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Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19

Semantic organization and verbal episodic memory in patients with mild and moderate Alzheimer's disease a

Agneta Herlitz & Matti Viitanen

b

a

Section of Psychology, Stockholm Gerontology Research Center, Department of Geriatric Medicine , Karolinska Institute University of Umeå , b

Department of Geriatric Medicine , Huddinge University Hospital, Karolinska Institute , Published online: 04 Jan 2008.

To cite this article: Agneta Herlitz & Matti Viitanen (1991) Semantic organization and verbal episodic memory in patients with mild and moderate Alzheimer's disease, Journal of Clinical and Experimental Neuropsychology, 13:4, 559-574, DOI: 10.1080/01688639108401071 To link to this article: http://dx.doi.org/10.1080/01688639108401071

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Journal of Clinical and Experimental Neuropsychology 1991, VOI. 13, NO. 4, pp. 559-574

0168-8634/91/1304-0559$3.00 Q Swets & Zeitlinger

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Semantic Organization and Verbal Episodic Memory in Patients With Mild and Moderate Alzheimer’s Disease* Agneta Herlitz Section of Psychology, Stockholm Gerontology Research Center, Department of Geriatric Medicine. Karolinska Institute, and University of Umel and Matti Viitanen Department of Geriatric Medicine, Huddinge University Hospital, Karolinska Institute

ABSTRACT The objective of the present research was to investigate the relationship between semantic organization and cue utilization in mildly and moderately demented patients with Alzheimer’s disease (AD). In Experiment 1, subjects were presented with two lists of words: a list with semantically unrelated words and a list with words from four semantic categories presented randomly intermixed. Free recall was assessed and following the organizable list, subjects received a cued recall test. Normal controls, as opposed to mildly and moderately demented patients, showed higher performance in the organizable list as compared to the random list. In addition, normal controls and mildly demented patients benefited from semantic cues in the organizable list and performed at a higher level in total recall as compared to free recall. In Experiment 2, subjects were presented with two lists of words: a list with words from four semantic categories presented randomly intermixed and a list with words from four semantic categories presented clustered, together with information about the organization of the list. Free recall and cued recall, with the category names serving as cues, were assessed. Free recall performance of normal controls was higher in the clustered than in the organizable list, whereas no such effect was observed for the AD patients. Normal controls and mildly demented patients performed at a higher level in total as compared to free recall in both lists, whereas this effect

* This work was supported by a predoctoral fellowship from the University of Umel awarded to the fust author. The Kungsholmen project is supported by a grant from the Stockholm Gerontology Research Center. The authors thank Hans Basun for clinical examination of patients, Kaarina Amberla for assistance in the data collection, and the staff of the Kungsholmen project for providing complementary data. The authors would also like to thank two anonymous reviewers for constructive comments on an earlier version of the manuscript. Correspondence concerning this article should be sent to Agneta Herlitz, Stockholm Gerontology Research Center, Dalagatan 9-1 1, S-I13 82 Stockholm, Sweden. Accepted for publication: September 14, 1990.

