Neuropsychology
1996, Vol. 10, No. 1, 57-65
Copyright 1996 by the American Psychological Association, Inc.
0894-4105/96/$3.00
Explicit and Implicit Memory in the Elderly: Evidence for Double
Dissociation Involving Medial Temporal- and Frontal-Lobe Functions
Gordon Winocur, Morris Moscovitch, and Donald T. Stuss
R o t m a n Research Institute of Baycrest Centre for Geriatric Care
Groups of normal old people living in institutions or in the community and young adults were
administered tests of implicit (IM) and explicit (EM) memory with word-stem (WSC) and
word-fragment (WFC) completion paradigms. Neuropsychological tests sensitive to frontal and
medial temporal lobe function were also administered. Age differences were observed on both tests
of EM and on all neuropsychological tests. Priming effects on WSC were smaller in the
institutionalized group than the other 2 groups. Comparisons of EM and IM test results with
neuropsychological test scores revealed several effects, including significant correlations (a)
between EM scores on both tests and performance on standard memory tests in both aged groups
and (b) between IM scores of both aged groups on WSC and frontal-lobe test performance. The
results provide evidence of a double dissociation with respect to involvement of brain regions in
EM and IM. They also indicate that repetition priming in WSC and WFC involve different
mechanisms and that frontal-lobe dysfunction is a factor in reduced priming on the WSC test.
identification in a word completion test are common examples
of implicit tests of memory. In general, cognitive processes that
underlie normal performance on such tests are preserved in
old age (see Howard, 1991; Light & LaVoie, 1993, for reviews),
but there are notable exceptions (Chiarello & Hoyer, 1988;
Davis et al., 1990; Howard, Shaw, & Heisey, 1986; Hultsch,
Masson, & Small, 1991; Rose, Yesavage, Hill, & Bower, 1986).
A primary purpose of the present study was to investigate
one type of implicit memory (word-stem completion) on which
age differences have been reported and to examine these
differences from a neuropsychological perspective. Word
completion as a measure of priming is usually studied in one of
two ways. In word-fragment completion, the individual is presented
initially with the complete word and then at test is given a
sample of the word's letters (e.g., s o l d i e r ; _ o _ _ i _ r); in
word-stem completion, the study phase is the same, but at test,
the first three letters of the target word are presented (e.g.,
soldier; s o l . . . .
) . In both cases, at test, the individual is
instructed to respond with the first word that comes to mind.
Comparisons of old and young people on tests of wordfragment completion reliably show no differences (Light &
Lavoie, 1993), but at least three investigations of word-stem
completion found less priming in aged individuals (Chiarello &
Hoyer, 1988; Davis et al., 1990; Hultsch et al., 1991).
Hultsch et al. (1991) speculated that inconsistent findings of
age effects in word completion priming studies are related to
the extent to which implicit tests are contaminated by explicit
memory. Critical differences in experimental procedure may
bias individuals toward using conscious memory strategies that
put the elderly at a disadvantage. For example, this would
occur if an explicit test of memory were administered prior to
the implicit priming test or if instructions for the priming test
implied that memory would be tested. However, after careful
examination, Hultsch et al. (1991) concluded that reduced
priming by old people on word-stem completion tests represented a legitimate age effect independent of contaminating
influences of explicit memory.
Memory loss is a frequent complaint of the elderly, but
extensive research over several decades has shown that not all
aspects of memory function decline at the same rate. Age
differences favoring young adults are most consistently reported on explicit (or direct) tests of memory that use recall or
recognition techniques to assess conscious recollection of
contextually based information. This type of memory loss is
often attributed to progressive deterioration of the hippocampus, a medial temporal lobe brain region that is critical to
memory function and known to be particularly sensitive to the
aging process (Albert & Stafford, 1986; Milner, 1966; Tomlinson, 1972).
Implicit (or indirect) tests of memory do not refer to specific
events. In these tests, memory is assessed by the effects of
experience on some measure of performance that does not
involve conscious awareness of any part of the prior experience. Tests of general knowledge, skill learning, and repetition
priming in which exposure to a word biases subsequent
Gordon Winocur, Rotman Research Institute of Baycrest Centre
for Geriatric Care, Toronto, Ontario, Canada, Department of Psychology, Trent University, Peterborough, Ontario, Canada, and Departments of Psychology and Psychiatry, University of Toronto, Toronto,
Ontario, Canada; Morris Moscovitch, Department of Psychology,
Erindale College, University of Toronto and Rotman Research Institute of Baycrest Centre for Geriatric Care; Donald T. Stuss, Rotman
Research Institute of Baycrest Centre for Geriatric Care and Departments of Psychology and Medicine (Neurology), University of Toronto,
Toronto, Ontario, Canada.
