a "yes" or " n o " answer affected the probability of correctly identifying a word. Although they found no
effect of LOP, presentation of a word in the first phase did
produce a significant priming effect in the second phase: Perceptual identification was significantly enhanced when test items
were old. Moreover, the amount of priming was the same
whether recognition memory was poor or near perfect.
An example of the dissociation produced by LOP manipulations in a developmental study was reported by Carroll et al.
(1985). They presented a list composed of pictures to 5-, 7-,
and 10-year-olds and a group of adults, instructing participants
either to search for pictures marked with a cross (the shallowencoding condition) or to judge the weight of the objects that
were pictured (the deep-encoding condition). At each age, performance was measured on both a recognition test and a naming
test. As expected, recognition improved with age. In addition,
priming was unaffected by either age or encoding condition, but
picture recognition was better in the deep than in the shallowencoding condition. In three experiments with elementary school
children and young adults, Naito (1990) similarly found no
effect of either age or LOP on priming in a word-completion
task, but recall increased with age and a deeper LOP.
In three experiments, we have obtained robust effects of LOP
on infants' performance in a delayed-recognition task (Adler,
Gerhardstein, & Rovee-Collier, in press). In all experiments,
attention during encoding was manipulated by training 3-montholds with a pop-out display composed of a unique target (e.g.,
L) amidst six distractors (e.g., +s). (A pop-out display is
thought to enhance attention to the target at the expense of
attention to the distractors.) In Experiment 1, infants tested after
a 24-hr delay with a homogeneous mobile composed entirely
of targets or distractors recognized both the original target and
the original distractors, confirming that both had been encoded
during training. In Experiment 2, infants who were trained with
the same pop-out mobile recognized Ls (the original target)
after delays more than twice as long as controls who were
trained with a mobile composed entirely of Ls; conversely, they
recognized Ls (the original distractors) after a delay less than
half as long as controls who were trained with a mobile composed entirely of Ls (see Figure 13). Finally, Experiment 3
replicated the retention advantage gained by enhancing infants'
attention during training with a pop-out mobile with +s. These
results were consistent with adult findings that increasing attention to an item during encoding increases its depth of processing
and protracts its retention on an explicit memory task. Reactivation data for the implicit task are not available.
Affect
Most of the research on the role of affect in retention has
focused either on the congruence of the mood during encoding
and retrieval or on the congruence between the nature of the
mood at the time of retrieval and the nature of what is retrieved
(e.g., G. H. Bower, 1981; Eich, Macaulay, & Ryan, 1994; for
review, see Blaney, 1986). Recently, researchers have begun to
explore the contribution of affect to memory performance on
implicit and explicit tests (Denny & Hunt, 1992; Hertel & Hardin, 1990; Macaulay, Ryan, & Eich, 1993; Watkins, Mathews,
Williamson, & Fuller, 1992). Research with both adults with
normal moods and adults with affective disorders has demonstrated that performance on explicit tests is sensitive to affect,
but performance on implicit tests is not (Tulving, 1983).
Hertel and Hardin (1990) queried college students who were
not depressed (scores < 6 on the Beck Depression Inventory
[BDI] ; Beck, Ward, Mendelson, Mock, & Erlbaugh, 1961 ) and
who were naturally depressed (BDI scores > 6 and < 9 ) about
the uncommon meanings of homophones, gave them depressiveor neutral-mood inductions, and then tested both their spelling
(an implicit task) and their recognition of old and new homophones. Neither induced nor naturally occurring depression affected spelling, but both impaired recognition of the old homophones. Watkins et al. (1992) assessed memory for affectively
valenced words with adults who were clinically diagnosed with
major depression or dysthymia (BDI scores > 19; mean BDI
score = 27.53) or were not depressed (BDI scores > 8, mean
BDI score = 3.71 ). Relative to who were not depressed, performance of adults who were depressed on a cued-recall test was
impaired, but the two groups performed equivalently on a wordcompletion test. Similarly, Denny and Hunt (1992) found that
the free recall of affectively valenced words was impaired in a
patient population of individuals who were clinically depressed
relative to adults who were not depressed, but the two groups
performed equivalently on a word-fragment completion test.
In mobile studies with 3-month-olds, Fagen and his colleagues
have repeatedly found that infants' delayed recognition is highly
sensitive to affect, but their memory performance in a reactivation task is not (for review, see Fagen & Prigot, 1993). In these
studies, infants were typically trained for two sessions with a
10-object mobile and then were shifted to a nonpreferred 2object mobile during a final session. In response to the shift,
approximately 50% of the infants usually cried. During delayedrecognition tests either 1 day or 1 week later, infants who did
not cry exhibited excellent retention irrespective of whether they
were tested with the 10-object or 2-object mobile, whereas infants who cried recognized the test mobiles after a 1-day reten-
ON THE DEVELOPMENT OF MEMORY SYSTEMS
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Retention Interval (Days)
Figure 13. The level-of-processing effect at 3 months of age, shown as the protracted recognition over
days of +s (left panel) and Ls (right panel) when they were the target (white columns) on the pop-out
training mobile. Also shown is the maximum duration of retention of control groups (striped columns) who
were trained with a homogeneous + or L mobile, respectively, and the diminished recognition over days of
+s and Ls when they were the distractors (dark columns) on the L or + pop-out training mobile, respectively.
The corresponding control group for the distractors was trained with a homogeneous mobile displaying the
same character as the distractor. (A retention ratio of 1.00 indicates no forgetting.) Asterisks mark groups
that displayed retention (baseline ratio > 1.00). Data are from Adler, Gerhardstein, & Rovee-Collier, in
press; Adler & Rovee-Collier, 1994.
tion interval but not after a 1-week delay (Fagen, Ohr, Singer, &
Klein, 1989; see Figure 14, left panel). Despite the impaired
performance of infants who cried on the 1-week delayed-recognition test, when a reactivation treatment was administered 3
Figure 14. The effect of crying on the magnitude of delayed recognition 1 day or 7 days after training (left panel) and the magnitude of
reactivation (right panel) 3 weeks after training at 3 months of age.
Asterisks mark groups that displayed retention (baseline ratio > 1.00).
Data are from Fagen, Ohr, Fleckenstein, & Ribner, 1985; Fagen, Ohr,
Singer, & Klein, 1989.
weeks after the conclusion of training, all infants exhibited the
same magnitude of reactivation 1 day later whether they had
cried after a mobile shift or not (see Figure 14, right panel;
Fagen, Ohr, Fleckenstein, & Ribner, 1985).
