Journal of Clinical and Experimental Neuropsychology

ISSN: 0168-8634 (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/ncen19

Are all subcortical dementias Alike?: Verbal learning and memory in Parkinson's and huntington's disease patients Paul J. Massman , Dean C. Delis , Nelson Butters , Bonnie E. Levin & David P. Salmon To cite this article: Paul J. Massman , Dean C. Delis , Nelson Butters , Bonnie E. Levin & David P. Salmon (1990) Are all subcortical dementias Alike?: Verbal learning and memory in Parkinson's and huntington's disease patients, Journal of Clinical and Experimental Neuropsychology, 12:5, 729-744, DOI: 10.1080/01688639008401015 To link to this article: http://dx.doi.org/10.1080/01688639008401015

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Journal of Clinical and Experimental Neuropsychology 1990, Vol. 12, NO. 5, pp. 729-744

0168-8634/90/1205-0729$3.a0 0 Swets & aillinger

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Are All Subcortical Dementias Alike?: Verbal Learning and Memory in Parkinson’s and Huntington’s Disease Patients* Paul J. Massman, Dean C. Delis, and Nelson Butters San Diego Veterans Administration Medical Center, School of Medicine, University of California, San Diego Bonnie E. Levin School of Medicine, University of Miami David P. Salmon School of Medicine, University of California, San Diego

ABSTRACT The utility of the concept of ‘subcortical dementia’ was investigated by comparing the verbal learning and memory abilities of Parkinson’s disease (PD) patients with those of Huntington’s disease (HD) patients. Many similarities between the PD and HD groups emerged, including impaired immediate memory spans, inconsistency of recall across learning trials, deficient use of a semantic clustering learning strategy, elevated intrusion rates on delayed recall, impaired recognition memory performance, normal retention of information over delay periods, normal vulnerability to proactive or retroactive interference, and normal types of intrusion errors. The HD subjects, however, displayed inferior free recall, deficient improvement across learning trials, abnormal serial position recall effects, higher perseveration rates, and supranormal improvement on recognition testing compared with free recall. Implications of these results for characterizing memory deficits associated with subcortical system dysfunction are discussed.

T h e concept of ‘subcortical dementia’ has engendered considerable interest and debate since its formulation 15 years ago. A variety of conditions h a v e been labeled as subcortical dementias, including progressive supranuclear palsy (PSP; Albert, Feldman, & Willis, 1974), Huntington’s disease (HD; McHugh & Fol-

* This study was supported by funds from the Medical Research Service of the Veterans Administration and by NIA grant AG-05131 to the University of California at San Diego. Address correspondence to: Paul J. Massman. Ph.D., Psychology Service (1 16B), VA Medical Center, 3350 La Jolla Village Drive, San Diego, CA 92161, USA. Accepted for publication: January 18, 1990.

