Neuropsychology Copyright 1996 by the American Psychological Association, Inc. 1996, Vol. 10, No. 1, 57-65 0894-4105/96/$3.00

Explicit and Implicit in the Elderly: Evidence for Double Dissociation Involving Medial Temporal- and Frontal-Lobe Functions

Gordon Winocur, Morris Moscovitch, and Donald T. Stuss Rotman 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. 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.

Memory loss is a frequent complaint of the elderly, but identification in a word completion test are common examples extensive research over several decades has shown that not all of implicit tests of memory. In general, cognitive processes that aspects of memory function decline at the same rate. Age underlie normal performance on such tests are preserved in differences favoring young adults are most consistently re- old age (see Howard, 1991; Light & LaVoie, 1993, for reviews), ported on explicit (or direct) tests of memory that use or but there are notable exceptions (Chiarello & Hoyer, 1988; recognition techniques to assess conscious recollection of Davis et al., 1990; Howard, Shaw, & Heisey, 1986; Hultsch, contextually based information. This type of memory loss is Masson, & Small, 1991; Rose, Yesavage, Hill, & Bower, 1986). often attributed to progressive deterioration of the hippocam- A primary purpose of the present study was to investigate pus, a medial temporal lobe brain region that is critical to one type of (word-stem completion) on which memory function and known to be particularly sensitive to the age differences have been reported and to examine these aging process (Albert & Stafford, 1986; Milner, 1966; Tomlin- differences from a neuropsychological perspective. Word son, 1972). completion as a measure of priming is usually studied in one of Implicit (or indirect) tests of memory do not refer to specific two ways. In word-fragment completion, the individual is presented events. In these tests, memory is assessed by the effects of initially with the complete word and then at test is given a experience on some measure of performance that does not sample of the word's letters (e.g., soldier; _ o_ _ i_ r); in involve conscious awareness of any part of the prior experi- word-stem completion, the study phase is the same, but at test, ence. Tests of general knowledge, skill learning, and repetition the first three letters of the target word are presented (e.g., priming in which exposure to a word biases subsequent soldier; s o l .... ). In both cases, at test, the individual is instructed to respond with the first word that comes to mind. Gordon Winocur, Rotman Research Institute of Baycrest Centre Comparisons of old and young people on tests of word- for Geriatric Care, Toronto, Ontario, Canada, Department of Psychol- fragment completion reliably show no differences (Light & ogy, Trent University, Peterborough, Ontario, Canada, and Depart- Lavoie, 1993), but at least three investigations of word-stem ments of Psychology and Psychiatry, University of Toronto, Toronto, completion found less priming in aged individuals (Chiarello & Ontario, Canada; Morris Moscovitch, Department of Psychology, Hoyer, 1988; Davis et al., 1990; Hultsch et al., 1991). Erindale College, University of Toronto and Rotman Research Insti- tute of Baycrest Centre for Geriatric Care; Donald T. Stuss, Rotman Hultsch et al. (1991) speculated that inconsistent findings of Research Institute of Baycrest Centre for Geriatric Care and Depart- age effects in word completion priming studies are related to ments of Psychology and Medicine (Neurology), University of Toronto, the extent to which implicit tests are contaminated by explicit Toronto, Ontario, Canada. memory. Critical differences in experimental procedure may This research was supported by grants from the Medical Research bias individuals toward using conscious memory strategies that Council of Canada and the Ontario Mental Health Foundation. We put the elderly at a disadvantage. For example, this would thank Lars Nyberg and Marko Jelicic for comments on an earlier occur if an explicit test of memory were administered prior to version of this article. Portions of this research were presented at the the implicit priming test or if instructions for the priming test Annual Meeting of the Memory Disorders Research Society, Boston, implied that memory would be tested. However, after careful October 1994. Correspondence concerning this article should be addressed to examination, Hultsch et al. (1991) concluded that reduced Gordon Winocur, Rotman Research Institute of Baycrest Centre for priming by old people on word-stem completion tests repre- Geriatric Care, 3560 Bathurst Street, North York, Ontario, Canada, sented a legitimate age effect independent of contaminating M6A 2El. Electronic mail may be sent to [email protected]. influences of .