Singer and Fagen (1992) repeated this procedure but used a
measure of infants' facial expressions of affect (AFFEX; Izard,
Dougherty, & Hembree, 1980) in addition to crying. Following
the shift to the 2-object mobile, infants who cried exhibited
decreasing amounts of interest expressions and increasing
amounts of anger and sadness expressions. During the 1-day
recognition test, infants who cried again displayed significantly
more anger expressions than infants who did not cry, but during
the 7-day recognition test, they displayed none. In addition to
providing a convergent measure of affect, these data confirmed
that the poor performance of infants who cried during the 1week test was not simply a result of their refusal to participate
in the task but an instance of true forgetting (Fagen & Prigot,
1993).
Finally, the interval between training with the preferred mobile and training with the nonpreferred mobile is an important
determinant of the degree of impairment in delayed recognition.
When a delay of 0, 2, 5, or 15 min was interpolated between
infants' exposure to the pre- and postshift mobiles, infants who
cried again failed to recognize the test mobile 1 week later;
when the interpolated delay was increased to 30 min, however,
their performance on the delayed-recognition test was excellent.
The performance of infants who did not cry on the l-week test,
by comparison, was excellent after all postshift delays (Fagen
et al., 1989).
484
ROVEE-COLLIER
Serial Position
The serial position of items on a study list has long been
known to produce strong and persistent primacy effects, recency
effects, or both on immediate tests of free recall, cued-recall,
and recognition memory (e.g., Bousfield, Whitmarsh, & Esterson, 1958; Gershberg & Shimamura, 1994; Murdock, 1962;
Wright, Santiago, Sands, Kendrick, & Cook, 1985). A handful
of researchers have found recency effects on implicit tests of
both word-stem completion (McKenzie & Humphries, 1991;
Rybash & Osborne, 1991 ) and word-fragment completion (Sloman et al., 1988), but Brooks (1994) observed that the instructions and procedures in these reports were either suspect or
reported in insufficient detail.
Two laboratories have recently used the same study instructions and test stimuli but different instructions for the implicit
and explicit tests. Gershberg and Shimamura (1994) obtained
inconsistent evidence for primacy and recency effects across
three experiments. Implicit word-stem completion tests, for example, yielded a primacy effect in two experiments and a recency effect in one, and these effects were highly transient when
they did occur. Different explicit tests (word-stern-cued-recall,
free-recall) also yielded inconsistent primacy, recency, or both
effects across experiments. Using word-stem completion and
word-stem-cued-recall tests with adults with normal memory,
Brooks (1994) found primacy effects on an explicit test in two
experiments and, when the items studied last were tested first,
a recency effect in the second of these. In neither experiment,
however, did serial position affect performance on the implicit
test. Taken together, the data indicated that the serial order of
the items on the study list had no effect on performance in
implicit tests but produced a primacy effect in explicit tests.
Finally, in two experiments, patients with both Korsakoff and
non-Korsakoff amnesia performed more poorly than controls
on tests requiring the recall, recognition, and sequencing of
words and facts (Shimamura, Janowsky, & Squire, 1991 ).
A delayed-recognition test with 6-month-olds also revealed
a strong primacy effect after a 24-hr delay (Merriman et al., in
press). In a study described earlier (cf. Number of Studied
Items), independent groups of infants were trained with a serial
list of three different mobiles for 2 min each on 3 successive
days and were tested 24 h later with a mobile from one of the
three serial positions or with a completely novel mobile. On the
delayed-recognition test, infants had recognized only the mobile
from Serial Position 1 (see Figure 12, left panel). A follow-up
study, also described earlier, demonstrated that infants' poor
recognition of the last two list items had not resulted from an
initial encoding failure; infants were capable of recognizing
items from as many as five serial positions 24 h later (Gulya &
Rovee-Collier, 1996; see Figure 12, right panel). We conjectured, therefore, that infants who were trained with the threemobile list may have failed to recognize the mobiles from Serial
Positions 2 and 3 because the single retrieval cue in the 24-hr
serial-probe recognition test had provided no order information.
This conjecture was confirmed when infants were trained on
a three-mobile list and then were primed for 2 rain by the mobile
from the preceding serial position (i.e., a sequential-probe procedure) immediately prior to the 24-hr test. (This procedure
closely resembles a stem-completion priming task in studies
with adults.) Infants recognized the test mobile from Serial
Position 2 if they were first primed by the mobile from Serial
Position 1 but not if they were primed by the mobile from Serial
Position 3. Infants also failed to recognize the test mobile from
Serial Position 3 after priming by the mobile from Serial Position 1, as did 4 of the 6 infants who were primed with the
mobile from Serial Position 2. When infants were successively
primed for 1 min each with the mobiles from Serial Position 1
and Serial Position 2, however, they recognized the test mobile
from Serial Position 3. Unlike the magnitude of retention on the
delayed recognition test, the magnitude of retention after the
priming treatment was not sensitive to serial position. Following
primes that were valid order cues, the primacy effect disappeared, and mobiles from Serial Positions 2 and 3 were recognized equally well and as well as the mobile from Serial Position
1 (see Figure 15).
Finally, Mandel, Kemler Nelson, and Jusczyk (1996), using
the high-amplitude sucking procedure, reported that infants as
young as 2 months could discriminate a change in the order of
spoken words on a 2-min delayed-recognition test if the change
was embedded in a well-formed sentence but not in a sentence
fragment. The authors concluded that the sentential prosody
helped infants remember the sequentially ordered words.
Studied Size
In studies with adults with normal memory and patients with
amnesia, a change in the studied size of an object at the time
of testing impairs performance on recognition memory tasks
Reactivation
Recognition
5.0
4.5
0
rl-o~
l-
4,0
3.5
~r
3,0
2.5
2.0
1.5
1.0
>
.....i
s / / i
1
2
1/2
3
Groups
i
.
se,,oe
1-2/3
Figure 15. The effect of the serial position of mobiles on a threemobile list on the magnitudeof delayed recognition (left panel) and the
magnitude of reactivation(right panel) 24 hr after training at 3 months
of age. The delayed-recognitionfunction (left panel) shows a classic
primacy effect that was eliminated (right panel) when mobiles in Serial
Positions 2 and 3 were primed with mobiles from the preceding serial
position or positions immediatelybefore the test. Asterisks mark groups
that displayedretention (baseline ratio > 1.00). Data are from Gulya &
Rovee-Collier, 1996; Merriman, Rovee-Collier, & Wilk, in press.