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stein, 1975), Parkinson’s disease (PD; Albert, 1978), Wilson’s disease (Cummings & Benson, 1983). idiopathic basal ganglia calcification (Cummings, Gosenfeld, Houlihan, & McCaffrey, 1983), and multiple sclerosis (MS; Rao, 1986). In addition, Caine (1981) proposed that the reversible dementia secondary to depression is similar to a subcortical dementia. The subcortical dementias are characterized as involving predominantly the basal ganglia, white matter, and/or brainstem structures and as causing disturbances in arousal, attention, retrieval, motivation, mood, and motor programming (Cummings & Benson, 1984). These fundamental deficits result in psychomotor slowing, memory impairment, difficulty in actively manipulating novel information, lack of efficiency in accessing old knowledge, and emotional changes (e.g., depression, apathy). This pattern of impairment is said to be different from that of patients with cortical dementias, of which Alzheimer’s disease (AD) is the hallmark. In addition to marked memory deficits, AD patients usually display anomia, agnosia, apraxia, and severe visuoconstructive deficits, especially as the disease progresses (Cummings & Benson, 1984). The validity of the subcortical-cortical dementia distinction is still a matter of controversy. Criticism of this dichotomy has been made primarily on neuroanatomical grounds (e.g., Whitehouse, 1986). Some patients with PD, for example, have been found to have cortical neuropathological changes similar to those found in AD patients (Boller, Mizutami, Roessmann, & Gambetti, 1980). In addition, pathological changes in subcortical structures, most notably the cholinergic nucleus basalis of Meynert, have been discovered in AD patients (Coyle, Price, & DeLong, 1983). Thus, it has been well documented that subcortical and cortical dementias do not involve exclusively subcortical or cortical pathophysiology, especially considering the complex interconnections between subcortical and cortical structures, Metabolic studies, though, have shown that subcortical dementias involve greater subcortical than cortical hypometabolism (Weinberger, Berman, Iadarola, Driesen, & Zec, 1988), whereas cortical dementia (AD) is characterized by the opposite pattern (Benson et al., 1983). These findings of relative differences in subcortical and cortical neurophysiology suggest that the subcortical-cortical dementia distinction could serve as a heuristically useful model for describing the neuropsychological performances of these patient groups. A number of studies, in fact, have found clear distinctions in explicit memory performances between AD and HD patients (Butters, Granholm, Salmon, Grant, & Wolfe, 1987; Butters et al., 1988). AD and PD patients (Helkala, Laulumaa. Soininen, & Riekkinen, 1988), AD and chronicprogressive MS patients (Filley, Heaton, Nelson, Burks, & Franklin, 1989), and AD and PSP patients (Pillon, Dubois, Lhermitte, & Agid, 1986). Overall, AD patients typically displayed severely impaired immediate free recall, rapid forgetting of information over time, and recognition memory impairment as severe as their free recall deficits. Subcortical dementia patients often exhibited immediate free recall deficits as severe as those seen in AD, but showed superior retention over time and marked improvement on recognition testing compared

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with free recall. Additionally, AD patients give higher rates of intrusion errors, particularly on delayed-recall trials (Kramer et al., 1988). While these findings support the validity of the subcortical-cortical dementia model, few direct comparisons between different subcortical dementias have been made. Consequently, it is unclear if the aggregation of subcortical dementias is warranted or if this label masks significant heterogeneity in memory abilities, Such heterogeneity does appear to exist in implicit memory abilities. Heindel, Salmon, Shults, Walicke, and Butters (1989) found that demented PD and HD patient groups both displayed impaired motor skill learning (unlike AD patients, who showed intact motor learning), but that the demented .PD group also exhibited impaired lexical priming (like AD patients) while the HD group did not. It would not be surprising to find some differences in the memory abilities of PD and HD patients, given the different patterns of subcortical neuropathology and neurotransmitter deficits caused by the two diseases. PD primarily involves dopaminergic loss in the nigrostriatal pathway (with dopamine (DA) depletion especially severe in the putamen), as well as milder dysfunciion in the mesolimbic and mesocortical DA pathways (German, Manaye, Smith, Woodward, & Saper, 1989; Kish, Shannak, & Hornykiewicz, 1988). The focus of neuropathology in HD is concentrated in the caudate and putamen, where there are severe losses of GABA neurons, and normal or increased levels of DA (see Martin & Gusella, 1986). Three studies (Caine, Ebert, & Weingartner, 1977; Fisher, Kennedy, Caine, & Shoulson, 1983; and Gainotti, Caltagirone, Masullo, & Miceli, 1980) have compared the explicit verbal memory abilities of PD and HD patients. On the various list-learning tasks utilized in these studies, PD subjects usually recalled significantly more words across trials than the HD subjects and tended to perform better on recognition tasks. However, any conclusions drawn from these three studies must remain tentative, because a number of methodological limitations were present. The most serious problem was that the HD and PD groups were not equated on current verbal intellectual functioning; thus, the quantitative differences found between groups could have been due to the influence of this variable. In addition, two of the studies (Fisher et al., 1983; Gainotti et al., 1980) failed to control for the variables of age and sex, both of which are strongly related to verbal memory test performances (Craik, 1984; Kramer, Delis, & Daniel, 1988). The sample sizes used in all of the studies were small, typically 10 subjects per group or less. Finally, mechanisms of learning and memory performance (e.g., learning strategies, types of errors made, serial position effects) were not examined. The present study attempts to provide a more accurate characterization of explicit verbal learning and memory in HD and PD patients while overcoming the methodological limitations of past studies. Larger patient and control samples (approximately twice the size of those in previous studies) were used in order to enhance power in detecting group differences. Groups were matched on level of

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current verbal intellectual functioning as well as on years of education (and therefore roughly on level of premorbid intellectual functioning). A standardized test of verbal learning and memory that assesses both levels and mechanisms of performance was used (the California Verbal Learning Test, CVLT; Delis, Kramer, Kaplan, & Ober,1987). In addition, extensive normative data on the various CVLT indices made it possible to convert raw scores to standard scores within different age groups and by sex, controlling for the influence of these two important variables.