57 58 WINOCUR, MOSCOVITCH, AND STUSS

There is a suggestion in the neuropsychological literature some tests of cognitive function than carefully matched coun- that word completion performance is not always normal in terparts living in the community. These differences were most memory-impaired individuals (Squire, Shimamura, & Graf, apparent on tests of frontal-lobe and medial temporal-lobe 1987) and that stem completion may be mediated by frontal function, suggesting that these regions of the brain were lobe regions of the brain. Mayes and Gooding (1989) tested a particularly affected by the combined effects of aging and mixed group of brain-damaged patients on new institutionalization. It was of interest to determine if differ- associative priming in a word-stem completion task. One of the ences between institutionalized and community-dwellingpar- interesting findings was that priming effects in the amnesia ticipants extended to the cognitive and memory functions patients, several of whom were Korsakoff patients with prob- under investigation in the present study. able frontal lobe dysfunction, correlated significantly with performance on the FAS test of verbal fluency (Borkowski, Method Benton, & Shapiro, 1967). Similarly, a significant correlation between word-stem completion and performance on the Wis- Participants consin Card Sorting Test (WCST), a test of frontal-lobe A total of 50 old adults (age range = 70-85 years) and 29 young function, was observed in normal old people by Davis et al. adults (age range = 20-35 years), livingin the Peterborough, Ontario, (1990). On the other hand, it should be noted that Shimamura, Canada, area, served as participants in this experiment. Of the elderly Gershberg, Jurica, Mangels, and Knight (1992) observed sample, 26 lived in senior citizens' residences (institutionalized old; normal word-stem priming in a group of 6 patients with group INS), and 24 lived in their own homes (community old; group frontal-lobe damage. On balance, overall pattern of results COM). The young adult group was recruited primarily through challenge the widely held view that word-stem completion is newspaper ads. dependent primarily on perceptual identification mechanisms All groups were comprised according to the same criteria. To (Schacter, 1992; Tulving & Schacter, 1990) and suggest that qualify, participants had to be free of gross cognitive deficits or neurological conditions; anyone with a history of stroke or serious nonperceptual mechanisms are also involved (Keane, Gabrieli, cardiovascular disease, chronic psychiatric problems, or sensory or Fennema, Growdon, & Corkin, 1991). perceptual disorders, was excluded from the study, as were people In contrast, word-fragment completion is probably a more receiving medication that affected mood or thought processes. Medical purely perceptual priming test and as such relies more heavily information was obtained from various sources, including a health on posterior brain mechanisms involved in word identification checklist, medical records, relatives, attending physicians, and other (Keane et al., 1991; Moscovitch, Vriezen, & Goshen-Gottstein, health care providers. In all cases, permission to obtain this informa- 1993; Schacter, 1992). The available evidence indicates that tion was obtained from the participants. As part of the screening word-stem and word-fragment completion involve different process, all prospective participants were administered the Vocabu- cognitive operations that are mediated by different neural lary subscale of the Wechsler Adult Intelligence Scale (Wechsler, 1981) (WAIS) and the CES Depression Scale (Radloff, 1977). Only structures. Because the frontal lobes appears to be more those individuals scoring at least in the normal range on these tests vulnerable to aging effects than posterior regions (Coffey et al., were included in the study. 1992; Fuster, 1989), it can be hypothesized that performance Participants were also selected according to educational back- on word-stem completion and word-fragment completion would ground and socioeconomic level. All those in the research had been to be affected differentially in old age. school for at least 8 years, and most had completed high school. For In the present study, groups of young and old adults were the most part, participants were drawn from middle-income levels with compared on explicit and implicit tests with word stems and a wide range of professional and semiskilled occupations represented. word fragments as partial cues. A primary purpose was to Table 1 provides a summary of demographic and screening informa- confirm selective age-related effects on word-stem completion tion for all groups. The three groups were similar in terms of the and, if successful, to determine if reduced priming on this test controlled variables. is related to impaired frontal-lobe function, as assessed by standard neuropsychoiogical tests (e.g., Wisconsin Card Sort- Test Materials and Procedure ing, FAS). No such correlations were predicted for word- Two sets of 60 familiar nouns were created---one for the word-stem fragment completion. All participants were also administered completion (WSC) tasks and the other for the word-fragment comple- explicit tests of cued recall, along with standard memory tests that involve conscious recollection (California Verbal Learn- ing Test, Rey, and ). There was no a priori reason to Table 1 expect