ON THE DEVELOPMENT OF MEMORY SYSTEMS
(Biederman & Cooper, 1992; Jolicoeur, 1987; Milliken & Jolicoeur, 1992; Schacter, Cooper, & Treadwell, 1993) and object
decision tasks (Cooper, Schacter, Ballesteros, & Moore, 1992;
Schacter, Cooper, Delaney, et al., 1991 ), but these same studyto-test size changes do not affect priming on either object naming tasks (Biederman & Cooper, 1991, 1992) or object decision
tasks (Schacter, Cooper, Tharan, & Rubens, 1991; Schacter,
Cooper, et al., 1993), whether the objects are novel or familiar.
The same pattern of impaired recognition and preserved priming has been obtained with 3-month-olds in delayed-recognition
and reactivation tests, respectively, following transformations in
studied size. In an initial study, infants who were trained with
a mobile composed of seven pink blocks with a black L on each
side exhibited excellent retention in a 24-hr delayed-recognition
test with the same characters (the no-change control group);
when tested with Ls that were either reduced or increased in
size by 25%, however, infants' performance on the delayedrecognition test was significantly impaired (Adler & RoveeCollier, 1994). In a subsequent study with a different stimulus
(Gerhardstein, Adler, & Rovee-Collier, 1996), the delayed recognition of 3-month-olds who were trained with a mobile displaying + s was significantly impaired when they were tested
24 hr after training with + s that were either reduced or increased
in size by 33% (see Figure 16, left panel). In contrast, the
magnitude of reactivation 2 weeks later was excellent and unaffected by transformations in the size of the + s used as reminders
to prime the memory (see Figure 16, right panel).
Memory Load
The term memory load has been used with reference to the
length of the retention interval, with longer test delays creating
a greater memory load (Quinn & Eimas, 1996), and to the
3.0
Recognition
Reactiv=ion
2.5
rt(D
¢-
l
l
O
2,0
\ ~ \ \ \ \
nn
1.0
--
-
. .
~
x ~ x x x x
. - .
x x x x x x
Change
No Change
Change
No Change
Size of Group
Figure 16. The effect of changing the size of the training character by
33% on the magnitude of delayed recognition 24 hr after training (left
panel) and the magnitude of reactivation (right panel) 3 weeks after
training at 3 months of age. The performance of no-change control
groups who were trained and either tested or primed with the original
character is also shown. Asterisks mark groups that displayed retention
(baseline ratio > 1.00). Data are from Gerhardstein, Adler, & RoveeCollier, 1996; Rovee-Collier,Hankins, & Bhatt, 1992.
485
amount of information that must be retained over a given delay
(G. Mandler, 1985). Both of these usages were considered earlier (see Retention Interval and Number of Studied Items). A
third factor that affects the memory load is the nature of the
to-be-remembered information. For infants as for adults, for
example, relational information creates a greater memory load
than absolute information. Adler and Rovee-Collier (1994) reported that 3-month-old infants could discriminate horizontal
and vertical line segments (two textons) in different spatial
relations (L versus T) during a l-hr delayed-recognition test
but not during a 24-hr test. However, they could discriminate
+ s, which contain a line crossing (a third texton), from both
Ls and ~ during a 7-day test. In addition, infants recognized
Ls and Ts for only 3 days, but they recognized + s for 7 days.
These data illustrate the greater retention advantage for absolute
information (texton number) relative to relational information
(spatial arrangement). Despite differences in the memorability
of these stimuli on delayed-recognition tests, their magnitude
of reactivation was equivalent when the same stimuli were used
as reminders with 3-month-olds 2 weeks after training (RoveeCollier, Hankins, et al., 1992) and with 6-month-olds 3 weeks
after training (Bhatt, Rovee-Collier, & Weiner, 1994).
In the following studies, increasing the memory load selectively impaired infants' retention of relational information on a
delayed-recognition task but not on a reactivation task. In a
sequel to the feature-combinations study described earlier
(Bhatt & Rovee-Collier, 1994; see Number of Studied Items),
3-month-olds differentially forgot the correlations between different training features (relational information) as the retention
interval increased from 1 day to 3 days, but they still recognized
the individual features (absolute information) and discriminated
them from novel features on a delayed-recognition test after a
4-day retention interval (Bhatt & Rovee-Collier, 1996). When
the number of feature sets on the training mobile was increased
from two to three, infants recognized the feature relations on
the two-set mobile but not on the three-set mobile during a 24hr delayed-recognition test. In a reactivation task, however, the
three-set mobile was an effective reminder 2 weeks later if it
displayed the original feature combinations but not if it displayed feature recombinations (Bhatt & Rovee-Collier, in
press). Finally, recall that 6-month-olds who were trained with
a three-mobile list had recognized only the mobile from Serial
Position 1 and had discriminated a novel one (absolute information) during a 24-hr serial-probe-recognition test (see Figure
14, left panel). In the reactivation task, however, infants had
also recognized items from Serial Positions 2 and 3 after the
same delay (see Figure 14, right panel), but only if the prime
and test cue were in the correct serial order (both absolute and
relational information; Gulya & Rovee-Collier, 1996).
Context
The role of context in retention has been of interest to psychologists for almost a century. Broadly speaking, the context
refers to global aspects of the experimental environment, including both external conditions (e.g., the room, the experimenter,
and the apparatus) and internal conditions (e.g., the inner state
of the individual, including the pharmacological state, the mood
or affective state, and processes associated with the point in the
486
ROVEE-COLLIER
circadian or uitradian cycle). However, the context can also refer
to more local stimuli, such as the visual stimuli that surround or
precede a target object or the items that accompany the target
item on each study trial. In such cases, the context usually
facilitates the interpretation of the target (for review, see Clark &
Carlson, 1981 ).
Tulving (1983) claimed that the effect of context on episodic
memory is more pronounced than on semantic memory, and G.
Mandler ( 1985 ), although rejecting a multiple memory-systems
approach, considered nonautomatic memories to be context dependent and automatic memories to be context free. Neely
(1989; Neely & Durgunoglu, 1985), however, concluded that
the evidence for these distinctions was ambiguous, and Richardson-Klavehn and Bjork (1988) observed small but persistent
context effects over a wide range of perceptual identification
(priming) studies, even though effects within a given study were
often not significant. In fact, although abundant research shows
that a change in context between study and test impairs performance on recognition and recall tests (R. L. Cohen, 1985; Spear,
1978; Thomson & Tulving, 1970; Underwood & Humphreys,
1979), less research has addressed the role of context in performance on implicit memory tests.