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was present only in the clustered list for the moderately demented patients. The overall pattern of results indicates that there are conditions under which memory facilitation from semantic organization may be obtained in AD. Memory problems are one of the earliest and most prominent symptoms of Alzheimer’s disease (AD), and have therefore received a large interest in the scientific community. The aim of the present research was to examine whether the described inablity of AD patients to utilize semantic knowledge in episodic memory tasks (Weingmer, Grafman, Boutelle, Kaye, & Martin, 1983) constitutes a complete inability to use semantic knowledge, or whether it is a reduction in efficiency in using semantic knowledge. Episodic memory, defined as the system that encodes and stores information about temporally and spatially dated episodes (Tulving, 1983), has been thoroughly examined in AD patients, and has been found to be severely disrupted (see Bilckman, MZLntylil, & Herlitz, 1990; Kaszniak, Poon, & Riege, 1986; Morris & Kopelman, 1986, for reviews). The disruptionis evident not only in that demented patients perform at a level far below normal older adults in episodic memory tasks, but also in that AD patients are insensitive to various manipulations at encoding and retrieval, which are known to be beneficial to memory performance in normal older adults. Such a pattern of data has been reported in studies examining, for example, the effects on memory of item richness (Rissenberg & Glanzer, 1986; Wilson, Kaszniak, Bacon, Fox, & Kelly, 1982). item organizability (Weingartner et al., 1982; Weingartner et al., 1981), word frequency (Wilson, Bacon, Kramer, Fox, & Kaszniak, 1983), self-generationactivity (Dick, Kean, & Sands, 1989; Mitchell, Hunt, & Schmitt, 1986). a multimodal and rich encoding (Herlitz, Adolfsson, Bilckman, & Nilsson, 1991; Karlsson et al., 1989), and prior knowledge (Bilchan & Herlitz, 1990). Semanticmemory, or the organized body of knowledge involving facts, words, concepts, as well as the rules for manipulatingthese words and concepts (Tulving, 1983). is also affected in AD (see Nebes, 1989, for a review). Not only do AD patients show deficits in language skills, such as object naming (Bayles & Tomoeda, 1983), verbal fluency (Emery & Breslau, 1988; Ober, Dronkers, Koss, Delis, & Friedland, 1986), vocabulary (Hier, Hagenlocker, & Shindler, 1985), and concept attributes (Grober,Buschke, Kawas, & Fuld, 1985; Martin & Fedio, 1983); they are also impaired in the use of semantic information. The deficit in utilization of semantic knowledge as an aid for episodic memory in AD is demonstrated in studies investigating level-of-processing (Corkin, 1982; Wilson et al., 1982), release from proactive interference (Cushman, Como, Booth, & Caine, 1988), SemaDtic organization(Diesfeldt, 1984), and prior p w l e d g e (Bilckman & Herlitz, 1990). In addition, Weingartner and collaboratots have in a series of studies demonstrated that AD patients perform equally well for organized and nonorganized word lists (Weingartner et al., 1982; Weingartner et al., 1981). When comparing memory for lists with either randomly selected words, words from two categories presented randomly intermixed, or words presented clustered into

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561

categories, it was found that whereas normal controls increased performance as the list went from random through unclustered to clustered, the mildly demented patients did not. These findings led Weingartner et al. (1983) to the conclusion that the episodic memory impairment seen in AD is due to a breakdown of semantic memory. This notion posits that a loss of access to semantic knowledge mediates the episodic memory impairment in AD. The studies showing a lack of beneficial effect of semantic activation at encoding (e.g., Backman & Herlitz, 1990; Corkin, 1982; Cushman et al., 1988; Diesfeldt, 1984; Weingartner et al., 1982; Weingartner et al., 1981; Wilson et al., 1982) support the “semantic deficit hypothesis” (Weingartner et al., 1983), and can be interpreted such that AD patients are unable to utilize semantic knowledge to improve episodic remembering. There are, however, studies demonstrating that patients with mild AD can benefit from semantic support when support is provided at both encoding and retrieval, in the form of a semantic orienting task at encoding and category cues at retrieval (Buschke, 1984; Diesfeldt, 1984; Herlitz et al., 1991; Martin, Brouwers, Cox, & Fedio, 1985). The mere provision of semantic category cues at retrieval does not result in increased recall in AD (Davis & Mumford, 1984; Diesfeldt, 1984). Two experiments were conducted in order to investigate potential differences between normal older adults, and patients with either mild or moderate AD in the ability to utilize semantic knowledge for episodic remembering. The episodic memory tasks used in the experiments were designed so as to involve an increasing degree of semantic support. It was hypothesized that if the ability to utilize semantic support as an aid for episodic remembering is impaired in AD, then the moderately demented patients would need more semantic support at encoding and retrieval than the mildly demented patients to improve episodic remembering. Similarly, mildly demented patients were expected to need more semantic support than normal controls to improve memory. Lists of words with increasing semantic organization were presented at encoding. Free and cued recall, with category names serving as cues, were assessed. Three groups participated in the experiments: healthy elderly adults, and patients with mild and moderate AD.

EXPERIMENT 1

In Experiment 1, mildly and moderately demented patients and normal controls were presented with two different word lists: semantically unrelated words and words from four semantic categories presented randomly intermixed. In both lists, memory performance was assessed by means of free recall. In the organizable word list, cued recall was also assessed. Normal controls were expected to benefit from the inherent semantic support and show higher free recall performance in the organizable list than in the random list. On the basis of earlier studies (Weingartner et al., 1982; Weingartner et al., 198l), it was hypothesized that mildly and moderately demented patients would perform at the same level for

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both lists. In agreement with the results from a recent study (Herlitz et al., 1991), the mildly demented patients and the normal controls,in contrast to the moderately demented patients, were expected to show beneficial effects of cues in the organizable word list.