This research was supported by grants from the Medical Research
Council of Canada and the Ontario Mental Health Foundation. We
thank Lars Nyberg and Marko Jelicic for comments on an earlier
version of this article. Portions of this research were presented at the
Annual Meeting of the Memory Disorders Research Society, Boston,
October 1994.
Correspondence concerning this article should be addressed to
Gordon Winocur, Rotman Research Institute of Baycrest Centre for
Geriatric Care, 3560 Bathurst Street, North York, Ontario, Canada,
M6A 2El. Electronic mail may be sent to [email protected].
57
58
WINOCUR, MOSCOVITCH, AND STUSS
There is a suggestion in the neuropsychological literature
that word completion performance is not always normal in
memory-impaired individuals (Squire, Shimamura, & Graf,
1987) and that stem completion may be mediated by frontal
lobe regions of the brain. Mayes and Gooding (1989) tested a
mixed group of brain-damaged amnesia patients on new
associative priming in a word-stem completion task. One of the
interesting findings was that priming effects in the amnesia
patients, several of whom were Korsakoff patients with probable frontal lobe dysfunction, correlated significantly with
performance on the FAS test of verbal fluency (Borkowski,
Benton, & Shapiro, 1967). Similarly, a significant correlation
between word-stem completion and performance on the Wisconsin Card Sorting Test (WCST), a test of frontal-lobe
function, was observed in normal old people by Davis et al.
(1990). On the other hand, it should be noted that Shimamura,
Gershberg, Jurica, Mangels, and Knight (1992) observed
normal word-stem priming in a group of 6 patients with
frontal-lobe damage. On balance, overall pattern of results
challenge the widely held view that word-stem completion is
dependent primarily on perceptual identification mechanisms
(Schacter, 1992; Tulving & Schacter, 1990) and suggest that
nonperceptual mechanisms are also involved (Keane, Gabrieli,
Fennema, Growdon, & Corkin, 1991).
In contrast, word-fragment completion is probably a more
purely perceptual priming test and as such relies more heavily
on posterior brain mechanisms involved in word identification
(Keane et al., 1991; Moscovitch, Vriezen, & Goshen-Gottstein,
1993; Schacter, 1992). The available evidence indicates that
word-stem and word-fragment completion involve different
cognitive operations that are mediated by different neural
structures. Because the frontal lobes appears to be more
vulnerable to aging effects than posterior regions (Coffey et al.,
1992; Fuster, 1989), it can be hypothesized that performance
on word-stem completion and word-fragment completion would
be affected differentially in old age.
In the present study, groups of young and old adults were
compared on explicit and implicit tests with word stems and
word fragments as partial cues. A primary purpose was to
confirm selective age-related effects on word-stem completion
and, if successful, to determine if reduced priming on this test
is related to impaired frontal-lobe function, as assessed by
standard neuropsychoiogical tests (e.g., Wisconsin Card Sorting, FAS). No such correlations were predicted for wordfragment completion. All participants were also administered
explicit tests of cued recall, along with standard memory tests
that involve conscious recollection (California Verbal Learning Test, Rey, and free recall). There was no a priori reason to
expect that age would differentially affect performance on
explicit tests that were cued by word stems or word fragments,
but it was predicted that age differences in cued recall would
correlate with performance on the standard memory tests.
The elderly participants were divided into institutionalized
and community-dwellinggroups. Participants from both environments were selected according to identical criteria that
controlled for effects of relevant variables such as age, health,
IQ, and education. In previous work (Moscovitch & Winocur,
1983; Winocur & Moscovitch, 1983, 1990), we found that old
people living in institutions consistently performed worse on
some tests of cognitive function than carefully matched counterparts living in the community. These differences were most
apparent on tests of frontal-lobe and medial temporal-lobe
function, suggesting that these regions of the brain were
particularly affected by the combined effects of aging and
institutionalization. It was of interest to determine if differences between institutionalized and community-dwelling participants extended to the cognitive and memory functions
under investigation in the present study.
Method
Participants
A total of 50 old adults (age range = 70-85 years) and 29 young
adults (age range = 20-35 years), livingin the Peterborough, Ontario,
Canada, area, served as participants in this experiment. Of the elderly
sample, 26 lived in senior citizens' residences (institutionalized old;
group INS), and 24 lived in their own homes (community old; group
COM). The young adult group was recruited primarily through
newspaper ads.
All groups were comprised according to the same criteria. To
qualify, participants had to be free of gross cognitive deficits or
neurological conditions; anyone with a history of stroke or serious
cardiovascular disease, chronic psychiatric problems, or sensory or
perceptual disorders, was excluded from the study, as were people
receivingmedication that affected mood or thought processes. Medical
information was obtained from various sources, including a health
checklist, medical records, relatives, attending physicians, and other
health care providers. In all cases, permission to obtain this information was obtained from the participants. As part of the screening
process, all prospective participants were administered the Vocabulary subscale of the Wechsler Adult Intelligence Scale (Wechsler,
1981) (WAIS) and the CES Depression Scale (Radloff, 1977). Only
those individuals scoring at least in the normal range on these tests
were included in the study.