In an early study of this sort, Jacoby (1983) had adults read
a list of words and then gave them a perceptual identification
test containing different proportions of words from the previously read list. Perceptual identification was facilitated by the
proportional overlap between the study and the test list. Likewise, Graf and Schacter (1985) found a larger priming effect
on a word-fragment completion task when college students and
patients with amnesia were primed with a word from a word
pair on a prior study list (same context condition) than with
other words (different context condition), but this difference
emerged only when the study task required elaborative processing. More recently, however, Allen and Jacoby (1990) determined that the priming effect on a perceptual identification test
was equivalent whether test words had been generated during
study (i.e., were easily recognized) or only read (i.e., were
poorly recognized). Changes in the modality of presentation
(Roediger & Blaxton, 1987), the visual display of the target
stimuli (Jacoby & Dallas, 1981 ), the environmental setting of
encoding and retrieval (Graf, 1988; Smith, Heath, & Vela,
1990), the perceived sense or meaning of a word (Lewandowsky, Kirsner, & Bainbridge, 1989), and mood (Macaulay et al.,
1993) have also been found to disrupt memory performance on
implicit tests.
In studies with infants, we have defined a training event as
consisting of the focal cue (either the mobile or train) and the
context in which training occurs (either the immediate visual
surround, created by draping a colored- and-patterned cloth over
the sides of the crib or playpen, or a room in the house). We have
repeatedly found that changing the immediate visual surround
impairs both delayed recognition and memory reactivation at 3
and 6 months (Borovsky & Rovee-Collier, 1990; Butler &
Rovee-Collier, 1989; Shields & Rovee-Collier, 1992). Likewise,
changing the room at the time of a reactivation treatment completely precludes memory reactivation in the mobile paradigm
at 3 months (Hayne, Rovee-Collier, & Borza, 1991 ) and in the
train paradigm at 6 months (Hartshorn & Rovee-Collier, 1997).
A room change also impairs the delayed recognition of older
infants in the train task but only after relatively long delays,
when the training memory is presumably weaker. At both 9 and
12 months of age, for example, a room change does not impair
performance on a delayed-recognition test 4 weeks after training, but it does impair recognition after the longest delay that
infants remember the task (6 weeks at 9 months, 8 weeks at 12
months). In contrast, a change in the focal cue impairs recognition after both test delays at each age (Aaron, Hartshorn, Klein,
Ghumman, & Rovee-Collier, 1995).
The deleterious effect of a context change on delayed recognition at 3 and 6 months of age can be overridden by explicitly
training infants in a different context in each session (Amabile & Rovee-Collier, 1991; Rovee-Collier & DuFault, 1991 ) - a condition like that which has long been known to override
the debilitating effect of a context change on adults' recall (Pan,
1926). The same effect was found by briefly exposing 6-montholds to a different distinctive surround within a day of the end
of training (Boller & Rovee-Collier, 1992; Boller et al., 1996)
and, at 3 months, by repeatedly reactivating the original memory
(Hitchcock & Rovee-Collier, 1996). In the latter study, infants
were initially reminded with the original mobile in the original
context; only their second or third reactivation treatment occurred in a different context. During all subsequent reactivation
treatments, the training memory was successfully primed in the
different context, indicating that the original contextual attributes had become inaccessible after the first reactivation treatment. The memory could not be reactivated, however, by a different mobile unless it had been reactivated twice previously and
a very long interval (5 weeks) had also elapsed since training
was completed.
All of the preceding studies are consistent in documenting
that the memory attributes representing contextual information
become inaccessible before those that represent the focal cue
(see also Riccio et al., 1992).
Memory for Place
According to Nadel, Willner, and Kurz (1985), "Virtually
all learning during infancy i s . . . independent of context" (p.
398). Their conclusion was based on (a) the assumption that
the hippocampal formation, which mediates the representation
of the environmental context in normal adults, is not functional
in infancy; and (b) evidence that habits and skills, which are
context free, are preserved in individuals with amnesia with
hippocampal dysfunction.
Evidence that infants' memory performance in the mobile
paradigm consists ofmore than a set of simple skills and habits
was presented earlier in this article. Direct evidence that contradicts this conclusion, however, comes from reactivation studies
with 3- and 6-month-olds who were trained with a particular
mobile (Borovsky & Rovee-Collier, 1990; Hayne et al., 1991 )
or train set (Hartshorn & Rovee-Collier, 1997) in one room in
their home and were reminded with the same mobile or train
set in another room. At both ages, the reactivation treatment in
the altered context was ineffective, indicating that information
about the particular place where infants had learned the task
was represented in the original training memory. At 3 months,
a reactivation treatment was also ineffective when infants were
trained in their crib in the bedroom and were reminded in exactly
ON THE DEVELOPMENT OF MEMORY SYSTEMS
the same spot in the same room but in a portacrib (which is
smaller and lower), or vice versa (Hayne et al., 1991 ).
Data of this sort led Butler and Rovee-Collier (1989) to postulate a hierarchical attention-gating model of memory retrieval
in which a perceptual match or mismatch between the most
remote test context (and then between increasingly less remote
levels of context) and the memory attributes representing the
training context determines whether or not the memory will be
retrieved. A mismatch at any level aborts the retrieval process
at that point. Over the first postnatal year, however, this process
apparently requires a smaller complement of contextual details
(Aaron et al., 1995; Earley, Bhatt, & Rovee-Collier, 1995).
I have speculated elsewhere (Rovee-Collier, 1996) that prior
to the onset of independent locomotion, infants learn what events
transpire in what places. Only after infants can crawl do they
learn the spatial relations among those different places (i.e., a
cognitive m a p ) - - i n f o r m a t i o n that is requisite for spatial navigation. This view distinguishes between place information, which
is absolute knowledge, and relational information about the spatial layout. Nadel et al. (1985) did not make such a distinction.
The infant data are compatible, however, with Nadel et al.'s
description of how a cognitive map contributes to environmental
recognition:
Upon entering a previously mapped environment, an organism identifies the place it is in by detecting a small set of things in a
particular spatial arrangement. Appropriate spatial arrangements activate enough elements in one particular map ensemble to initiate
place recognition. This recognition p r o c e s s . . , disposes the organism to interpret or act upon the environment in certain ways, reflecting the "expectations" embodied in the environment-specific
activation . . . . In the complete absence of the hippocampal system,
organisms seem oblivious to the familiarity/unfamiliarity of environments. (p. 391)8
Clearly, either the hippocampal formation matures earlier than
Nadel et al. thought, or some other part of the brain mediates
the representation of place information early in development.
M e m o r y for a S p e c i f i c P r i o r E p i s o d e :
Deferred Imitation Revisited
Some researchers have claimed that the deferred-imitation
task, in which nonverbal infants are exposed on a single occasion to an adult demonstrating several target actions, provides
evidence of deliberate, conscious recall and explicit (declarative) memory (Bauer, 1996; Bauer & Hertsgaard, 1993; J. M.