METHOD Subjects A total of 57 subjects were tested in this study: 19 patients with HD (12 males, 7 females), 19 patients with PD (10 males, 9 females), and 19 normal controls (13 males, 6 females). The HD patients were diagnosed by a staff neurologist on the basis of a positive family history of HD, the presence of involuntary choreiform movements, and the presence of dementia. They had been experiencing motor symptoms for a mean of approximately 3.9 years. The diagnosis of idiopathic PD was made by a staff neurologist. Patients with parkinsonism secondary to known neurologic disease (e.g.. cerebral vascular disease) were excluded from the study. An effort was made to select PD patients whose WAIS-R agescaled Vocabulary scores were similar to those of the HD subjects. Since scores on this subtest are highly associated with verbal intellectual ability, matching subjects on these scores minimizes the possibility that group differences in verbal leaming and memory performances are attributable to differences in overall verbal functioning. The PD subjects had been diagnosed with the illness a mean of 6.3. years prior to their participation in the study, and all had been taking anti-parkinsonian medications for prolonged periods of time. According to Hoehn and Yahr’s (1967) motor impairment seventy stages, ranging from 1 (mild) to 4 (severe), there were 5 PD patients in stage 1 , 4 in stage 2, 5 in stage 3, and 5 in stage 4. The normal control subjects were recruited from the community and exclusion criteria included a history of alcoholism, psychiatric illness, serious cardiovascular disease, cerebral vascular disease, head trauma, or other significant neurologic conditions. Normal subjects were selected for inclusion in the study if their age and education levels were comparable to those of the HD and PD patients. Table 1 shows the mean ages, years of education, and WAIS-R age-scaled Vocabulary scores of the three subject groups. Neither patient group differed significantly in age from the normal control group (p > .10 for both t tests), but the PD patients were significantly older than the HD patients, t (36) = 2.73, p = -01,This difference is expected, since the peak age of onset for PD is in the 50’s and that for HD is in the 30’s (Adams & Victor, 1981). This age difference and the varying distributions of males and females in the groups make it important to utilize normative data that are stratified by age and sex. As noted earlier, such normative data are available for the CVLT indices used in this study, thereby affording a control of the age and sex differences between groups. There were no significant differences in years of education between the normal, PD, and HD groups (p > .20 for all t tests). The normal controls had significantly higher Vocabulary scores than the PD and HD groups (p < , 0 0 1 for both r tests), but the patient groups did not differ, r (36) = 1 . 5 8 , = ~ .12.

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Table 1. Means and Standard Deviations of Group Characteristics Age (Years)

Years of Education

Age-Scaled Vocabulary Score

19

53.2 (13.5)

13.3 (1.7)

11.6 (2.5)

Parkinson’s disease patients

19

57.5 (13.3)

12.6 (1.9)

8.9 (1.2)

Huntington’s disease patients

19

45.7 (13.2)

13.4 (1.8)

(1.6)

Group

n

Normal controls

8.2

Procedure The CVLT was administered by experienced masters-level or doctoral-level psychologists as part of a larger set of neuropsychological tests. The test involves oral presentation of a“shopping” list of 16 items (List A) over five immediate-recall trials. The items on the list are presented in the same order on all five trials and examinees are asked to recall the items in whatever order they please and to recall all the items they can, including those they reported on previous trials. The list consists of four items from each of four categories (fruits, spices, clothing, and tools), but examinees are not informed of this. Adjacent words on the list are from different categories, which affords an assessment of the degree to which an examinee uses the active, effective learning strategy of recalling the words in semantic clusters. Also, the items are not exemplars of their categories (e.g.. ‘tangerines’ is in the fruit category but ‘apples’ is not), so if examinees start guessing prototypical category members, these responses are correctly labeled as intrusion errors. Following the five learning trials, a second, interference list (List B) is presented for one trial. List B is also composed of four items each from four categories; two categories are the same as those in List A (fruits, spices) and two are new (fish, utensils). Following recall of List B, free and category-cued recall of List A is tested (termed the “short delay” trials). After a 20-min interval in which nonverbal testing occurs (the “long delay”), free recall, category-cued recall, and recognition of List A are assessed. The yes/no recognition test contains the 16 List A target items and 28 distractors (8 List B items, 8 items phonemically similar to the target items, 8 items unrelated to the targets, and 4 prototypical members of the List A categories). Descriptions of the CVLT indices used in the present study can be found in Table 2. The paper-and-pencil protocols were scored using the CVLT scoring software (Fridlund & Delis, 1987). This software produces a printout containing the subject’s responses, raw scores, and standard scores on 25 verbal learning and memory variables (those listed in Table 2).