Participants were also selected according to educational background and socioeconomiclevel. All those in the research had been to
school for at least 8 years, and most had completed high school. For
the most part, participants were drawn from middle-income levelswith
a wide range of professional and semiskilled occupations represented.
Table 1 provides a summary of demographic and screening information for all groups. The three groups were similar in terms of the
controlled variables.
Test Materials and Procedure
Two sets of 60 familiar nouns were created---one for the word-stem
completion (WSC) tasks and the other for the word-fragment compleTable 1
Characteristics of Participants in the Three Study Groups
Institutionalized
Community
Young
Characteristic
M
SD
M
SD
M
SD
Age (years)
Education (years)
WAIS Vocabulary
(absolute score)
CES--Depression
Scale (score)
79.2
11.7
5.89
2.20
77.8
11.9
6.11
2.51
27.3 5.06
12.8 2.28
53.7
7.09
56.4
7.01
5 2 . 6 6.74
11.4
2.56
11.5
2.96
10.8 2.44
Note. CES = Center for EpidemiologicalStudies; WAIS = Wechsler
Adult Intelligence Scale.
59
EXPLICIT AND IMPLICIT M E M O R Y
tion (WFC) tasks. All words in the WSC lists contained five letters.
Each word began with a different three-letter stem that could be
completed to form several words. All words in the WFC lists consisted
of six letters. The stimulus words, 40 in each set, were printed in large
black letters on 3 × 5 in. (8 x 13 cm) white index cards.
All participants received explicit and implicit versions of the WSC
and WFC tasks. Half of the participants received the WSC tasks
followed approximately 6 weeks later by the WFC tasks; the other half
were tested in the reverse order.
Training and testing procedures were similar for both tasks. Initially,
in both cases the 40 stimulus words were presented one at a time to
each participant. As each word was presented, the participant was
instructed to tell the examiner how many vowels there were in the
word. A second presentation trial followed in which the words were
shown in the same way, but this time participants were asked to read
aloud each word. Testing followed a 20-min delay that was filled with
nonverbal testing (e.g., Rey-Osterrieth and line orientation), and
distracting conversation. For each test condition, the participant was
given three response sheets, each consisting of 20 incomplete words.
On two of the sheets, the letter cues referred to 20 stimulus words, and
on the third to 20 control words that the participants had not seen
before. The control words were included to provide baseline estimates
of word completion.
For WSC testing, the first three letters for each of the 60 words were
presented followed by two blank lines (e.g., beach; B e a __). For
WFC testing, three of the six letters were presented as cues, separated
by blank lines (e.g., radish; __ a d _ __ h). The selection of letters as
cues was arbitrary in each case.
Test instructions were read aloud to each participant and were the
same for WSC and WFC testing. Instructions for implicit recall, which
preceded one list of stimulus words and the list of control words, were
as follows:
Here we have a list of parts of some common words. What I want
you to do is fill out these words to make the first word that comes
to mind.
Rey-Osterrieth Complex Figure Test. In this test, the individual
initially copies a complex line drawing and 20 rain later reproduces it
from memory. Standardized scoring procedures are used to assess
performance at test. Deficits in recalling the drawing are associated
with right temporal lobe dysfunction (Taylor, 1969).
California Verbal Learning Test (CVL T). The CVLT is a widely
used standardized test of short- and long-term free recall of a
categorized list (Delis, Kramer, Kaplan, & Ober, 1987). In this test,
four words from each of four categories are presented aurally in a
mixed order, and the participant recalls as many of the 16 words as
possible. The list was presented five times with recall tested following
each presentation according to the procedure described by Delis et al.
(1987).
Delayed recall. A single list of 10 familiar words was constructed
and printed in bold, black letters on white index cards. At study, the
words were presented one at a time at a 2-s rate, and the participant
was instructed to read each word aloud and be prepared recall them
later. The list was presented once only and followed by a 60-s delay
during which the participant was engaged in distracting conversation.
A test of free recall followed in which the participant was instructed to
provide as many words as possible in any order from the preceding list.
This test was based on a similar test on which old people were
impaired relative to young adults (Winocur & Moscovitch, 1990).
Results
T h e m e a n p r o p o r t i o n s o f c o r r e c t w o r d c o m p l e t i o n s in t h e
explicit a n d implicit v e r s i o n s o f t h e W F C a n d W S C tasks are
p r e s e n t e d in T a b l e 2. In all cases, t h e s c o r e s w e r e d e r i v e d f r o m
t h e o b t a i n e d value for p a r t i c i p a n t s m i n u s t h e i r b a s e l i n e levels.