that age would differentially affect performance on Characteristics of Participants in the Three Study Groups explicit tests that were cued by word stems or word fragments, Institutionalized Community Young but it was predicted that age differences in cued recall would Characteristic M SD M SD M SD correlate with performance on the standard memory tests. The elderly participants were divided into institutionalized Age (years) 79.2 5.89 77.8 6.11 27.3 5.06 and community-dwellinggroups. Participants from both envi- Education (years) 11.7 2.20 11.9 2.51 12.8 2.28 WAIS Vocabulary ronments were selected according to identical criteria that (absolute score) 53.7 7.09 56.4 7.01 52.6 6.74 controlled for effects of relevant variables such as age, health, CES--Depression IQ, and education. In previous work (Moscovitch & Winocur, Scale (score) 11.4 2.56 11.5 2.96 10.8 2.44 1983; Winocur & Moscovitch, 1983, 1990), we found that old Note. CES = Center for Epidemiological Studies; WAIS = Wechsler people living in institutions consistently performed worse on Adult Intelligence Scale. EXPLICIT AND IMPLICIT MEMORY 59 tion (WFC) tasks. All words in the WSC lists contained five letters. Rey-Osterrieth Complex Figure Test. In this test, the individual Each word began with a different three-letter stem that could be initially copies a complex line drawing and 20 rain later reproduces it completed to form several words. All words in the WFC lists consisted from memory. Standardized scoring procedures are used to assess of six letters. The stimulus words, 40 in each set, were printed in large performance at test. Deficits in recalling the drawing are associated black letters on 3 × 5 in. (8 x 13 cm) white index cards. with right temporal lobe dysfunction (Taylor, 1969). All participants received explicit and implicit versions of the WSC California Verbal Learning Test (CVL T). The CVLT is a widely and WFC tasks. Half of the participants received the WSC tasks used standardized test of short- and long-term free recall of a followed approximately 6 weeks later by the WFC tasks; the other half categorized list (Delis, Kramer, Kaplan, & Ober, 1987). In this test, were tested in the reverse order. four words from each of four categories are presented aurally in a Training and testing procedures were similar for both tasks. Initially, mixed order, and the participant recalls as many of the 16 words as in both cases the 40 stimulus words were presented one at a time to possible. The list was presented five times with recall tested following each presentation according to the procedure described by Delis et al. each participant. As each word was presented, the participant was (1987). instructed to tell the examiner how many vowels there were in the Delayed recall. A single list of 10 familiar words was constructed word. A second presentation trial followed in which the words were and printed in bold, black letters on white index cards. At study, the shown in the same way, but this time participants were asked to read words were presented one at a time at a 2-s rate, and the participant aloud each word. Testing followed a 20-min delay that was filled with was instructed to read each word aloud and be prepared recall them nonverbal testing (e.g., Rey-Osterrieth and line orientation), and later. The list was presented once only and followed by a 60-s delay distracting conversation. For each test condition, the participant was during which the participant was engaged in distracting conversation. given three response sheets, each consisting of 20 incomplete words. A test of free recall followed in which the participant was instructed to On two of the sheets, the letter cues referred to 20 stimulus words, and provide as many words as possible in any order from the preceding list. on the third to 20 control words that the participants had not seen This test was based on a similar test on which old people were before. The control words were included to provide baseline estimates impaired relative to young adults (Winocur & Moscovitch, 1990). 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; Bea __). For Results WFC testing, three of the six letters were presented as cues, separated The mean proportions of correct word completions in the by blank lines (e.g., radish; __ ad_ __ h). The selection of letters as cues was arbitrary in each case. explicit and implicit versions of the WFC and WSC tasks are Test instructions were read aloud to each participant and were the presented in Table 2. In all cases, the scores were derived from same for WSC and WFC testing. Instructions for implicit recall, which the obtained value for participants minus their baseline levels. preceded one list of stimulus words and the list of control words, were Baseline measures in the control condition of either task as follows: represented the proportion of completed words that matched the target words. The mean baseline rates for WFC and WSC Here we have a list of parts of some common words. What I want across all groups was .17 and .19 respectively. There were no you to do is fill out these words to make the first word that comes to mind. differences between groups on these measures nor did baseline scores correlate with neuropsychological test performance. 