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Table 2. Descriptions of the CVLT Indices Included in the Analyses Variable

Description

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Trials 1-5 List A Trial 1 recall List A Trial 5 recall List A total recall Percent primacy recall

Number of List A words recalled on Trial 1 Number of List A words recalled on Trial 5 Total number of List A words recalled across Trials 1-5 Percentage of total words recalled that are from the primacy region of List A ( f i t four words) Percent middle recall Percentage of total words recalled that are from the middle region of List A (middle eight words) Percent recency recall Percentage of total words recalled that are from the recency region of List A (last four words) Slope of a least-squares regression line calculated to fit Learning slope changes in correct response scores across Trials 1-5 Percentage of List A words recalled on one of the first Consistency of item recall four trials that are also recalled on the very next trial Ratio of List A words from the same category recalled Semantic clustering together over chance-expected semantic clustering Ratio of List A words recalled in the same order as they Serial clustering were presented over chance-expected serial clustering Number of List B words recalled on the one immediate List B recall recall trial List B vs. List A Trial 1 recall Change in recall of List B relative to Trial 1 of List A; reflects vulnerability to proactive interference Number of List A words recalled immediately after the Short delay free recall List B trial without re-presentation of List A Change in recall on short delay free recall relative to Short delay vs. Trial 5 recall Trial 5 of List A; reflects vulnerability to retroactive interference and the short delay Number of List A words recalled when category names Short delay cued recall are provided Long delay free recall Number of List A words recalled after a 20-min delay following the short delay cued recall trial Long delay vs short delay recall Change in recall on long delay free recall relative to short delay free recall; reflects vulnerability to the effects of long delay Long delay cued recall Number of List A words recalled when category names are provided Free recall intrusions Total number of nontarget items reported on all free recall trials of Lists A and B Cued recall intrusions Total number of nontarget items reported on the two cued recall trials of List A Total number of responses repeated on each trial Perseverations summed across all free and cued recall trials of Lists A and B Signal detection index of overall accuracy on recogniDiscriminability tion test incorporating number of misses and false positive errors Continued

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Table 2 (Continued) Variable Discriminability vs. long delay free recall

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False positives Response bias

Description Change in recognition discriminability relative to long delay free recall; reflects impact of recognition testing format Number of distractor items identified as List A items on the recognition test Difference in number of false positives and misses corrected for total number of errors made; reflects possible bias in response criterion on recognition testing

RESULTS The means and standard deviations of the three subject groups on the CVLT measures are presented in Table 3. The numbers in the table’are standard deviation scores (e.g., a mean score of -1.74 indicates that the subjects in the group scored an average of 1.74 standard deviations below persons of their age group and sex in the CVLT normative sample). The eta-squared values in the far right column represent the proportion of variance accounted for by group membership. One-way analysis of variance (ANOVA) was performed on each variable and Tukey post-hoc tests of group differences were carried out if the ANOVA result was significant. Because of the large number of analyses performed, it was decided to adopt a more conservative significance criterion (and therefore lessen the probability of Type 1 error), so an ANOVA F-ratio was considered significant only at the p < .01 level (see also Ober, Koss, Friedland, & Delis, 1985). Some additional analyses of variables not listed in the table were performed, and there was substantial heterogeneity of variance between groups on a number of these measures. When this occurred, nonparametric Mann-Whitney U tests were performed and the significance level was again set at p < .01. The additional analyses involved the use of raw scores rather than standard scores, so the effects of age and sex were no longer controlled for; however, most of these analyses entailed the calculation of ratio indices that adjusted for level of recall, which is most affected by aging.