B a s e l i n e m e a s u r e s in t h e c o n t r o l c o n d i t i o n o f e i t h e r task
r e p r e s e n t e d t h e p r o p o r t i o n o f c o m p l e t e d w o r d s that m a t c h e d
t h e t a r g e t words. T h e m e a n b a s e l i n e r a t e s for W F C a n d W S C
across all g r o u p s was .17 a n d .19 respectively. T h e r e w e r e n o
d i f f e r e n c e s b e t w e e n g r o u p s o n t h e s e m e a s u r e s n o r did b a s e l i n e
s c o r e s c o r r e l a t e with n e u r o p s y c h o l o g i c a l test p e r f o r m a n c e .
The instructions for explicit recall, which preceded one list of stimulus
words, were as follows:
Explicit Memory
Here we have a list containing parts of words that I showed you
earlier on the cue cards. What I want you to do is fill these words
correctly, so that they match the words you saw on the cue cards.
The order of list presentation was randomly determined for each
participant. The participants were instructed to respond as quickly as
possible and advised that they had 3 min to complete each task.
During the interval between WSC and WFC testing, participants
were administered a series of neuropsychological tests. The tests were
usually administered on two or three occasions, each separated by
about a week. The following is a summary of each test, including the
Rey-Osterrieth test, which was administered between the WSC study
and test trials.
Wisconsin Card Sorting Test. This is a standardized test of set
formation and attentional shift in which participants sort cards
containing multidimensional drawings into different categories. The
procedure followed in this study has been described in detail by Milner
(1964). The test yields several measures believed to be sensitive to
frontal-lobe dysfunction (Milner, 1964); those reported here are total
errors and perseverative errors.
Word fluency. In this test, individuals are asked to generate orally
words beginning with the letters, F, A, S, with 1 min allowed for each
letter (Borkowski et al., 1967). The measure reported here is the total
number of words produced in 3 min. The test is widely used to assess
frontal lobe damage in clinical populations (Milner, 1964).
A s e x p e c t e d , t h e p r o p o r t i o n s o f c o r r e c t r e s p o n s e s in b o t h
explicit tests o f m e m o r y w e r e h i g h e r in t h e y o u n g g r o u p t h a n
t h e a g e d g r o u p s . This was c o n f i r m e d by s e p a r a t e analyses o f
v a r i a n c e ( A N O V A s ) , w h i c h r e v e a l e d significant g r o u p effects
in t h e W S C , F ( 2 , 76) = 4.29, p < .001, a n d t h e W F C , F ( 2 ,
76) = 41.61, p < .001, v e r s i o n s o f c u e d recall. P o s t h o c
c o m p a r i s o n s , c o n d u c t e d with t h e T u k e y test, s h o w e d t h a t
e p i s o d i c m e m o r y was n o t a f f e c t e d by type o f c u e i n g in any o f
the groups.
Table 2
Mean Proportion o f Words Correctly Recalled on Explicit
Version of Word-Stem Completion (WSC) and Word-Fragment
Completion (WFC) Tests
WSC
WFC
Group
M
SD
M
SD
Institutionalized
Community-dwelling
Young
.29
.38
.46
.12
.09
.13
.26
.35
.38
.12
.14
.11
Note. Values represent each participant's obtained mean of each
participant's recall score minus the baseline score.
60
WINOCUR, MOSCOVITCH, AND STUSS
the two aged groups on all measures although by the Tukey
test differences between the young and community-dwelling
groups on the WCST measures approached statistical significance (both ps < .10). Significant differences favoring the
community-dwelling group were observed between the two
aged groups on both W C S T measures (bothps < .01) and the
FAS test (p < .01). Overall, these results indicated an effect
of normal aging and a combined effect of aging and institutionalization on frontal-lobe function.
Medial temporal lobe. The memory tests yielded a similar
pattern of results. Significant differences in group performance
were observed on the CVLT, F(2, 76) = 43.28, p < .001,
Rey-Osterrieth test, F(2, 76) = 13.76, p < .001, and the
Delayed recall test, F(2, 76) = 41.62,p < .001.
Tukey tests conducted on the CVLT scores showed that the
three groups differed significantly from each other on the
CVLT and Delayed recall tests (ps < .05). On both tests, the
highest mean scores were obtained by the young group,
followed by the community-dwelling group and the institutionalized group.
A slightly different pattern was observed on the ReyOsterrieth test. On this test, the institutionalized group was
significantly worse than the young group (p < .01) and the
community-dwelling group ( p < .05). Although the young
group appeared to perform better than the communitydwelling group, the difference did not reach statistical significance (p < .10).
Table 3
Mean Proportion of Correct Word Completion on the Implicit
Version of the Word-Stem Completion (WSC) and
Word-Fragment Completion (WFC) Tests
WSC
WFC
Group
M
SD
M
SD
Institutionalized
Community-dwelling
Young
.13
.17
.20
.12
.09
.10
.17
.19
.20
.15
.09
.11
Note. Values represent each participant's obtained priming score
minus baseline score.