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METHOD Subjects AD patients and normal controls were selected from the Kungsholmen project, which is a population-based, longitudinal study with the aim of defining the Occurrence and possible risk factors of AD and other dementias in a population 75 years and older (Fratiglioni. in press). The final diagnosis of AD was reached on the basis of DSM-III-R diagnostic criteria (American Psychiatric Association, 1987), using information from neuropsychologicalexamination,Mini Mental-State Examination (h4MSE; Folstein, Folstein, & McHugh, 1975). family interview, laboratory screening (i.e., blood status, vitamin B12 and folate levels, electrolytes, renal function, and thyroid function), psychiatric interview, and medical examination. Memory loss and other cognitive deficits were demonstrated on the neuropsychological examination, MMSE, and were reported on the family interview. Based on information obtained from the family interview, the AD patients had an insidious onset and progression of cognitive deficits which interfered with work and social activities. Medical and psychiatric data were collected and used to rule out delirium, depression and other psychiatric disorders (i.e., Comprehensive Psychopathologal Rating Scale; Pems, Eisemann, von h o n i n g . & Pems. 1984). Patients with a Hachinski score exceeding 4 were excluded. As assessed by the MMSE (Folstein et al., 1975). demented subjects were classified as mildly (MMSE = 21-24), and moderately (MMSE = 11-20) demented. Normal controls, who underwent the same examination,were noninstitutionalized, healthy elderly adults (MMSE> 27). Subject characteristics are presented in Table 1. As can be seen in Table 1, years of formal education are low in the groups examined, but reflect the actual educational level for this cohort in Stockholm, Sweden (Statistiska Centralbyrh, 1985). As indicated by one-way ANOVAs, neither differences among groups in mean age, nor differences in years of formal education reached statistical significance, F e 1. The three groups differed in MMSE score, F (2,23) = 118.73.~c .001. Subsequent post hoc tests according to Tukey’s HSD method (Kirk, 1968) indicated that the effect was due to significant differences among all groups, ps < . 01. Material and Procedure Two lists of nouns were prepared. The words in the two lists were five to seven letters long and were equal with respect to word frequency and imagery (Molander, 1984). The

Table 1. Subject Characteristics in Experiment 1 Female/ Age Male

Years of Education

MMSE

~~

n

M

SD

M

SD

M

SD

Normal Controls

10/2 611

78.2 79.1 79.4

(1.4) (2.2) (1.9)

8.7

AD, Mild AD, Moderate

8.4

(2.6) (2.9)

7.3

(0.8)

29.2 21.8 16.0

(0.7) (1.1) (3.0)

Group

5/2

563

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first list consisted of 12 random words (i.e., random list), and the second (i.e.. organizable list) consisted of 12 words from four different categories (e.g.. vegetables, toys), with three subordinates each (e.g., potato, cucumber, spinach) presented randomly intermixed. To avoid guessing. the words chosen were not selected among the most common instances of the categories (Nilsson, 1973). The words were printed in three-centimeter high capital letters, and were presented one by one at a rate of five seconds per word. Subjects were tested individually and were instructed to remember each of the presented words for a later recall test. Following presentation of a list, subjects were immediately asked to free recall all words they could remember. Two minutes were allowed for this task. Following free recall of the organizable list, subjects received a cued recall test with the four category names serving as cues. Two minutes were allowed for the cued recall test as well. Presentation order of the two lists was counterbalanced, and there were other cognitive tests in between presentation of the two lists. The testing lasted approximately 1 hour.

RESULTS AND DISCUSSION

Results were based on a strict scoring criterion. With the exception of the plural and definite forms, only those responses that were identical to the corresponding target word were accepted as correct. Mean free recall performance in the two lists as a function of group is portrayed in Figure 1. As can be seen in this figure,

Controls

MildAD

Makrate AD

Group Fig. 1. Mean free recall performance with standard deviations in the random and organizable lists by normal controls and patients with mild and moderate AD.