Immediate and Delayed Recall Large group differences were found on all of the immediate and delayed recall measures (see Table 3). The normal control group obtained significantly higher standard scores than the PD and HD groups on all of these free- and cued-recall indices. The immediate-recall spans of the PD and HD groups (as measured by their performances on Trial 1 of List A and on the one trial of List B) did not differ significantly. However, on Trial 5 of List A, the PD patients achieved

736 Table 3.

PAUL J. MASSMAN ET AL.

Group Means and Standard Deviations of the CVLT Standard Scores Normals

SD

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M List A Trial 1** List A Trial 5** List A Total** List B** Short delay free** Short delay cued** Long delay free** Long delay cued** Percent primacy* Percent middle** Percent recency* Learning slope* Consistency* Semantic clustering** Serial clustering Free recall intrusions Cued intrusions** Perseverations* Discriminability** False positives** Response bias List B vs. Trial 1 Short delay vs. Trial 5 Long vs. short delay

.05'vb .71 .16**b 1.01 .02*Sb 1.01 .ll*'b .99 .16'*b 1.01 1.29 .I1 .OO'*b 1.05 .16'sb 1.17 .ll .94 .ll 1.15 -.05b .91 .05b .91 -.16'.b .83 .ll .94 -.21 1.03 .I6 1.46 -.37'sb .76 -.21 .86 -.32**b .82 -.11 .57 -.16 .83 .05 .91 .OO .88 -.16 .69 'sb

*Bb

Parkinson's Patients

Huntington's Patients

M

SD

M

-1.74 -2.27 -2.30 -1.74 -2.21 -1.79 -2.32 -2.16 -.68 -.37 .68 -.63 -2.05 -.84 .05 -74 1.63 -.84 -1.74 1.74 .47

1.10 1.15 1.17 1.24 1.13 1.32 1.25 .96 1.29 1.26 1.49 1.16 1.93 1.12 1.13 1.94 1.92 .60 1.70 1.73 1S O 1.11 .91 .66

-2.1 1 -3.63 -3.39 -1.74 -3.21 -3.16 -3.1 1 -3.32 -1.63 -1.84 2.89 -1.26 -2.16 -1.37 .05 .53 1.16 .42 -2.1 1 2.16 .89 .37 .42 .11

.oo

.05 -.ll

SD 1.10 1.54 1.23 1.20 1.27 1S O 1.41 1.49 1.74 1.so 1.63 1.10 1S O .96 1.39 1.35 1.71 1.68 1.49 1.80 1.63 1.16 .84 -81

EtaSquared .49 .62 .62 .38 .62 SO

.54 .59 .22 .30 .47 .21 .29 .28 .01 .02 .24 .18 .25 .32 .10 .02 .05

.03

*ANOVA F-ratio significant at p < .01. **ANOVA F-ratio significant at p < .001. a Group mean significantly different from the PD group mean (Tukey test). Group mean significantly different from the HD group mean (Tukey test).

higher standard scores than the HD patients, and their total recall p-rformance across the five List A learning trials was superior to that of the HD group. In addition, the PD patients performed better than the HD patients on the delayedrecall trials. There was not a significant group effect for the difference between the long-delay free recall and short-delay free recall standard scores, suggesting that the PD and HD patients' retention of the information they had learned was equivalent to that of the control subjects. (One HD patient scored at the floor on both the short- and long-delay free-recall trials and was omitted from the above retention analysis).

Learning Characteristics A number of group differences in List A learning characteristics emerged from

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the analyses (see Table 3). Dramatic group differences occurred in the serial position effects in the groups’ immediate free-recall performances. The HD patients achieved significantly lower standard scores than the control group on the percent primacy recall and percent middle recall variables (they also differed from the PD patients on the latter variable). Furthermore, the HD patients obtained much higher scores than both the normal and PD subjects on the percent recency recall variable (i.e., an abnormally high proportion of the items they recalled were from the recemy region of the list). There was little overlap between the HD group and the other two groups on the percent recency variable; 16 of the 19 HD patients obtained a standard score of 2 or above on this measure, while only 6 of 19 PD patients and 2 of 19 controls had a score in this range. The HD group’s mean learning slope standard score was inferior to the control group’s, but the PD group did not differ from the controls. The PD and HD groups displayed equivalent levels of impairment in consistency of item recall across trials, obtaining standard scores significantly lower than the control group on this measure. Semantic clustering scores were significantly poorer in the patient groups than in the normal group, but the PD and HD groups did not differ. There were no group differences in serial clustering standard scores, one of the few CVLT variables that did not show such differences.