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 As expected, the proportions of correct responses in both correctly, so that they match the words you saw on the cue cards. explicit tests of memory were higher in the young group than The order of list presentation was randomly determined for each the aged groups. This was confirmed by separate analyses of participant. The participants were instructed to respond as quickly as variance (ANOVAs), which revealed significant group effects possible and advised that they had 3 min to complete each task. in the WSC, F(2, 76) = 4.29, p < .001, and the WFC, F(2, During the interval between WSC and WFC testing, participants 76) = 41.61, p < .001, versions of cued recall. Post hoc were administered a series of neuropsychological tests. The tests were comparisons, conducted with the Tukey test, showed that usually administered on two or three occasions, each separated by was not affected by type of cueing in any of about a week. The following is a summary of each test, including the the groups. Rey-Osterrieth test, which was administered between the WSC study and test trials. Table 2 Wisconsin Card Sorting Test. This is a standardized test of set formation and attentional shift in which participants sort cards Mean Proportion of Words Correctly Recalled on Explicit containing multidimensional drawings into different categories. The Version of Word-Stem Completion (WSC) and Word-Fragment procedure followed in this study has been described in detail by Milner Completion (WFC) Tests (1964). The test yields several measures believed to be sensitive to WSC WFC frontal-lobe dysfunction (Milner, 1964); those reported here are total errors and perseverative errors. Group M SD M SD Word fluency. In this test, individuals are asked to generate orally Institutionalized .29 .12 .26 .12 words beginning with the letters, F, A, S, with 1 min allowed for each Community-dwelling .38 .09 .35 .14 letter (Borkowski et al., 1967). The measure reported here is the total Young .46 .13 .38 .11 number of words produced in 3 min. The test is widely used to assess Note. Values represent each participant's obtained mean of each frontal lobe damage in clinical populations (Milner, 1964). participant's recall score minus the baseline score. 60 WINOCUR, MOSCOVITCH, AND STUSS

Table 3 the two aged groups on all measures although by the Tukey Mean Proportion of Correct Word Completion on the Implicit test differences between the young and community-dwelling Version of the Word-Stem Completion (WSC) and groups on the WCST measures approached statistical signifi- Word-Fragment Completion (WFC) Tests cance (both ps < .10). Significant differences favoring the community-dwelling group were observed between the two WSC WFC aged groups on both WCST measures (bothps < .01) and the Group M SD M SD FAS test (p < .01). Overall, these results indicated an effect Institutionalized .13 .12 .17 .15 of normal aging and a combined effect of aging and institution- Community-dwelling .17 .09 .19 .09 alization on frontal-lobe function. Young .20 .10 .20 .11 Medial temporal lobe. The memory tests yielded a similar Note. Values represent each participant's obtained priming score pattern of results. Significant differences in group performance minus baseline score. were observed on the CVLT, F(2, 76) = 43.28, p < .001, Rey-Osterrieth test, F(2, 76) = 13.76, p < .001, and the Table 2 shows that the young group's proportion of correct Delayed recall test, F(2, 76) = 41.62,p < .001. scores generally was higher than those for the INS and COM Tukey tests conducted on the CVLT scores showed that the groups. Post hoc comparisons showed that on the WSC test the three groups differed significantly from each other on the three groups differed significantly from each other (ps < .01), CVLT and Delayed recall tests (ps < .05). On both tests, the indicating an overall age effect, as well as an adverse effect of highest mean scores were obtained by the young group, institutionalization on cued recall performance. On the WFC followed by the community-dwelling group and the institution- test, the INS group differed significantly from the COM and alized group. young groups, but the latter groups did not differ from each A slightly different pattern was observed on the Rey- other. Osterrieth test. On this test, the institutionalized group was significantly worse than the young group (p < .01) and the Implicit Memory community-dwelling group (p < .05). Although the young group appeared to perform better than the community- Table 3 shows that the proportion of word completion scores dwelling group, the difference did not reach statistical signifi- in implicit memory testing did not vary among groups on the cance (p < .10). WFC task. However, on the WSC task, the institutionalized group completed fewer stimulus words than the community- dwelling and young groups. These observations were con- Correlations Between Test Scores firmed by an ANOVA that revealed a significant difference between groups on the WSC test, F(2, 76) = 3.38,p < .05, but Pearson correlation coefficients were computed for each not on the WFC test, F(2, 76) < 1. Subsequent analysis with group to assess relationships between performance on the the Tukey test showed that the group effect on the WSC test explicit and implicit versions of the WSC and WFC tasks and resulted from significant differences between the institutional- the neuropsychological test scores. The coefficients are pre- ized group and the other two groups on the WSC task sented in the correlation matrices