Table 2 shows that the young group's proportion of correct
scores generally was higher than those for the INS and C O M
groups. Post hoc comparisons showed that on the WSC test the
three groups differed significantly from each other (ps < .01),
indicating an overall age effect, as well as an adverse effect of
institutionalization on cued recall performance. O n the W F C
test, the INS group differed significantly from the C O M and
young groups, but the latter groups did not differ from each
other.
Implicit Memory
Table 3 shows that the proportion of word completion scores
in implicit memory testing did not vary among groups on the
W F C task. However, on the WSC task, the institutionalized
group completed fewer stimulus words than the communitydwelling and young groups. These observations were confirmed by an A N O V A that revealed a significant difference
between groups on the WSC test, F(2, 76) = 3.38,p < .05, but
not on the W F C test, F(2, 76) < 1. Subsequent analysis with
the Tukey test showed that the group effect on the WSC test
resulted from significant differences between the institutionalized group and the other two groups on the WSC task
(ps < .05).
Correlations Between Test Scores
Pearson correlation coefficients were computed for each
group to assess relationships between performance on the
explicit and implicit versions of the WSC and W F C tasks and
the neuropsychological test scores. The coefficients are presented in the correlation matrices of Tables 5 and 6.
Institutionalized group. Examination of the correlation matrices for the institutionalized group reveals a clear double
dissociation involving the explicit (see Table 5) and implicit
(see Table 6) memory scores on the WSC test and their
neuropsychological correlates. This group's mean score on the
WSC implicit test correlated significantly with its FAS test
score (r = .55; p < .01) and its WCST error scores (total
errors: r = - . 4 7 ; p < .025; perseverative errors: r = - .45;
p < .025). At the same time, performance on the explicit
memory version of the WSC task correlated significantly with
performance on the Delayed recall test (r = .47;p < .025) and
CVLT (r = .54; p < .01). The explicit and implicit memory
Neuropsychological Test Scores
Mean scores for the three groups on all neuropsychological
tests are presented in Table 4. The tests are organized as
measures of frontal-lobe and medial temporal-lobe function.
Frontal lobe. Strong group differences were observed on
both tests of frontal-lobe f u n c t i o n - - t h e WCST, total errors,
F(2, 76) = 19.29, p < .001; perseverative errors, F(2, 76) =
14.00,p < .001, and the FAS fluency task, F(2, 76) = 34.11,
p < .001. The young group consistently performed better than
Table 4
Neuropsychological Test Scores for All Study Groups
CVLT
WCST error
Delayed
recall
Rey
FAS
Total
Perseverative
Group
M
SD
M
SD
M
SD
M
SD
M
SD
M
SD
Institutionalized
Community-dwelling
Young
32.08
48.08
60.07
12.81
10.78
8.46
11.90
16.79
20.16
6.40
5.70
5.41
3.04
4.25
6.03
1.25
1.03
1.35
26.27
37.17
46.21
8.76
9.37
8.73
24.89
12.46
8.66
12.81
8.82
7.82
11.92
5.71
3.72
5.86
6.65
5.30
Note. CVLT = California Verbal Learning Test; Rey = Rey-Osterrieth Complex Figure Test; FAS = commonly used name for the Controlled
Oral Word Association Test or Word Fluency Test; WCST = Wisconsin Card Sorting Test.
EXPLICIT AND IMPLICIT MEMORY
scores on the WSC task did not correlate significantly with
each other.
Performance by the institutionalized group on the W F C explicit memory test was found to correlate significantly with
the Delayed recall test (r = .45; p < .02), C V L T (r = .48;
p < .025), and the WSC-explicit memory test score (r = .51;
p < .025). The WFC-implicit memory score did not correlate
significantly with performance on any other test, although the
correlation between performance on this test and that of the
WSC-implicit memory test approached statistical significance
(r = .38;p < .10).
Examination of the neuropsychological tests for the INS
group revealed significant correlations between the Delayed
recall test score and the C V L T (r = .83; p < .001) and FAS
(r = .39; p < .05) tests, and between FAS and W C S T error
scores (total errors: r = - . 4 4 ; p < .05; perseverative errors:
r = - . 4 8 ; p < .025).
Community-dwelling group. A double dissociation, implicating different functions in explicit and implicit memory
performance on the WSC task was also observed in the
community-dwelling group. As in the institutionalized group,
the WSC-implicit memory test score correlated significantly
with the FAS (r = .54; p < .01) and W C S T total errors
(r = - . 4 5 ; p < .05) and perseverative errors (r = - . 5 7 ;
p < .01) score (see Table 5). The community-dwelling group's
score on the WSC-explicit memory test correlated significantly
with the C V L T score (r---.44; p < .05), but not with the
Delayed recall score (r = .28; p < .20; see Table 6). Interestingly unlike the institutionalized group, for the communitydwelling group, the correlation between the explicit and
implicit versions of the WSC test did reach statistical significance (r = .44;p < .05).