Proactive Interference The detrimental effect of prior learning on the learning iind retention of subsequently presented material is referred to as proactive interference (PI; Postman & Underwood, 1973). PI may manifest itself in a number of ways on the CVLT. Immediate recall of List B may be worse than immediate recall on the first trial of List A due to interference from the learning of List A over the five immediaterecall trials. There was not a significant group effect for the difference between the List B and List A Trial 1 standard scores (see Table 3), suggesting that the patient groups were not displaying an increase or decrease in vulnerability to PI. Another indication of PI would be the intrusion of List A items during List B recall. Mann-Whitney tests revealed no group differences in either the number of such intrusion errors (p > .10 for all comparisons) or in the percentage of List B recall responses that were List A items (p > .10 for all comparisons). These errors were uncommon in the three groups; the medians in the normal, PD, and HD groups were all zero. There were also no significant group effects when level of List A recall was adjusted for by calculating the percentage of these intrusion errors relative to the number of items recalled on Trial 5 of List A (p > .lo for all comparisons). Overall, then, the PD and HD groups appeared to exhibit normal PI effects. Retroactive Interference The detrimental effect of subsequent learning on the retention of previously learned material is referred to as retroactive interference (RI; Postman & Underwood, 1973). A decrement in short-delay free recall relative to recall on Trial 5

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PAUL J. MASSMAN ET AL.

of List A may be attributed to a combination of the short-delay period and to RI caused by the presentation and recall of List B. There was not a significant group effect for the difference between the short-delay free recall and List A Trial 5 standard scores (see Table 3), suggesting that, as measured by levels of recall, the PD and HD patients were not more vulnerable than the normal controls to the effects of the short-delay or to RI. (Two HD subjects obtained scores at the floor on both Trial 5 and short-delay free recall, and these subjects were excluded from the above RI analysis.) Another manifestation of RI would be the intrusion of List B items during delayed free and cued recall of List A. Mann-Whitney tests showed that the three groups did not differ on this variable (p > .15 for all comparisons); the median numbers of these intrusion errors were 0.00,1.OO, and 1.oO in the normal, PD, and HD groups, respectively. In addition, the percentages of these intrusion errors relative to the total number of delayed-free and cued-recall responses were not significantly different in the three groups (p > .10 for all comparisons). Finally, when level of List B recall was adjusted for by calculating the percentage of List B intrusions during List A delayed recall relative to the number of items recalled on the List B recall trial, the group differences were again not significant (p > .10 for all comparisons). Overall Intrusions and Perseverations There was not a significant group effect for the standard scores of the overall number of intrusion errors made on the free-recall trials (see Table 3), but the PD and HD patients obtained significantly higher intrusion scores on the cued-recall trials than the controls. Because the patient groups gave fewer overall responses than the normals, the percentages of responses that were intrusions were also examined. Mann-Whitney tests revealed no significant group differences in the percentage of intrusion errors made during the five List A learning trials @ > .15 for all comparisons). The median percentages of the normal, PD, and HD groups were 1.56, 2.44, and 3.45, respectively. However, on the short- and long-delay free-recall trials, Mann-Whitney tests showed that the PD and HD groups both produced significantly higher percentages of intrusion errors than the controls (p < .01 for both comparisons), but that the patient groups did not differ (p > .90). The median percentages of the normal,PD, and HD groups were 0.00,16.67, and 15.59, respectively. Similarly, the PD and HD groups both gave significantly higher percentages of intrusion errors than the controls on the short- and longdelay cued-recall trials @ < .001 for both comparisons) and did not differ from each other (p > .40). The median percentages for the normal, PD, and HD groups were 3.45.20.83,and 18.86, respectively. It is important to examine the types of intrusion errors committed. Intrusions that are semantically unrelated to target words (i.e., from different semantic categories) represent a greater breakdown in memory discrimination than do intrusions that are semantically related to target words (i.e., from the same semantic categories). It was found that the three subject groups produced very few