of Tables 5 and 6. (ps < .05). Institutionalized group. Examination of the correlation ma- trices for the institutionalized group reveals a clear double Neuropsychological Test Scores dissociation involving the explicit (see Table 5) and implicit (see Table 6) memory scores on the WSC test and their Mean scores for the three groups on all neuropsychological neuropsychological correlates. This group's mean score on the tests are presented in Table 4. The tests are organized as WSC implicit test correlated significantly with its FAS test measures of frontal-lobe and medial temporal-lobe function. score (r = .55; p < .01) and its WCST error scores (total Frontal lobe. Strong group differences were observed on errors: r = -.47; p < .025; perseverative errors: r = - .45; both tests of frontal-lobe function--the WCST, total errors, p < .025). At the same time, performance on the explicit F(2, 76) = 19.29, p < .001; perseverative errors, F(2, 76) = memory version of the WSC task correlated significantly with 14.00,p < .001, and the FAS fluency task, F(2, 76) = 34.11, performance on the Delayed recall test (r = .47;p < .025) and p < .001. The young group consistently performed better than CVLT (r = .54; p < .01). The explicit and implicit memory

Table 4 Neuropsychological Test Scores for All Study Groups WCST error Delayed CVLT Rey recall FAS Total Perseverative Group M SD M SD M SD M SD M SD M SD Institutionalized 32.08 12.81 11.90 6.40 3.04 1.25 26.27 8.76 24.89 12.81 11.92 5.86 Community-dwelling 48.08 10.78 16.79 5.70 4.25 1.03 37.17 9.37 12.46 8.82 5.71 6.65 Young 60.07 8.46 20.16 5.41 6.03 1.35 46.21 8.73 8.66 7.82 3.72 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 61

scores on the WSC task did not correlate significantly with Table 6 each other. Correlation Between Scores of Institutionalized and Performance by the institutionalized group on the WFC- Community-Dwelling Elderly on Implicit Versions of Word-Stem explicit memory test was found to correlate significantly with Completion (WSC) and Word-Fragment Completion (WFC) the Delayed recall test (r = .45; p < .02), CVLT (r = .48; Tests and Scores on Neuropsychological Tests p < .025), and the WSC-explicit memory test score (r = .51; Implicit test scores p < .025). The WFC-implicit memory score did not correlate WCST errors significantly with performance on any other test, although the Type of Delayed correlation between performance on this test and that of the task FAS Total Perseverative CVLT Rey recall WSC-implicit memory test approached statistical significance Institutionalized (r = .38;p < .10). WSC .55*** -.47** -.45** -.09 .28 .20 Examination of the neuropsychological tests for the INS WFC .12 .08 .00 .01 -.30 .11 group revealed significant correlations between the Delayed Communi~-dwelling recall test score and the CVLT (r = .83; p < .001) and FAS (r = .39; p < .05) tests, and between FAS and WCST error WSC .54** -.45* -.57*** .31 .03 -.01 scores (total errors: r = -.44; p < .05; perseverative errors: WFC .10 .10 -.02 -.05 .47* -.16 r = -.48;p < .025). Note. FAS = commonly used name of Controlled Oral Word Community-dwelling group. A double dissociation, impli- Association Test or Word Fluency Test; WCST = Wisconsin Card Sorting Test; CVLT = California Verbal Learning Test; Rey = cating different functions in explicit and implicit memory Rey-Osterrieth Complex Figure Test. performance on the WSC task was also observed in the *p < .05. **p < .025. ***p < .01. community-dwelling group. As in the institutionalized group, the WSC-implicit memory test score correlated significantly WFC-explicit and the CVLT test scores approached signifi- with the FAS (r = .54; p < .01) and WCST total errors cance (r = .36;p < .10). (r =-.45; p < .05) and perseverative errors (r =-.57; As in the institutionalized group, the Delayed recall test p < .01) score (see Table 5). The community-dwelling group's score correlated significantly with the CVLT score (r = .60; score on the WSC-explicit memory test correlated significantly p < .01), although the significant correlation observed be- with the CVLT score (r---.44; p < .05), but not with the tween the Delayed recall and FAS scores in the institutional- Delayed recall score (r = .28; p < .20; see Table 6). Interest- ized group was not found in the community-dwelling group ingly unlike the institutionalized group, for the community- (r = .23;p < .20). In the community-dwelling group, the FAS dwelling group, the correlation between the explicit and score correlated significantly with the CVLT score (r = .44; implicit versions of the WSC test did reach statistical signifi- p < .05) and with the perseverative error score on the WCST cance (r = .44;p < .05). (r = -.42; p < .05). The correlation between the FAS and The correlation between the WFC-explicit memory score WCST test total score just failed to reach statistical signifi- and the WSC-explicit memory score was statistically significant cance (r = -.34;p < .10). (r = .40; p < .05). The community-dwelling group's WFC- Young group. There was very little relationship between explicit memory score also correlated significantly with its any of the scores obtained by the young group. The only scores on the Delayed recall test (r = .43; p < .05) and the significant correlation was found between the WSC-implicit Rey-Osterrieth test (r = .40). The correlation between the memory and WFC-implicit memory scores (r = .47; p < .01). The correlation between the two explicit memory scores was in Table 5 the expected direction but failed to achieve statistical signifi- Correlation Between Scores of Institutionalized and cance (r = .26;p < .20). Community-Dwelling Elderly on Explicit Versions of Word-Stem Completion (WSC) and Word-Fragment Completion (WFC) Discussion Tests and Scores on Neuropsychological Tests Explicit test scores A major finding of the present study was a functional double dissociation in old people between performance on implicit WCST errors Type of Delayed and explicit tests on the one hand and performance on tests task FAS Total Perseverative CVLT Rey recall sensitive to different brain regions on the other. The results Institutionalized confirmed that age differences occur in word-stem completion WSC .27 -.11 -.04 .54*** .36 .47** but not in word-fragment completion. In addition, we report WFC -.17 -.12 .09 .48** .12 .45** the novel finding that in old people performance on stem Community-dwelling completion, but not fragment-completion, was correlated with tests of frontal lobe function, but not with standard and WSC .06 -.31 -.35 .44* .23 .28 laboratory tests of explicit memory. We also found the ex- WFC .20 -.04 -.03 .36 .40* .43* pected age difference on explicit versions of word-stem and Note. FAS = commonly used name of Controlled Oral Word word-fragment completion. However, performance on the Association Test or Word Fluency Test; WCST = Wisconsin Card Sorting Test; CVLT = California Verbal Learning Test; Rey = explicit tests did not correlate with tests of frontal function but Rey-Osterrieth Complex Figure Test. correlated instead with scores on standard memory tests that *p < .05. **p < .025. ***p < .01. are sensitive to medial temporal lobe dysfunction. 62 WINOCUR, MOSCOVITCH, AND STUSS

It is not surprising that performance by older adults on stem conscious recollection and implicit memory. This contrasts completion is not correlated with standard neuropsychological with the traditional view that automatic processes are associ- tests of memory sensitive to medial temporal lobe damage. ated only with implicit memory and strategic processes with This type of dissociation between implicit and explicit tests of conscious recollection. Moscovitch (1989, 1992) has postulated memory has been reported many times in normal individuals that when the participant is aware of the proximal cues that are and amnesia patients. The important finding is that stem linked most directly to the memory trace, access to the memory completion was correlated with several measures of frontal- trace is gained automatically. This automatic, cue-dependent lobe function. That this correlation did not hold for word- retrieval process operates via the medial temporal lobes if the fragment completion indicates that different cognitive pro- trace has been recentlY acquired. This interpretation accounts cesses underlie the two types of priming. This aspect of the for the observed correlation between performance on the results is consistent with the view that fragment completion is explicit versions of stem completion and fragment completion perceptually driven and mediated by the posterior neocortex, and other memory tests sensitive to medial temporal-, but not whereas stem completion has a substantial strategic compo- frontal-lobe damage. The frontal lobes are involved only if the nent. cues are inadequate and strategic search processes are neces- Another explanation for the pattern of correlations ob- sary to identify the effective proximal cue. served in the present study is that the relatively poor perfor- With respect to implicit tests, the correlation between tests mance of old people on the frontal tests reflects overall of frontal-lobe function and performance on stem completion cognitive decline rather than selective impairment. Deficits in makes the important point that despite being implicit strategic WCST and FAS have been reported in patients with posterior processes are involved in performing this task. In contrast, cortical lesions, and problems of initiation and word finding strategic processes do not contribute to performance on may be observed in patients with disorders, regard- fragment completion. Stem and fragment completion are less of lesion location (Anderson, Jones, Tranel, Tranel, & similar in that both include a perceptual component, and both Damasio, 1990; Joanette & Goulet, 1986; Miceli, Caltagirone, tests require participants to produce the first word that comes Gainotti, Massulo, & Silveri, 1981). It could be argued that to mind. However, they differ in the types of processes evoked deficits in these functions, resulting from generalized cortical by the separate cues. In word-stem completion, there is a atrophy, account for performance of old people on our strong generative component. The stem biases the participant WSC-implicit and frontal tests. However, it is important to to search the for a word beginning with the stem. In this note that participants in both aged groups were carefully regard, stem completion can be considered to be a variation of screened, with normal performance on WAIS Vocabulary an letter fluency, a test which is known to be sensitive to important criterion for selection. As shown in Table 2, there frontal-lobe dysfunction. Thus, word stems in addition to were no differences between any of the groups on this triggering