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normal controls appear to benefit from the internal organization of the organizable list as compared to the random list. This effect is less pronounced for the two groups of AD patients. These impressions were tested in a 3 (Group) x 2 (List) ANOVA, with repeated measures on the last factor. There were main effects of Group, F (2,24) = 15.23, p < .001, and of List, F (1, 24) = 9.67, p < .01. The Group by List interaction was not significant, p < .32. As this interaction involved one of the main predictions of the present study, tests of simple effects were conducted (Kirk, 1968). These tests showed that the performance of normal controls was significantly higher in the organizable list than in the random list, F (1.24) = 12.95, p < .001, whereas t h i s effect was nonsignificant for both p u p s of AD patients, ps > .lo. Two scoring procedures were used in the cued recall analysis. The first score, which here will be termed cued recall, was based on what the subjects actually recalled when provided with the category cues. The second score, total recall, was based on the number of words recalled in free recall together with new words recalled in cued recall. Thus, the cued recall score is always equal to or less than the total recall score. Data on free and cued recall in the organizable word list as a function of group will be reported first. As can be seen in Figure 2, normal controls show a

I&

G

10

-

H FreeRecall El CuedRecall

I

4

0 2

Controls

MildAD

Group Pig. 2. Mean free and cued recall performance with standard deviations in the organizable list by n o d controls and patients with mild and moderate AD.

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slight increase from free to cued recall, whereas the mildly and moderately demented patients show a slight decrease in performance from free to cued recall. A 3 (Group) x 2 (Test) ANOVA was conducted on the data. There was a main effect of Group, F (2,24) = 24.15, p < .001, but the Group by Test interaction fell short of significance, F (2, 24) = 2.12, p < .14. Tests of simple effects showed that normal controls recalled slightly more words in cued recall as compared to free recall, F (1, 24) = 3.20, p < .06. Neither the mildly nor the moderately demented patients showed beneficial effects of cues, p > .lo. The results from the ANOVA conducted on the free and total recall data showed a different pattern. As can be seen in Figure 3, normal controls and mildly demented patients, in contrast to moderately demented patients, performed at a higher level in total recall than in free recall. A 3 (Group) x 2 (Test) ANOVA showed main effects of Group, F (2,24) = 153.08, p < .001, and of Test, F (1,24) = 40.96, p < .001.Furthermore, the Group x Test interaction was marginally significant, F (2, 24) = 2.67, p < .08.A subsequent Tukey test indicated an increase from free to total recall for normal controls and mildly demented patients, p < .01, whereas no such increase was obtained for the moderately demented patients, p > .lo.

Controls

Mild AD

Moderate AD

Group Fig. 3. Mean free and total recall performance with standard deviations in the organizable list by normal controls and patients with mild and moderate AD.

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Several aspects of the data from Experiment 1 should be highlighted. First, normal older adults were able to benefit from the inherent semantic organization in the organizable list. Second, mildly and moderately demented patients were not able to benefit from the semantic organization provided at encoding, thereby replicating earlier findings (e.g., Weingartner et al., 1982; Weingartner et al., 1981). Third, the mildly demented patients performed at a higher level in total recall as compared to free recall. This effect was, however, not evident in the free-cued recall contrast. Fourth, moderately demented patients did not show beneficial effects of cues either in cued recall OT in total recall. As discussed before, there are two potential reasons for this latter result: (a) AD patients suffer from a mediational deficit with respect to utilization of semantic organization. This would imply that there is a major breakdown of semantic memory, which becomes evident later in the disease; or (b) the semantic support provided at encoding (e.g., inherent semantic organization) and retrieval (e.g., category cues) was not sufficient as an aid for the moderately demented patients. Such a notion implies that differences between AD patients and normal controls in semantic organization and memory are quantitative rather than qualitative.