Mandler, 1988, 1990; McDonough et al., 1995). J. M. Mandler
(1990), for example, concluded that because adults use recall
to solve the deferred-imitation task, its solution by nonverbal
infants must also require conscious awareness. Bauer (1996)
similarly concluded that, unlike other changes in nonverbal behavior from which memory is inferred, conscious recollection
can unambiguously be inferred from infants' performance in the
deferred-imitation task because it "engages the same cognitive
processes as those involved in verbal recall by older children
and adults" (p. 31). McDonough (quoted in B. Bower, 1995,
p. 86) claimed that "deferred imitation relies on brain structures
essential for declarative memory, the capacity for intentionally
calling to mind specific facts and events."
487
The latter claim was based on the finding that healthy adults
and patients with frontal-lobe damage could reproduce correct
action sequences after delays of 1 day and 3 months after seeing
them demonstrated on a single occasion, but individuals with
amnesia performed at control levels on a similar test (McDonough et al., 1995). Because ll-month-old infants had performed similarly in the deferred-imitation task in an earlier
study, McDonough characterized the results from the McDonough et al. study with adults with normal memory and individuals with amnesia as "the first solid evidence that infants consciously remember what they have learned . . . .
But our data
don't address whether infants consciously remember where and
when they learned the same i n f o r m a t i o n . . . " (quoted in B.
Bower, 1995, p. 86). Unfortunately, these claims and the evidence for them are based on two unacceptable inferences: (a)
that any conclusions at all can be drawn about the capacities or
the abilities of nonverbal infants from a study with adults with
normal memory or otherwise, and (b) that there is a one-to-one
mapping of a particular task (here, the deferred-imitation task)
to an underlying memory system (here, the explicit or declarative memory system). Jacoby (1991) characterized the latter
inference as " m o r e than a little shaky" and observed that the
" u s e of memory for a prior episode as a source of automatic
influences . . . does not imply that one can or does recollect
that prior episode" (p. 534; see also Jacoby & Witherspoon,
1982). Tulving (1990) similarly warned that conscious recollection cannot be inferred from performance on an explicit memory
test because conscious experience and such behavior are not
necessarily related. In fact, there is no direct evidence of conscious awareness in deferred-imitation experiments with preverbal infants (see also Fagan, 1990; Thompson, 1990; Werker,
1990), and memory studies with adults offer no direct insights
into the basis of memory performance of nonverbal infants.
The same researchers have also claimed that the fact that
preverbal infants can display deferred imitation of action sequences after a single exposure, with no opportunity for practice
prior to the test, distinguishes it from the memory performance
of preverbal infants in delayed-recognition studies, which they
nonselectively attribute to an implicit or nondeclarative memory
system (Bauer, 1996; Bauer & Hertsgaard, 1993; J. M. Mandler,
1984, 1988, 1990; McDonough et al., 1995; Schacter & Moscovitch, 1984). This position was summarized by Bauer
(1996):
What tasks that tap declarative memory have in common is that
they require recollection of a specific episode. In contrast, what
tasks that tap nondeclarative memory have in common is that recollection of a specific episode is not required, and in most cases
(priming being an exception), learning proceeds gradually, as a
result of repeated practice. (p. 31 )
In the mobile paradigm, however, even 3-month-olds can perform an action on an object on the basis of a single prior
exposure with no opportunity for practice prior to testing (Greco
et al., 1990; Hayne, Greco-Vigorito, & Rovee-Collier, 1993;
Rovee-Collier et al., 1993). In a prototypic study, infants were
8 Fagen et al. (1984) discussed the development of infants' expectations in the mobile task.
488
ROVEE-COLLIER
exposed to stained-glass-and-metal wind chime that was being
jiggled by the experimenter for 3 min (Rovee-Collier et al.,
1993). This occurred on only a single occasion, 4 days after
infants had learned to kick to move yellow-block mobiles that
displayed As or 2s on all sides of each block. When presented
with a stationary wind chime during a delayed-recognition test
1-10 days later (i.e., 5 - 1 4 days after the end of mobile training), infants kicked vigorously, apparently attempting to move
it with the same response they had previously used to move
the yellow-block mobiles. Their memory performance depended
solely on having previously seen that the wind chime could
move; infants who viewed a stationary wind chime did not
kick during the test (Greco et al., 1990; Rovee-Collier, GrecoVigorito, et al., 1993).
Because infants had never previously moved the wind chime
by kicking, it cannot be argued that they were simply running
off a stimulus-response habit that they had acquired gradually
or incrementally through reinforced or repeated practice (Bachevalier, 1990; Bachevalier & Mishkin, 1984; Bauer, 1996; J. M.
Mandler, 1990; Schacter & Moscovitch, 1984). On the contrary,
these infants merely applied an action that was already in their
behavioral repertoire upon the test object in order to make it
function as, on a single prior occasion, they had seen it could.
No perceptual information about its function was available at
the time of testing. As in the deferred-imitation paradigm, neither the target action nor its consequence was physically present
to be recognized at the time of the test (see Bauer, 1996; J. M.
Mandler, 1984, p. 79, and 1990, p. 491 ). Also as in the deferredimitation paradigm, the experimenter provides the infant with
the "props" (e.g., a mobile, the context) in lieu of instructions,
thereby creating an occasion for cued recall, but the specific
action to be performed is not externally cued. This was especially apparent in the experiments of Timmons ( 1994, described
below in Associative Relations), in which infants learned two
different responses to two different cues prior to testing.
The major difference between the deferred imitation and the
mobile passive-exposure study is that infants in the mobile study
observed an object action instead of an experimenter action.
Because they associated the wind chime with the training mobile
only if they had seen the wind chime in motion, the functional
similarity of the wind chime to the training mobile was clearly
the basis for their performance on the delayed-recognition test.
Also, because both adults and infants had psychophysically
scaled the wind chime as "highly physically different" from
the training mobiles, infants' response to the wind chime could
not have been based on a generalized response to a similar
object form (see also The Structural Descriptions System and
Infant Memory, next).
In another study, infants' delayed recognition was also based
on what they merely witnessed during a single prior episode.