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semantically unrelated intrusions. In fact, in all three groups the median number of these intrusions was zero. Mann-Whitney tests showed no significant group differences in either the absolute number of such intrusions across all immediate- and delayed-recall trials or in the percentage of these errors relative to the total number of responses given across all trials (p > .05 for all comparisons). Thus, although the patient groups produced greater proportions of intrusions, these intrusions were qualitatively similar to those given by normals-they were almost always semantically related to target words. The HD subjects obtained significantly higher perseveration scores (i.e.. made more perseveration responses) than thz PD subjects (see Table.3). Group differences were also evident when the percentages of perseverative responses relative to the total number of responses given were calculated. These median percentages for the normal, PD and HD groups were 2.38,0.00, and 8.42, respectively. Mann-Whitney tests revealed that the HD group’s percentage was significantly higher than the normal and PD groups’ percentages (p < .005 for both comparisons) and that the normal and PD groups did not quite differ significantly (p > .02).

Recognition Memory On recognition testing, the patient groups obtained significantly lower standard scores than the control group on the discriminability index (a nonparametric signal detection measure that reflects the ability to discriminate between hits and false positives); however, the PD and HD groups did not differ on this variable (see Table 3). The group effect for the response bias variable was not significant. In order to examine whether the patient groups benefited from the recognition testing format, difference scores between recognition discriminability and longdelay free recall were analyzed. Scores from the normal group were omitted from this analysis, because their high level of recall left little room for improvement on recognition testing. Also, one HD subject obtained scores at the floor on both measures and was excluded from the analysis. The PD group’s mean difference score of .58 did not differ from zero (p = .12), but the HD group’s mean difference score of 1.06 was significantly different from zero, ? (17) = 3.12, p < .01. This improvement of over a full standard deviation (relative to the CVLT normative sample) on recognition testing indicated that the HD patients benefited substantially from aid to retrieval. The PD and HD groups’ difference scores were not significantly different, however, ? (35) = -.97, p = .34. The PD and HD patients obtained significantly higher false positive standard scores (i.e., made more false positive errors) than the controls. In addition, the types and frequencies of false positive errors made by the PD and HD patients were examined in more detail. First, the incidence of false positive errors that were List B items was examined. Since recall of List B items should influence the potential for these items to be endorsed during recognition testing, the percentage of these false positive errors relative to the number of items recalled on the List B trial was calculated for each subject. Mann-Whitney tests revealed

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PAUL J. MASSMAN ET AL.

significant group differences (p c .00l) between the normal and PD, and normal and HD groups on this percentage index. The median percentages for the normal, PD, and HD groups were 0.00,50.00,and 85.71.Thus, the PD and HD patients’ recall of List B items appeared to dispose them to endorse List B items when attempting to recognize List A items. Incorrect endorsements of List B items could be characterized as ‘good’ errors since these items were, in fact, presented. False positive errors in response to distractors that were never presented are indicative of more serious problems in discrimination. As noted previously, on the CVLT recognition test there are non-List B distractors that are either phonemically similar to targets, prototypical of the targets’ semantic categories, or semantically and phonemically unrelated to the targets. The numbers of false positive errors made in response to these three types of distractors were summed for each subject (the highest possible error score was 20). Mann-Whitney tests showed that the PD and HD patients’ summed scores did not differ (p > .go), but both patient groups differed significantly from the normal controls (p < .001 for both comparisons). The median error scores for the normal, PD, and HD groups were 0.00,3.00, and 2.00, respectively. Only 1 of 19 normals made 2 or more such errors, while 13 of 19 PD patients and 13 of 19 HD patients made 2 or more of these errors. Thus, while not committing an overwhelming number of these more serious false positive errors, the PD and HD subjects were clearly more prone to make at least 2 such errors than were normals.

DISCUSSION

Considering the results as a whole, the similarities between the PD and HD groups were more impressive than their differences. These similarities included impaired immediate memory spans, inconsistency of recall across trials, deficient use of a semantic clustering learning strategy, normal retention of information over delay periods, normal vulnerability to proactive or retroactive interference, elevated intrusion rates on delayed recall, impaired recognition memory, and normal types of intrusion errors (i.e., intrusions semantically related to target words). Thus, in characterizing these aspects of memory performance, the term ‘subcortical dementia’ does appear to have explanatory utility. These prominent resemblances suggest that, although the neurotransmitter deficits characteristic of the diseases are quite different, basal ganglia neuropathology in PD and HD causes a distinctive pattern of spared and impaired components of verbal learning and memory functioning. Specifically, it appears that on the CVLT, basal ganglia dysfunction is associated with mildly deficient encoding (as reflected in mildly impaired recognition memory performance and heightened delayed-recall intrusion rates), intact storage (normal retention over delay periods, even in the face of interference), and marked difficulty initiating systematic retrieval strategies (impaired semantic clustering and inconsistent recall of words from trial to trial). It is likely that the bradyphrenia characteristic