EXPERIMENT 2 The purpose of Experiment 2 was to explore whether a stronger semantic support provided at encoding would result in higher recall and cue utilization particularly for moderately demented patients. Normal controls and patients with a mild and moderate AD were presented with two word lists: (a) words from four categories presented randomly intermixed, and (b) words from four categories presented clustered, together with information about the semantic categories in the list. Recall was assessed by means of free and cued recall. METHOD

Subjects The groups of AD patients were recruited from the Department of Geriatric Medicine, Huddinge University Hospital and the Department of Psychiatry, S:t Gbans Hospital, Stockholm. The diagnosis of Alzheimer's disease was based on DSM-III-R research criteria (American Psychiatric Association, 1987) and included history taking from relatives, complete medical records, medical, neuropsychological,psychiatric, and neurological examinations, laboratory tests (i.e., blood status, vitamin B12 and folate levels, electrolytes, renal function, syphilis serology, and thyroid function), EEG- and ECG investigations, and CT scan or MRI of the skull. Memory loss and other cognitive deficits were demonstrated on the neuropsychological examination, MMSE, and were reported on the family interview. The AD patients had an insidious onset and progression of cognitive deficits which interfered with work and social activities. Subjects with a Hashinski score exceeding 4 were excluded. All patients were followed clinically for at least one year with repeated examinations. Hereby, the progressive course of the disease could be documented. According to the MMSE, demented subjects were classified as mildly (MMSE = 21-25), or moderately (MMSE = 11-20)demented. The control group was recruited from local

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Table 2. Subject Characteristics in Experiment 2

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Female/ Age Male

Years of Education

MMSE

Group

n

M

SD

M

SD

M

SD

NormalControls AD, Mild AD, Moderate

6/4 413 512

75.3 70.0 76.4

(4.5)

(8.3) (4.0)

9.5 10.1 8.9

(3.3) (2.5) (3.8)

29.0 24.5 12.3

(1.1) (1.6) (3.7)

senior citizens' associations. All controls were noninstitutionalized community members and reported being in good health (MMSE > 27). Subject characteristics are presented in Table 2. Neither differences among groups in mean age, nor differences in years of formal education reached statistical significance, ps > .05, as indicated by one-way ANOVAs. The three groups differed in MMSE score, F (2, 21)= 110.53,p < .001. Tukey tests revealed that the effect was due to significant differences among all groups, ps < .01.

Materials and Procedure Subjects were presented with two lists of words. The words were five to seven letters long and were equal with respect to word frequency and imagery (Molander, 1984). Each list consisted of 12 words from four different categories, with three category subordinates each. To avoid guessing, the words chosen were not selected among the most common instances of the categories (Nilsson, 1973). Words in one list (i.e.. organizable) were presented randomly intermixed, whereas words in the other list (i.e., clustered) were presented clustered into categories. The testing procedure and presentation format were identical to those in the organizable list in Experiment 1, with one exception: information that the words belonged to four different categories and the names of the four categories were provided prior to presentation of the clustered list. Following presentation and immediate free recall of each list, subjects were provided with the category names as cues. Two minutes were allowed for the free and cued recall tests, respectively. Words selected for the two lists were alternated between the lists, so that one list of words was presented as the organizable list for half of the subjects, and the same words were presented clustered for the other half of subjects, and vice versa. Presentation order of the two lists was counterbalanced, and there were other cognitive tests in between presentation and recall of the two lists. The testing lasted approximately one hour.

RESULTS AND DISCUSSION As in Experiment 1, results were based on a strict scoring procedure. In addition to free recall, cued recall and total recall scores were computed. Data on free and cued recall across list and group will be reported first. As can be seen in Figure 4, normal controls performed at the ceiling in the clustered list, but appear to benefit from the provision of category cues in the organizable list. I n addition, normal controls showed higher overall recall in the clustered list as compared to the organizable list. Neither mildly nor moderately demented patients showed beneficial effects of either a clustered presentation o r cues.

AGNETA HERLiTZ AND IUA'TTI VIITA"

12

anizable, Cued Recall

10

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8

6 4 2

0 Controls

MildAD

ModerateAD

Group Fig. 4. Mean frte and cued ncall performance with standard deviations in the organizable and clustered lists by normal controls and patients with mild and moderate AD.