The correlation between the WFC-explicit memory score
and the WSC-explicit memory score was statistically significant
(r = .40; p < .05). The community-dwelling group's W F C explicit memory score also correlated significantly with its
scores on the Delayed recall test (r = .43; p < .05) and the
R e y - O s t e r r i e t h test (r = .40). The correlation between the
Table 5
Correlation Between Scores of Institutionalized and
Community-Dwelling Elderly on Explicit Versions of Word-Stem
Completion (WSC) and Word-Fragment Completion (WFC)
Tests and Scores on Neuropsychological Tests
Explicit test scores
Type of
task
WCST errors
FAS
Total
Perseverative
CVLT
Rey
Delayed
recall
.54***
.48**
.36
.12
.47**
.45**
.23
.40*
.28
.43*
Institutionalized
WSC
WFC
.27
-.17
-.11
-.12
-.04
.09
Community-dwelling
WSC
WFC
.06
.20
-.31
-.04
-.35
-.03
.44*
.36
Note. FAS = commonly used name of Controlled Oral Word
Association Test or Word Fluency Test; WCST = Wisconsin Card
Sorting Test; CVLT = California Verbal Learning Test; Rey =
Rey-Osterrieth Complex Figure Test.
*p < .05. **p < .025. ***p < .01.
61
Table 6
Correlation Between Scores of Institutionalized and
Community-Dwelling Elderly on Implicit Versions of Word-Stem
Completion (WSC) and Word-Fragment Completion (WFC)
Tests and Scores on Neuropsychological Tests
Implicit test scores
WCST errors
Type of
task
FAS
Total
WSC
WFC
.55***
.12
-.47**
.08
WSC
WFC
.54**
.10
-.45*
.10
Perseverative
CVLT
Rey
-.09
.01
.28
-.30
Delayed
recall
Institutionalized
-.45**
.00
.20
.11
Communi~-dwelling
-.57***
-.02
.31
-.05
.03
.47*
-.01
-.16
Note. FAS = commonly used name of Controlled Oral Word
Association Test or Word Fluency Test; WCST = Wisconsin Card
Sorting Test; CVLT = California Verbal Learning Test; Rey =
Rey-Osterrieth Complex Figure Test.
*p < .05. **p < .025. ***p < .01.
WFC-explicit and the C V L T test scores approached significance (r = .36;p < .10).
As in the institutionalized group, the Delayed recall test
score correlated significantly with the C V L T score (r = .60;
p < .01), although the significant correlation observed between the Delayed recall and F A S scores in the institutionalized group was not found in the community-dwelling group
(r = .23;p < .20). In the community-dwelling group, the F A S
score correlated significantly with the C V L T score (r = .44;
p < .05) and with the perseverative error score on the W C S T
(r = - . 4 2 ; p < .05). The correlation between the FAS and
W C S T test total score just failed to reach statistical significance (r = - . 3 4 ; p < .10).
Young group. There was very little relationship between
any of the scores obtained by the young group. The only
significant correlation was found between the WSC-implicit
memory and WFC-implicit memory scores (r = .47; p < .01).
The correlation between the two explicit memory scores was in
the expected direction but failed to achieve statistical significance (r = .26;p < .20).
Discussion
A major finding of the present study was a functional double
dissociation in old people between performance on implicit
and explicit tests on the one hand and performance on tests
sensitive to different brain regions on the other. The results
confirmed that age differences occur in word-stem completion
but not in word-fragment completion. In addition, we report
the novel finding that in old people performance on stem
completion, but not fragment-completion, was correlated with
tests of frontal lobe function, but not with standard and
laboratory tests of explicit memory. We also found the expected age difference on explicit versions of word-stem and
word-fragment completion. However, performance on the
explicit tests did not correlate with tests of frontal function but
correlated instead with scores on standard memory tests that
are sensitive to medial temporal lobe dysfunction.
62
WINOCUR, MOSCOVITCH, AND STUSS
It is not surprising that performance by older adults on stem
completion is not correlated with standard neuropsychological
tests of memory sensitive to medial temporal lobe damage.
This type of dissociation between implicit and explicit tests of
memory has been reported many times in normal individuals
and amnesia patients. The important finding is that stem
completion was correlated with several measures of frontallobe function. That this correlation did not hold for wordfragment completion indicates that different cognitive processes underlie the two types of priming. This aspect of the
results is consistent with the view that fragment completion is
perceptually driven and mediated by the posterior neocortex,
whereas stem completion has a substantial strategic component.