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of PD and HD patients interferes with their ability to utilize active, efficient encoding and retrieval strategies on an unstructured learning and memory task such as the CVLT. However, it has been demonstrated that HD patients are able to benefit from encoding cues when they are instructed to use cues which are provided for them at stimulus presentation (Butters et al., 1983; Granholm & Butters, 1988). Thus, it appears that HD does not disrupt fundamental encoding processes, but interferes with the spontaneous utilization of effective encoding strategies. In contrast, even on structured retrieval tasks of modest difficulty, such as category fluency, HD patients perform very poorly, suggesting that basic retrieval processes are defective (Butters et al., 1987). The pattern of verbal learning and memory performance displayed by the PD and HD patients is quite different from that typically shown by AD (cortical dementia) patients. AD patients exhibit severe recognition memory deficits and generate excessive numbers of intrusion errors (Butters et al., 1987; Fuld, Katzman, Davies, & Terry, 1982; Ober et al., 1985), indicative of markedly impaired encoding processes. Unlike HD patients, AD subjects do not benefit from encoding aids provided for them (Butters et al., 1983; Granholm & Butters, 1988). Additionally, unlike the PD and HD subjects in the present study, AD patients have been found to have severe storage deficits, as reflected in their very poor retention of both verbal and visuospatial information (Butters et al., 1988; Moss, Albert, Butters, & Payne, 1986, Wilson, Bacon, Fox, & Kaszniak, 1983). Lastly, AD patients’ recognition memory impairment is as severe as their freerecall impairment (Delis et al., in press), whereas the HD patients in the current study showed disproportionate improvement on recognition testing (see also Butters, Wolfe, Granholm, & Martone, 1986; Butters, Wolfe, Martone, Granholm, & Cermak, 1985). This suggests that retrieval deficits are more salient in HD than in AD. Overall, these results appear to provide further support for the neuropsychological validity of the cortical-subcortical dementia distinction. There were, however, a number of differences between the CVLT performances of the PD and HD groups. The HD group displayed greater free recall impairment, a deficient rate of improvement across learning trials, and an increased perseveration rate. Also, the HD patients clearly showed supranormal improvement on recognition testing compared with free recall, and the PD patients exhibited only a trend @ = .12) toward disproportionate improvement on recognition. Finally, the PD group exhibited normal serial position effects, whereas the HD group showed a reduced primacy effect and an accentuated recency effect. Impaired primacy recall has been reported previously in HD patients (Wilson et al., 1987), as well as in amnesic patients (Baddeley & Warrington, 1970) and AD patients (Wilson, Bacon, Fox, & Kaszniak, 1983), and has been equated with deficient long-term storage. In contrast to amnesic and AD patients, though, HD patients in the present study displayed normal retention of information over time and disproportionate improvement on recognition testing. Thus, it seems problematic to attribute their reduced primacy recall to impaired storage. It can be argued that primacy words are more difficult to retrieve

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than recency words, so HD patients’ retrieval deficits may play an important role in their impaired primacy recall. The foregoing differences in performance between PD and HD patients appear to be quantitative rather than qualitative, and suggest that the HD group had more severe retrieval deficits than the PD group. The nature and extent of this greater impairment should be investigated further, by comparing the performances of P D and H D patients on more structured, less demanding retrieval tasks, such as category and letter fluency. In summary, these results indicate that the aggregation of PD and HD under the rubric of ‘subcortical dementia’ is appropriate for characterizing the majority of their spared and impaired components of verbal learning and memory. The few differences in performance that did emerge suggest that HD patients have greater retrieval deficits than PD patients.

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Are all subcortical dementias alike? Verbal learning and memory in Parkinson's and Huntington's disease patients.

The utility of the concept of 'subcortical dementia' was investigated by comparing the verbal learning and memory abilities of Parkinson's disease (PD...
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