A 3 (Group) x 2 (List) x 2 (Test) mixed ANOVA, with repeated measures on the last two factors, showed main effects of Group, F (2,21) = 126.15, p < .001, and of List, F (1,21) = 19.58, p < .001. The Group x List interaction was significant, F (2, 21) = 7.83,p < .01. Neither the Group x Test nor the Group x List x Test interactionreached significance, ps > .05. Tukey tests revealed that the Group x List interaction was due to the fact that normal controls showed a significant performance increase in the clustered list as compared to the organizable list, p < .01. For the groups of mildly and moderately demented patients this difference was not reliable, ps > .lo. The results on free and total recall as a function of list and group can be seen in Figure 5. The total recall data show a different pattern than the cued recall data for the mildly demented patients. Normal controls performed at ceiling in the clustered list, but benefited from the provision of category cues in the organizable list. Mildly demented patients showed higher performance in total recall as compared to free recall, although this effect appears to be more-pronounced in the clustered list. Moderately demented patients showed a slight increase from free to total recall only in the clustered list. In addition, noxmal controls performed better with the clustered than with the organizable list, and this effect is also apparent in the free recall data.

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12 I I

I

I

1 4 -

Organizable,Total Recall Clustered, Free Recall Clustered, Total Recall

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10

4 2 0

~

Controls

MildAD

ModerateAD

Group Iean free and total recall performance with standard deviations in the organizab e and clustered lists by normal controls and patients with mild and moderate AD.

A 3 (Group) x 2 (List) x 2 (Test) mixed ANOVA showed main effects of Group, F (2, 21) = 164.29, p < .001, of List, F (1, 21) = 18.65, p < .001, and of Test, F (1,21) = 42.54, p < .001. The Group x List interaction was significant, F (2, 21) = 6.69, p c .01, as was the interaction among Group, List, and Test, F (2, 21) = 5.74, p < .01. Tukey tests showed that normal controls and mildly demented patients performed at a higher level in total recall as compared to free recall in the organizable list, ps < .01. Moderately demented patients did not show such an improvement, p > .lo. The mildly as well as the moderately demented patients, however, performed significantly better in total recall as compared to free recall in the clustered list, p < .01 and p < .05, respectively. Due to ceiling effects, the results of normal controls in the clustered list are blurred and cannot be properly evaluated. Finally, the normal controls showed a higher free recall performance in the clustered list than in the organizable list, p < .01. The overall performance of the patients with moderate AD was relatively low. As a consequence, the beneficial effects of the category cues may reflect guessing, rather than episodic remembering. However, in order to prevent guessing, we chose category subordinates which were not among the most common instances of the categories (Nilsson, 1973). In addition, at the time of testing, the

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Table 3. Mean Number of Intrusion Errors in Experiment 1 and Experiment 2 (Standard

Deviations are Within Parentheses) Organizable Exp. 1

Group

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Normal Controls

AD,Mild AD,Moderate

M SO 1.85 2.00

SD (52) (2.85)

(2.64)

Organizable Bxp. 2

Clustered Exp. 2

M

SD

M

SO 2.28 1.00

(.71) (1.25) (1.29)

.10 1.57 1.28

SD (.32) (1.39) (1.49)

subjects were not encouraged to guess. To provide a measure of guessing, we calculated intrusion rates for the response protocols in both experiments. These intrusion data are portrayed in Table 3. The mean n u m b of intrusions should be seen in relation to the cued recall score. It then becomes evident that the mean number of intrusions was relatively low for the normal older adults, and somewhat higher for the mildly and moderately demented patients. For both the mildly and the moderately demented patients the ratio between intrusions and the cued recall score is higher in the organizable word lists than in the clustered word list, which may indicate an improved memory accuracy in the clustered list. The strongest argument for rejecting the hypothesis that beneficial effects of category cues mainly are due to guessing comes from a control task used in the Herlitz et al. (1991) study. Patients with mild and moderate AD were here asked to generate subordinates to the category names which served as cues in the experimental conditions of that experiment. It was found that the total number of words generated was low, as was the "hit rate" (category subordinates which were present in the experimental lists). The hit rate was much lower than the number of category subordinates remembered in the experimental cued recall condition. As the experimental conditions in the present experiment were similar to those of Herlitz et al. (1991), it is conceivable that the effects of category cues for the AD patients in the present experiments were not due to guessing. The present results extend the results of Weingartner et al. (1981) by demonstrating that not even a strong support at encoding (i.e.. category information at encoding and a clustered presentation of words) boosts AD patients' memory performance, as measured by free recall. In addition, the data show that moderately demented patients can improve performance in total as compared to free recall when strong support is provided at encoding. GENERAL DISCUSSION Normal controls benefited from semantic support provided at encoding and improved free recall performance as the list went from random to organizable, and from organizable to clustered. This was not true for the mildly or for the moder-