perceptual identification processes, initiate genera- measure. Moreover, a global deficit interpretation cannot tive search processes. Fragment completion does not evoke readily explain why WSC-implicit performance was selectively this strategy because unlike initial stems, letters drawn ran- impaired and WFC-implicit performance was spared. Indeed, domly from the word are poor cues for locating words in the if old people were experiencing a severe and generalized lexicon. Instead, fragment completion is best viewed as a cognitive decline, a double dissociation of the type observed perceptual identification test in which the fragment evokes the here would be unlikely. Although there is no doubt that old perceptual record of the target. people perform worse than young people on many tests of With respect to the idea that WSC in a priming task involves cognitive function, the present study shows that it is possible to a generative search process that implicates the frontal lobes, distinguish between decline in specific functions and relate the question arises as to whether a similar process occurs these impairments to corresponding decline in specific brain during baseline performance. Because baseline WSC perfor- regions. mance did not correlate with FAS performance in any of the To understand the nature of frontal lobe involvement in groups, that would not appear to be the case. In baseline stem completion, it is necessary to compare the pattern of testing, the word stem elicits a single prepotent response. results on the explicit and implicit versions of stem completion. Following priming, response alternatives are probably acti- The low correlation between performance on stem-cued recall vated by the cue with the recently primed response vying with and tests of frontal function was predicted on the evidence that the prepotent baseline response for selection. The latter frontal lobe damage normally does not affect performance on process is less automatic and more likely to involve the frontal explicit tests of memory that are cue-dependent and do not lobes than the former. This account suggests that the frontal involve strategic processes. Frontal-lobe involvement might be lobes may be involved in response-selection, as well as response- expected on the explicit version of stem completion because of generative processes. The observed correlations between WSC its conceptually driven component. The apparent inconsis- and FAS, a generative task, on the one hand, and between tency is compounded by evidence that the frontal lobes are WSC and WCST, a task with a significant selective component, implicated in the implicit test of stem completion, which on the other hand, is consistent with this view. traditionally has been viewed as relying more on automatic, Other investigators have also suggested that automatic and perceptual processes (Blaxton, 1989; Jacoby, Lindsey, & Toth, strategic processes contribute to performance on implicit and 1992; Roediger, 1990). explicit tests of memory. The prevailing view is that no test of To resolve this apparent inconsistency, we propose that memory is process pure: Strategic processes intrude on perfor- automatic and strategic processes can contribute to both mance on implicit tests of memory, and conversely automatic, EXPLICIT AND IMPLICIT MEMORY 63 implicit processes influence performance on explicit tests. frontal and medial temporal lobe function. Performance on Acknowledging this position, we emphasize the importance of experimental tests of memory was consistent with these obser- the additional point we are making. In our view, there is also vations, as well as with the framework we have proposed. The an automatic component to conscious recollection that is institutionalized group was most impaired on the explicit tests independent of the automatic implicit component. A similar that were correlated with standard tests of medial temporal interpretation has been offered by other investigators who lobe function and on implicit stem completion, which was contrast voluntary with involuntary processes in conscious correlated with frontal function. Importantly, there were no recollection (e.g., Richardson-Klavhen, Gardiner, & Java, statistical differences among the groups on implicit fragment 1994). In addition, we maintain that there is a strategic completion that is presumed to be mediated by posterior component involved in generating responses on some implicit neocortical structures that are relatively preserved with age. tests that is independent of the strategic recollective process Although we took great care to match institutionalized and that may be operative on explicit tests. J. D. E. Gabrieli community-dwelling old people on psychological and health- (October, 1994, personal ) made a similar point related measures, it is clear that important differences remain in demonstrating a generative component to some implicit between these groups. For example, our own research, has tests, like stem completion and category-exemplar generation, shown that the institutionalized elderly are more sensitive to which is selectively impaired in Alzheimer's disease. psychosocial factors that can adversely affect performance on The above framework accounts for the age-related deficits tests of medial temporal or frontal lobe function (Winocur & we obtained, as well as for most of the functional dissociations Moscovitch, 1987). It may