Another explanation for the pattern of correlations observed in the present study is that the relatively poor performance of old people on the frontal tests reflects overall
cognitive decline rather than selective impairment. Deficits in
WCST and FAS have been reported in patients with posterior
cortical lesions, and problems of initiation and word finding
may be observed in patients with language disorders, regardless of lesion location (Anderson, Jones, Tranel, Tranel, &
Damasio, 1990; Joanette & Goulet, 1986; Miceli, Caltagirone,
Gainotti, Massulo, & Silveri, 1981). It could be argued that
deficits in these functions, resulting from generalized cortical
atrophy, account for performance of old people on our
WSC-implicit and frontal tests. However, it is important to
note that participants in both aged groups were carefully
screened, with normal performance on WAIS Vocabulary an
important criterion for selection. As shown in Table 2, there
were no differences between any of the groups on this
measure. Moreover, a global deficit interpretation cannot
readily explain why WSC-implicit performance was selectively
impaired and WFC-implicit performance was spared. Indeed,
if old people were experiencing a severe and generalized
cognitive decline, a double dissociation of the type observed
here would be unlikely. Although there is no doubt that old
people perform worse than young people on many tests of
cognitive function, the present study shows that it is possible to
distinguish between decline in specific functions and relate
these impairments to corresponding decline in specific brain
regions.
To understand the nature of frontal lobe involvement in
stem completion, it is necessary to compare the pattern of
results on the explicit and implicit versions of stem completion.
The low correlation between performance on stem-cued recall
and tests of frontal function was predicted on the evidence that
frontal lobe damage normally does not affect performance on
explicit tests of memory that are cue-dependent and do not
involve strategic processes. Frontal-lobe involvement might be
expected on the explicit version of stem completion because of
its conceptually driven component. The apparent inconsistency is compounded by evidence that the frontal lobes are
implicated in the implicit test of stem completion, which
traditionally has been viewed as relying more on automatic,
perceptual processes (Blaxton, 1989; Jacoby, Lindsey, & Toth,
1992; Roediger, 1990).
To resolve this apparent inconsistency, we propose that
automatic and strategic processes can contribute to both
conscious recollection and implicit memory. This contrasts
with the traditional view that automatic processes are associated only with implicit memory and strategic processes with
conscious recollection. Moscovitch (1989, 1992) has postulated
that when the participant is aware of the proximal cues that are
linked most directly to the memory trace, access to the memory
trace is gained automatically. This automatic, cue-dependent
retrieval process operates via the medial temporal lobes if the
trace has been recentlY acquired. This interpretation accounts
for the observed correlation between performance on the
explicit versions of stem completion and fragment completion
and other memory tests sensitive to medial temporal-, but not
frontal-lobe damage. The frontal lobes are involved only if the
cues are inadequate and strategic search processes are necessary to identify the effective proximal cue.
With respect to implicit tests, the correlation between tests
of frontal-lobe function and performance on stem completion
makes the important point that despite being implicit strategic
processes are involved in performing this task. In contrast,
strategic processes do not contribute to performance on
fragment completion. Stem and fragment completion are
similar in that both include a perceptual component, and both
tests require participants to produce the first word that comes
to mind. However, they differ in the types of processes evoked
by the separate cues. In word-stem completion, there is a
strong generative component. The stem biases the participant
to search the lexicon for a word beginning with the stem. In this
regard, stem completion can be considered to be a variation of
letter fluency, a test which is known to be sensitive to
frontal-lobe dysfunction. Thus, word stems in addition to
triggering perceptual identification processes, initiate generative search processes. Fragment completion does not evoke
this strategy because unlike initial stems, letters drawn randomly from the word are poor cues for locating words in the
lexicon. Instead, fragment completion is best viewed as a
perceptual identification test in which the fragment evokes the
perceptual record of the target.
With respect to the idea that WSC in a priming task involves
a generative search process that implicates the frontal lobes,
the question arises as to whether a similar process occurs
during baseline performance. Because baseline WSC performance did not correlate with FAS performance in any of the
groups, that would not appear to be the case. In baseline
testing, the word stem elicits a single prepotent response.
Following priming, response alternatives are probably activated by the cue with the recently primed response vying with
the prepotent baseline response for selection. The latter
process is less automatic and more likely to involve the frontal
lobes than the former. This account suggests that the frontal
lobes may be involved in response-selection, as well as responsegenerative processes. The observed correlations between WSC
and FAS, a generative task, on the one hand, and between
WSC and WCST, a task with a significant selective component,
on the other hand, is consistent with this view.
Other investigators have also suggested that automatic and
strategic processes contribute to performance on implicit and
explicit tests of memory. The prevailing view is that no test of
memory is process pure: Strategic processes intrude on performance on implicit tests of memory, and conversely automatic,
63
EXPLICIT AND IMPLICIT MEMORY
implicit processes influence performance on explicit tests.
