Neuropsychology Copyright 1996 by the American Psychological Association, Inc. 1996, Vol. 10, No. 1, 57-65 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 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. 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. 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 recall 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 implicit memory (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 explicit memory. 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 amnesia 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), living in 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,