also be the case that institutional- as revealed by different patterns of correlations among the ized old people who outwardly appear normal for their age various implicit and explicit memory tests. However, there arc may be at greater risk neurologically. Recently, Boone, Miller, some findings that still need to be explained. In the community- and Lesser (1993) studied a group of apparently normal old dwelling group, significant correlations were observed between people and found that 75% of participants over 70 years had performance on delayed recall of the Rey-Osterrieth figure detectable vascular lesions in white matter. A small group of and performance on explicit and implicit versions of fragment these individuals had lesions of sufficient size to be associated completions. In this group, significant correlations were found with frontal cognitive deficits. It is possible that this subgroup also between performance on explicit and implicit versions of is overrepresented in samples of normal institutionalized old stem completion. It is tempting to attribute the source of these people. Further research is needed to determine the full range correlations to perceptual components that the tests have in of factors that differentiate healthy, high-functioning old common. The difficulty is that this interpretation would predict people living in institutions from those living in the community. other correlations that were not found. Specifically, perfor- Our results have implications for issues related to aging and mance on implicit and explicit tests of fragment completion did the organization of memory. A point to emphasize is the not correlate with each other, nor were similar positive significance of the functional double dissociation that we correlations found in the institutionalized group. obtained. To our knowledge, this is one of the first demonstra- The finding that age-related deficits in WSC-priming in old tions in a single study of differential decline with age of people correlated with performance on frontal-lobe tests separable memory functions mediated by different systems appears to conflict with reports of normal WSC performance (see also Glisky, Polster, & Routhieaux, 1995). The finding of a in patients with Huntington's disease (HD) and in nondemen- double dissociation means that declines in performance with tia patients with Parkinson's disease (PD; e.g., Bondi & age cannot be attributed to a uniform effect across all Kaszniak, 1991; Heindel, Salmon, Shults, Walicke, & Butters, functions, nor to a selective effect on those functions that are 1989; Huberman, Moscovitch, & Freedman, 1994). Of course, most vulnerable in old age. Thus, our finding of frontal lobe such patients frequently show signs of frontal-lobe damage. deficits in old people, for example, cannot be attributed to However, none of these studies provided information on the diffuse brain dysfunction, as is sometimes claimed (Goldberg relation between performance on WSC and performance on & Bilder, 1987; Stuss & Gow, 1992). tests that are sensitive to frontal lobe function. This informa- Double dissociation studies have a distinct advantage over tion is crucial, given the great variability in performance on single dissociation studies. By focusing only on a single frontal-lobe tests in these patients and in controls who them- function and ignoring others, the single dissociation approach selves are usually old. It is important to bear in mind that in the can leave the impression that an observed deficit can be present study performance on WSC was correlated with attributed exclusively to the function being studied. In the performance on frontal lobe tests in community-dwelling older present study, the results show thht age differences in word adults, even though their scores on WSC were not significantly stem completion can be attributed to frontal-lobe, but not different from those obtained by young adults. Thus, the medial temporal dysfunction, whereas the reverse is true of absence of a significant deficit in WSC in patients with HD or explicit tests of memory. PD is not inconsistent with our hypothesis. It is expected that in these patients, as in our older adults, performance on WSC References would correlate significantly with performance on frontal tests. The present results confirm previous findings that institution- Albert, M. S., & Stafford, J. L. (1986). CT scan and neuropsychological alization exacerbates the process of cognitive decline associ- relationships in aging and dementia. In G. Goldstein & R. E. Tasker ated with aging. 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Wechsler, D. (1981). WAIS-R Manual." Wechsler Adult Intelligence Winocur, G., & Moscovitch, M. (1990). A comparison of cognitive Scale Revised. New York: Psychological Corporation. function in community dwelling and institutionalized old people of Winocur, G., & Moscovitch, M. (1983). Paired-associate learning in normal intelligence. Canadian Journal of Psychology, 44, 435 444. institutionalized and noninstitutionalized old people: An analysis of interference and context effects. Journal of Gerontology, 30, 455-464. Winocur, G., & Moscovitch, M. (1987). An investigation of cognitive Received January 25, 1995 function in relation to psychosocial variables in institutionalized old Revision received July 21, 1995 people. Canadian Journal of Psychology, 41, 257-269. Accepted July 28, 1995 •