Hayne et al. (1993) trained 3-month-olds in their home cribs
for three sessions with a different mobile in each session. During
Session 3 only, a blue-and-red-striped cloth was draped around
the sides of the crib. When Session 3 was over, the ankle ribbon
was detached from the overhead suspension hook and the training mobile was removed, but then the stationary wind chime
was merely hung from the hook for 3 min while the blue-andred-striped context was still in place. On the following day,
infants received a standard delayed-recognition test 24 h later
with the stationary wind chime in the absence of the blue-andred-striped context. Even though the distinctive context was not
present at the time of testing, infants kicked robustly, apparently
trying to move the wind chime, even though they had never
before seen it move. A control group, treated exactly like the
experimental group except that the distinctive blue-and-redstriped cloth was not present either during the third training
session or when the wind chime was exposed, did not recognize
the wind chime (i.e., kick) during the ensuing test.
Hayne et al. (1993) concluded that the representation of the
wind chime had been integrated with the infants' prior training
memory via the common distinctive context that was present on
only a single prior occasion--during their final training session
and during their subsequent exposure to the wind chime. Here,
the context acted in the manner of a catalyst: It was necessary
in order for the initial integration of the two events, but it was
no longer necessary (e.g., for subsequent memory performance)
once the integration had occurred. This study unambiguously
demonstrates that infants' performance during the 24-hr delayed-recognition test resulted from the retrieval of their memory for a specific prior episode. The infants' delayed-recognition
behavior fully satisfies the description put forth by Nadel et al.
(1985) for an internal model representing connections among
contextual elements (see also Hayne & Findlay, 1995 ). As with
deferred imitation, however, this result offers no evidence that
infants consciously recollected that particular prior episode.
In summary, in both delayed-recognition and deferred-imitation tasks, infants have been presented with an object that they
saw in a single prior episode. This object cues retrieval of the
memory of that episode, enabling infants to perform the target
action upon it. Whether infants in either task are consciously
aware of having previously seen the object can only be inferred
from their behavior (J. M. Mandler, 1990); nothing in their test
performance supports such an inference (Thompson, 1990).
The fact that infants' delayed recognition was based on a specific prior episode also yields no insights into the brain mechanisms responsible for their performance (see McDonough,
quoted in B. Bower, 1995). The fact that even 6-month-olds, if
given a long enough exposure to the demonstrator, can imitate
three specific actions that they only watched on a single occasion
24 hr earlier (Barr et al., 1996) challenges the functional significance of describing memory development in terms of the
sequential maturation of two separable memory systems.
The Structural Descriptions System and Infant Memory
Several years ago, Schacter introduced the structural descriptions system as a subsystem of implicit memory (Schacter, 1990;
Schacter, Cooper, & Delaney, 1990). This is a perceptual representation system dedicated to the representation of information
about the form and structure of visual objects, including a description of an object's plane of orientation about a central axis
(Cooper, Schacter, & Moore, 1991 ) but not its size (Schacter,
Cooper, et al., 1993). This system also includes no semantic
information about either the functions that an object can perform
or its associative properties. The dominant paradigm for evaluating memory performance mediated by this system is the object
decision task, in which individuals make perceptual decisions
about the test stimuli, such as whether or not a particular drawing
ON THE DEVELOPMENT OF MEMORY SYSTEMS
could possibly exist as a three-dimensional object (Schacter &
Cooper, 1993; Schacter et al., 1990; Schacter, Cooper, Delaney,
et al., 1991). The research findings demonstrate the familiar
memory dissociation: Priming is preserved for both novel
(Schacter, Cooper, et al., 1993) and familiar (Cave & Squire,
1992) objects, but recognition memory is impaired (Biederman & Cooper, 1992; Schacter, Cooper, et al., 1993).
Because the structural descriptions system is cast as a subsystem of implicit memory (Schacter, 1990), it is presumed to be
present quite early in development. In view of its other characteristics, however, the. structural descriptions system cannot account for evidence that object function (Greco et al., 1990)
and object size (Gerhardstein et al., 1996) affect the delayed
recognition of infants as young as 3 months and that associations
between memories (Timmons, 1994) affect the memory performance of infants as young as 6 months. The evidence pertaining
to object function and associations between memories is described below; evidence pertaining to object size was described
previously (Studied Size).
Object Function
A mobile that infants previously learned to move by kicking
is an effective reminder in a reactivation task if it is moving but
not if it is stationary (Fagen, Yengo, Royce-Collier, & Enright,
1981; Greco et al., 1990; see also Schacter & Moscovitch,
1984). In a delayed-recognition task, however, the same mobile
cues retrieval when it is stationary. This difference probably
reflects the fact that fewer or different cues are needed to retrieve
memories that are more accessible (Rovee-Collier, Schechter,
Shyi, & Shields, 1992; Spear, 1978). Information about object
function is not requisite for memory reactivation, however, if
the cue that is used as a reminder was originally nonfunctional.
The original training context obviously did not move, for example, yet it is an effective reminder for the training memory when
presented alone, in the absence of the original training mobile
(Hayne & Findlay, 1995; Rovee-Collier, Griesler, & Earley,
1985).
Additional evidence that object function plays a critical role
in infant memory comes from studies involving the passiveexposure procedure. In this procedure, mentioned in the preceding section, infants are merely exposed to (i.e., do not interact
with) a novel object that is functioning as their prior training
mobile had functioned. The exposure is brief--only 3 min for
3-month-olds and only 2 min for 6-month-olds--and occurs only
once after posttraining delays that can be as long as days or
weeks. Infants then receive a delayed-recognition test, also after
delays that can be as long as days or weeks, in which either the
training mobile or the exposed object is presented as the retrieval
cue.9 The passive-exposure procedure has revealed that infants'
memories are readily modified or updated to include the exposed
object in addition to (memory expansion) or in place of (memory impairment) the original mobile (Boiler, Grabelle, & RoveeCollier, 1995; Boiler et al., 1996; Muzzio & Rovee-Collier, 1996;
Rovee-Collier et al., 1994; Rovee-Collier, Borza, et al., 1993;
for review, see Rovee-Collier & Boiler, 1995), despite the fact
that infants do not respond to a novel test mobile otherwise.
This updating occurs even if the exposed object and the prior
training mobile are highly physically dissimilar, as long as they
489
are functionally equivalent. Passive exposure to the novel object
in the absence of equivalent functional information does not
affect the prior training memory (unless another common attribute mediates their integration; Hayne et al., 1993), and infants
continue to discriminate the novel object during the delayedrecognition test (Boiler et al., 1995; Greco et al., 1990).
Associative Relations
A number of theorists have proposed that items are stored in
a memory network and connected to each other by links (e.g.,
Collins, 1975; Collins & Quillian, 1969). According to spreading-activation models, the presentation of a retrieval cue activates a memory at a particular node in the network; as this
excitation spreads to nodes that are linked to the original one,
they are activated as well. As a result, memories associated with
nodes indirectly activated in this fashion also become more
accessible.