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ately demented patients. These results replicate earlier research (Weingartner et al., 1982; Weingartner et al., 1981), and extend those by demonstrating that increasing semantic support at encoding (i.e., clustered presentation together with information about the semantic organization of the list) does not enhance AD patients’ free recall performance as compared to weak semantic support at encoding (i.e., the random list). Thus, these results support the notion that AD patients show a deficit in utilizing semantic knowledge as an aid for episodic remembering. Before discussing the cued recall data, a methodological issue will be addressed. There were two main reasons for the inclusion of two scoring procedures for the cued recall data (i.e., cued and total recall). First, studies on cued recall in AD have often employed different testing procedures (Buschke, 1984; Martin et. al., 1985)’ and the scoring procedures have not always been documented (Cushman et al., 1988; Diesfeldt, 1984). The differences in cuing- and scoring procedures among studies motivate the inclusion of both cued and total recall in this research. A second reason for including both the cued and the total recall score is that clinical observation suggests that the pattern of data may differ for AD patients depending on scoring procedure. Data on the cued recall score demonstrated that normal controls were able to utilize cues in the organizable lists. Potential beneficial effects of cues in the clustered list could not be properly evaluated due to ceiling effects in free recall. However, past research (e.g., Backman & Karlsson, 1986; Hultsch, 1975) has strongly suggested that normal older adults show beneficial effects of category cues when items are organizable. Neither mildly nor moderately demented patients showed effects of cues following the organizable or the clustered list. This result is in contrast with the notion held by Buschke (1984) that items retrieved in free recall also should be retrieved in cued recall. The results from the present study demonstrate that AD patients forget items from free to cued recall, as evidenced by the difference between cued recall and total recall. In spite of this, the provision of category cues at test activates the memory traces of some items not previously retrieved in free recall. Providing category cues, however, do not guarantee activation of memory traces for items already retrieved in free recall. The information appear to be weakly encoded and, accordingly, the cues are not sufficient to trigger the encoded information. The results of the present experiments indicate that category cues are not sufficient to evoke all of the items AD patients have encoded. This finding is supportive of the notion that AD patients have difficulties in utilizing semantic knowledge as an aid for episodic memory. The total recall data showed a different pattern. The total recall score provides an estimate of the items actually encoded, or as Buschke (1984, p. 434) notes in arguing for the use of total recall: “The total recall resulting from the addition of cued recall to free recall provides a minimal estimate of the number of recallable items available in storage...”. As measured by total recall, it was demonstrated that the mildly demented patients improved their level of recall in the organizable and in the clustered lists. Moderately demented patients improved their

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recall only in the clustered list. The results for the normal older adults were comparable with those obtained in the free-cued recall contrast. As the total recall score is a measure of the combined effect of support during encoding and retrieval, the present data suggest that when increasing semantic support is provided, in the form of an organizable list at encoding and category cues at retrieval, patients with a mild AD can improve memory performance and utilize semantic knowledge. Patients with a moderate AD need the additional support of the clustered presentation at encoding and category cues at retrieval to be able to utilize semantic knowledge for memory. The tasks used in the present experiment can be viewed as instances on a continuum, with the random, the organizable, and the clustered list reflecting increasing semantic support at encoding. Similarly, the free and cued recall tasks differ with respect to level of retrieval support provided, and the total recall score gives an estimate of the s u m of the supportive conditions at encoding and retrieval. The results of the present experiments demonstrate that the ability to utilize semantic knowledge in episodic memory tasks is impaired in AD and, in addition, that patients with a moderate AD are more severely affected than patients with a mild AD in this respect. The data pattern, also, indicates that, although AD patients show a reduction in efficiency in using semantic knowledge for episodic remembering, there are conditions under which memory facilitation from semantic organization may be obtained in AD. These patients need more semantic support than normal older adults to improve memory, and the level of support needed seems to increase as a function of increasing severity of dementia.

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Semantic organization and verbal episodic memory in patients with mild and moderate Alzheimer's disease.

The objective of the present research was to investigate the relationship between semantic organization and cue utilization in mildly and moderately d...
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