Acknowledging this position, we emphasize the importance of
the additional point we are making. In our view, there is also
an automatic component to conscious recollection that is
independent of the automatic implicit component. A similar
interpretation has been offered by other investigators who
contrast voluntary with involuntary processes in conscious
recollection (e.g., Richardson-Klavhen, Gardiner, & Java,
1994). In addition, we maintain that there is a strategic
component involved in generating responses on some implicit
tests that is independent of the strategic recollective process
that may be operative on explicit tests. J. D. E. Gabrieli
(October, 1994, personal communication) made a similar point
in demonstrating a generative component to some implicit
tests, like stem completion and category-exemplar generation,
which is selectively impaired in Alzheimer's disease.
The above framework accounts for the age-related deficits
we obtained, as well as for most of the functional dissociations
as revealed by different patterns of correlations among the
various implicit and explicit memory tests. However, there arc
some findings that still need to be explained. In the communitydwelling group, significant correlations were observed between
performance on delayed recall of the Rey-Osterrieth figure
and performance on explicit and implicit versions of fragment
completions. In this group, significant correlations were found
also between performance on explicit and implicit versions of
stem completion. It is tempting to attribute the source of these
correlations to perceptual components that the tests have in
common. The difficulty is that this interpretation would predict
other correlations that were not found. Specifically, performance on implicit and explicit tests of fragment completion did
not correlate with each other, nor were similar positive
correlations found in the institutionalized group.
The finding that age-related deficits in WSC-priming in old
people correlated with performance on frontal-lobe tests
appears to conflict with reports of normal WSC performance
in patients with Huntington's disease (HD) and in nondementia patients with Parkinson's disease (PD; e.g., Bondi &
Kaszniak, 1991; Heindel, Salmon, Shults, Walicke, & Butters,
1989; Huberman, Moscovitch, & Freedman, 1994). Of course,
such patients frequently show signs of frontal-lobe damage.
However, none of these studies provided information on the
relation between performance on WSC and performance on
tests that are sensitive to frontal lobe function. This information is crucial, given the great variability in performance on
frontal-lobe tests in these patients and in controls who themselves are usually old. It is important to bear in mind that in the
present study performance on WSC was correlated with
performance on frontal lobe tests in community-dwelling older
adults, even though their scores on WSC were not significantly
different from those obtained by young adults. Thus, the
absence of a significant deficit in WSC in patients with HD or
PD is not inconsistent with our hypothesis. It is expected that
in these patients, as in our older adults, performance on WSC
would correlate significantly with performance on frontal tests.
The present results confirm previous findings that institutionalization exacerbates the process of cognitive decline associated with aging. As in our previous studies, we found substantial group differences on standard neuropsychological tests of
frontal and medial temporal lobe function. Performance on
experimental tests of memory was consistent with these observations, as well as with the framework we have proposed. The
institutionalized group was most impaired on the explicit tests
that were correlated with standard tests of medial temporal
lobe function and on implicit stem completion, which was
correlated with frontal function. Importantly, there were no
statistical differences among the groups on implicit fragment
completion that is presumed to be mediated by posterior
neocortical structures that are relatively preserved with age.
Although we took great care to match institutionalized and
community-dwelling old people on psychological and healthrelated measures, it is clear that important differences remain
between these groups. For example, our own research, has
shown that the institutionalized elderly are more sensitive to
psychosocial factors that can adversely affect performance on
tests of medial temporal or frontal lobe function (Winocur &
Moscovitch, 1987). It may also be the case that institutionalized old people who outwardly appear normal for their age
may be at greater risk neurologically. Recently, Boone, Miller,
and Lesser (1993) studied a group of apparently normal old
people and found that 75% of participants over 70 years had
detectable vascular lesions in white matter. A small group of
these individuals had lesions of sufficient size to be associated
with frontal cognitive deficits. It is possible that this subgroup
is overrepresented in samples of normal institutionalized old
people. Further research is needed to determine the full range
of factors that differentiate healthy, high-functioning old
people living in institutions from those living in the community.
Our results have implications for issues related to aging and
the organization of memory. A point to emphasize is the
significance of the functional double dissociation that we
obtained. To our knowledge, this is one of the first demonstrations in a single study of differential decline with age of
separable memory functions mediated by different systems
(see also Glisky, Polster, & Routhieaux, 1995). The finding of a
double dissociation means that declines in performance with
age cannot be attributed to a uniform effect across all
functions, nor to a selective effect on those functions that are
most vulnerable in old age. Thus, our finding of frontal lobe
deficits in old people, for example, cannot be attributed to
diffuse brain dysfunction, as is sometimes claimed (Goldberg
& Bilder, 1987; Stuss & Gow, 1992).
Double dissociation studies have a distinct advantage over
single dissociation studies. By focusing only on a single
function and ignoring others, the single dissociation approach
can leave the impression that an observed deficit can be
attributed exclusively to the function being studied. In the
present study, the results show thht age differences in word
stem completion can be attributed to frontal-lobe, but not
medial temporal dysfunction, whereas the reverse is true of
explicit tests of memory.
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Received January 25, 1995
Revision received July 21, 1995
Accepted July 28, 1995 •