Timmons (1994) obtained evidence that infants form associations between independent memories by 6 months of age. In an
initial study, she trained infants to either move a mobile suspended over the playpen or turn on a music box affixed to the
playpen rail by either arm pulling or foot kicking--an analog
of the traditional paired-associate task used in studies of adult
verbal learning and memory. Infants were trained in a distinctive
context for 2 days with one cue-response pair; 3 days later,
they learned the other cue-response pair in the same context.
Three days after learning the second pair, independent groups
received a delayed-recognition test with one of the cues. During
testing, infants produced only the particular response that had
originally been associated with a given cue, regardless of which
action it was (arm movement, foot kick) and which response
was learned last. This result confirmed that the memories of the
cue-response pairs were independent and that the retrieval of
each response was specific to its associated cue.
In a second experiment, Timmons (1994) trained infants as
before. Three weeks after training on the second pair, when both
of the training memories had been forgotten, she exposed infants
either to the mobile or the music box as a memory prime in a
reactivation task. During testing the next day, she presented only
the mobile as the retrieval cue to all infants. As expected, infants
who were both reminded and tested with the mobile exhibited
the mobile-appropriate response. Surprisingly, however, infants
who were primed with the music box and tested with the mobile
also exhibited the mobile-appropriate response--and no
other--to the mobile test cue (see Figure 17).
For the latter infants, the mobile memory had not been directly
primed with the mobile and was clearly forgotten when their
music box memory had been primed with the music box. Timmons (1994) concluded, therefore, that the music box prime
had indirectly activated the memory node representing the mobile paired associate through spreading activation, thereby enabling infants to perform the mobile-appropriate response to the
mobile cue 24 hr later. Thus, even though the memories of the
two cue-response pairs were independent and highly specific,
9A novel context has also been used in the passive-exposure
procedure.
490
ROVEE-COLLIER
0.80
+
Reactivation
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0.70
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° ~0
0.60
n.c_
0.50
T
0.40
None
T
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~\\\\\\N
........
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xxxxxxxx
\ \ \ \ \ \ \ N
........
.\\\\\-,~
. . . . . . . .
~ \ \ \ x x x \
xxxxxxxx
~xxx~\xx
xx\xx\xx
\ \ \ \ \ \
~ \ \ \ \ \
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, \ \ \ \ \
"\xxxxx~
\ \
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xxxxxxxx
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xxxxxxxx
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..
Mobile
Music Box
Reactivation Cue
Figure 17. Associative priming exhibited by 6-month-olds who originally learned to perform different responses to a mobile and to a music
box cue. The forgotten memories of the two experimental groups were
primed by either a mobile or a music box reminder 3 weeks after training,
and both groups were tested only with the mobile 1 day later• The control
group received no reactivation treatment. The magnitude of reactivation
was the same whether reactivation was direct (Mobile) or indirect (Music Box). The baseline ratio was calculated by the formula B/A + B.
Asterisks mark groups that displayed retention (baseline ratio > .50),
where B = infant's kick rate during the long-term retention test; A =
infant's level of learning. Data are from Timmons (1994).
they were associatively linked--probably via the common context in which both pairs were a c q u i r e d - - i n a common mnemonic network. As a result, reactivating one memory brought
to mind the memory of the other. According to J. M. Mandler
(1984), recall " c a n occur incidentally through a process of
being reminded• We are not trying to retrieve a piece of information, but an external or internal cue automatically brings it to
our a w a r e n e s s . . . [without] a deliberate search taking place"
(pp. 7 9 - 8 0 ) . In fact, excluding "awareness," her description
exactly fits Timmons' data.
Sheffield and Hudson (1994) similarly observed an indirect
reactivation phenomenon in a memory study with 14- to 18month-old toddlers. Using a multiple-activities paradigm, they
allowed toddlers to engage in six different structured activities
at different stations in the laboratory. After toddlers' memory
of their visit had been forgotten, they retumed to the laboratory,
and half of the activities were modeled by the experimenter
while the children merely watched. Twenty-four hours later, the
children were asked to produce the three activities they had not
seen modeled plus the three that they had. As expected, children
of the same age who had viewed the modeling but had not been
originally trained produced only the three activities they had
seen modeled the day before, and children who had been originally trained but had not received the reactivation treatment (the
modeling) produced none. However, children who had been
originally trained and had also seen three activities modeled as
a reminder produced the three modeled activities as well as the
three activities that had not been modeled• As in the Timmons
(1994) study, directly reactivating some activities led to the
indirect reactivation of others--again, probably mediated by the
common context in which the activities had originally been
performed. Clearly, then, associative-memory priming is not
unique to the mobile task; it also can be observed with older
infants in a paradigm that involves no preconditioning of the
target response whatsoever.
The preceding evidence demonstrates that object function affects memory performance by 3 months of age and that associations between memories affect memory performance by 6
months of age. Yet, these variables are thought to be the sole
domain of the explicit memory system, not the implicit memory
system (Schacter, 1990).
A r e Infants and O t h e r N o n v e r b a l O r g a n i s m s
Consciously Aware?
To reiterate, the defining characteristic of an explicit memory
s y s t e m - - c o n s c i o u s a w a r e n e s s - - c a n n o t be directly measured
in infants and other nonverbal organisms. To quote Olton
(1989), "the absence of p r o o f . . ,
is not proof of absence"
(p. 167). The question of whether organisms other than linguistically competent humans possess conscious awareness has
vexed philosophers since the time of the ancient Greeks. The
issue was temporarily resolved in the 17th century by the
cartesian distinction between mind versus matter. The recent
introduction of the explicit versus implicit memory dichotomy
with emphasis on conscious awareness has reinvigorated advocates of dualism as well as its critics. In considering how consciousness should be defined, the philosopher John Searle
(1995) suggested a commonsense rather than an analytic
definition:
"Consciousness" refers to those states of sentience and awareness
that typically begin when we awake from a dreamless sleep and
continue until we go to sleep again, or fall into a coma or die or
otherwise become "unconscious." (p. 60)
He argued that conscious experiences are emergent properties
of neurobiological processes in the b r a i n - - a n approach that
places consciousness squarely in the realm of other ordinary
biological phenomena such as physiological thermoregulation,
mitosis, and digestive processes (Searle, 1984, 1995). This argument echoes Hubbard's (1975) conclusion that mental phenomena are direct consequences of neural activity. Although
Searle (1983) argued that brain processes cause consciousness,
he viewed it as simply a feature of the brain, just as the solidity
of a table is a feature of the table's molecular structure: "mental
states are both caused by the operations of the brain and realized
in the structure of the brain" (p. 265).
Tulving (1987), however, insisted that the " p r o b l e m of consciousness and memory is different from problems of consciousness with which many generations of thinkers have wrestled
• . . problems such as what consciousness is, and how it
emerges from the physical-chemical brain activity" (p. 75). He
argued that the problem of conscious awareness "concerns the
selective but systematic occurrence of conscious awareness in
remembering, as well as in other mental activities" (Tulving,
1987, p. 75 ). Although Tulving's distinction between consciousness and conscious awareness has intuitive appeal, he offered
ON THE DEVELOPMENT OF MEMORY SYSTEMS
no operational definition for it (see also Shapiro & Olton, 1994,
p. 108).
More than 2 decades ago, a parallel issue arose in the field
of animal communication. At that time, the common criterion
for distinguishing animal from human language was the assumption that animals lacked both conscious awareness of their own
mental experiences (if they had any) and a conscious intent to
communicate (e.g., Terwilliger, 1968). Griffin (1976), however,
characterized this assumption as antagonistic to the "general
principle of evolutionary kinship and continuity" between animals and men. He argued,
The hypothesis that some animals are indeed aware of what they
do, and of internal images that affect their behavior, simplifies our
view of the universe by removing the need to maintain an unparsimonious assumption that our species is qualitativelyunique in this
important attribute. (Griffin, 1976, p. 101)
Like Searle (1995), Griffin proposed that mental experiences
are directly linked to neurophysiological processes that are
highly similar in all multicellular animals. Indeed, this is a plausible hypothesis (Griffin, 1976). Perhaps we should similarly
simplify our view of the universe and either assume that preverbal infants and animals are consciously aware or eliminate conscious awareness as a defining characteristic of explicit memory.
Conclusion
There is no empirical evidence that the implicit and explicit
memory systems follow a hierarchical developmental sequence,
with the implicit memory system maturing early in the 1st year
and the explicit memory system maturing late in the 1st year.
On the contrary, evidence collected directly from infants reveals
that they display the same memory dissociations as adults in
response to the same independent variables on tasks analogous
to those used to distinguish these systems. Moreover, data collected in the delayed-recognition paradigm over the first 18
months of life (see Figure 4) reveal a striking developmental
continuity over a period previously thought to be marked by
discontinuities of one sort or another, including the emergence
of explicit memory and language. This continuity in infants'
delayed recognition is independent of task and response system
(Hartshorn & Rovee-Collier, 1997; Hartshorn et al., in press).
Taken together, infants' memory dissociations and the developmental continuity in their memory performance reveal that the
assumption that the implicit and explicit memory systems mature at different rates during the 1st year of life is fundamentally
incorrect. If there indeed are two memory systems, then they
develop simultaneously and not sequentially from early in life.
Crowder (1988) argued that the important question is not
whether different tasks and different independent variables yield
dissociations but what such dissociations portend regarding the
question of underlying memory systems. Murdock (1988) noted
that although experimental dissociations might be expected if
there are separate and distinct underlying memory systems, the
finding of experimental dissociations does not confirm that they
actually exist. A similar argument was made by Olton (1989),
who took issue with the fact that most double dissociations,
which are often taken as evidence of functional dissociations
and dichotomies in neuropsychological experiments, have been
491
obtained with only a single set of parameters. After demonstrating how different levels of a variable such as task demand
can lead to different outcomes with different interpretations, he
concluded that such data "are not capable of proving a dichotomy at any level of analysis" (Olton, 1989, p. 163) and proposed that theories of memory should emphasize dimensions
rather than dichotomies.
In fact, the dissociations in infants' memory performance in
the reactivation and delayed-recognition tasks are conducive to
an analysis of this sort. The long recognition latencies at 3
and 6 months clearly demonstrate that reactivation (priming) is
strictly a perceptual identification process that proceeds more
or less automatically, much like parallel processing (see also
Jacoby, 1983; Jacoby & Dallas, 1981 ). The reactivation or priming task reveals what of the information that was originally
encoded is still available in memory (see also Treisman, 1992).
What the delayed-recognition task entails is a more difficult
problem and one with which I, like Olton and numerous other
researchers, have wrestled for some time. In general, I find it
useful to conceptualize of memory in terms of a series of processing stages. This succession of stages necessarily begins with
perceptual processing because what is perceived (i.e., encoded)
provides the data upon which the memory processes operate.
The delayed-recognition task must reveal the product of subsequent processing stages in which information that is perceived
at the time of testing is integrated with previous memory tokens
that have been retrieved into short-term or working memory and
given meaning (for discussion, see Rovee-Collier, 1995, and
Rovee-Collier, Borza, et al., 1993). By this very sketchy account, reactivation or priming reflects one extreme of a memoryprocessing continuum, and delayed recognition reflects a point
near, but perhaps not yet at, the other extreme. By this account,
a memory failure could reflect a disruption of processing at any
of several points along this continuum.
Whatever account of memory processing ultimately proves
to be most satisfactory, accounts based on simple dichotomies
are bound to be wrong. Most certainly, they are unlikely to
capture the richness of representational systems or processes
that have evolved in different species under different selection
pressures (Oakley, 1983; Sherry & Schacter, 1987). Roediger
(1990) speculated that five major systems and 20 subsystems,
at a minimum, would be necessary to accomplish this, and
Johnson ( 1983, 1992) proposed a unitary memory system (multiple-entry modular system or MEM) with 16 subsystems or
modules to account for the many varieties of memory. The popularity of simple dichotomies is likely to persist for some time,
however, because dichotomies, like two-way interactions, are
easier to contemplate than systems or subsystems entailing 16or 20-way interactions, or more.
To summarize, this article presented evidence collected in
studies with preverbal infants that refutes the notion that two
separable and functionally distinct memory systems mature at
different rates during the 1st year of life. The core argument
was that very young infants exhibit memory dissociations that
resemble those exhibited by adults with normal memory on
memory tasks that are used to distinguish these systems. The
data demonstrate that implicit and explicit memory develop simultaneously rather than sequentially in infancy and challenge
492
ROVEE-COLLIER
the utility of conscious recollection as a defining characteristic
of explicit memory.
Cognitive neuroscience is currently poised to move beyond
the level of simple classification and seek the actual mechanisms
that underlie memory performance. The robust experimental
dissociations and the developmental continuity in the memory
performance of preverbal infants point to the infancy period as
a promising place to begin the search.
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Received M a r c h 26, 1996
Revision received September 24, 1996
Accepted September 24, 1996 •