stimulus-preference and memory factors in korsakoff's ... - Science Direct

Neuropsyehologia,1977, Vol. 15, pp. 99 to 106. PergamonPress. Printed in England.

STIMULUS-PREFERENCE AND MEMORY FACTORS IN KORSAKOFF'S SYNDROME* MARLENE OSCAR-BERMAN'~ a n d INA SAMUELS~

Aphasia Research Center, Boston Veterans Administration Hospital, and Neurology Department, Boston University School of Medicine, 150 So. Huntington Avenue, Boston, MA 02130, U.S.A. ;'{" and Psychology Department, University of Massachusetts, Boston, MA, U.S.A.:[: (Received 7 December 1975)

Abstract--Patients with Korsakoff's syndrome were compared to aphasic patients and to neurologically-intact control subjects on a task designed to assess the effects of stimulus preferences on visual discrimination learning and retention. Although both the Korsakoff and the aphasic groups made more errors on this task than the normal controls, the two braindamaged groups showed different patterns of response: (1) Korsakoff patients made more errors on non-preferred than on preferred stimulus dimensions, while the aphasics did not, and (2) only the Korsakoffs made significantly more errors on later test trials than on earlier ones. These results support previous suggestions that Korsakoff's disease may affect cognitive functioning independently of retention. RECENT studies of Korsakoff's syndrome due to alcoholism are consistent in demonstrating severe deficits for these patients on a variety o f m e m o r y tasks [1-5]. The question remains, however, whether difficulties in retention are the sole factor underlying the p o o r performance o f K o r s a k o f f patients, or whether these patients have cognitive deficiencies which are independent o f their m e m o r y problems. In a series o f dichotic listening tasks, GLOSSER, BUTTERS and SAMUELS[6] have shown that the performance of Korsakoff patients deteriorates with increasing information load. That is, Korsakoff patients performed normally when required to identify a single critical digit presented in either or both ears, but were impaired when two critical digits were presented simultaneously. In a separate series of investigations, OSCAR-BERMAN [7] has assessed the cognitive strategies employed by Korsakoffs (and other brain-damaged patients) on visual discrimination problems involving stimuli that varied along several dimensions (i.e. shape, color, size and position). The strategies used by K o r s a k o f f patients were inefficient and most often did not lead to correct solutions. K o r s a k o f f patients tended to perseverate with one or two preferred hypotheses (e.g. color and/or size) while ignoring the remaining stimulus dimensions. Further, they continued to focus u p o n a limited n u m b e r o f stimulus dimensions even when they were provided with m e m o r y aids such that problem solution depended u p o n information fully available at the time o f testing. The findings o f OSCAR-BERMAN [7] and GLOSSER et al. [6] suggest that K o r s a k o f f patients are limited in the a m o u n t o f relevant information they can process from complex stimuli. *Preliminary results of these experiments were presented at the 81st annual meeting of the American Psychological Association, Montreal, Quebec, 1973. Support for this study was provided by in part by PHS Grants NS-10577 and NS-06209 to Boston University, and NS-07615 to Clark University. Reprint requests may be sent to M. O-Berman, BVAH, 150 So. Huntington Ave., Boston, MA 02130. 99

100

MARLENE OSCAR-BERMANand INA SAMUELS

To assess this possibility, the present study employed a modified version of the procedure used by HOUSE and ZEAMAN [8] for testing discrimination learning in retardates. This procedure permits an analysis of the specific stimulus dimensions and cues used by subjects during visual discrimination learning. Dimensions are broad categories of stimulus characteristics (such as color, size, form and position) while cues are subsets of a dimension (red and blue, for example, are color cues; large and small are size cues; etc.). With this procedure, we sought to answer the following questions: (a) Are Korsakoff patients restricted in the number of dimensions (or cues) they process? (b) Do Korsakoff patients make more errors on non-preferred than on preferred stimulus dimensions and cues? (c) Can the performance of Korsakoff patients be improved by the use of memory aids ? METHOD Subjects There were a total of 41 subjects from the Boston VA Hospital, divided into the following four groups: (I) 10 male Korsakoff patients, diagnosed by the neurology services of the Boston and/or Brockton VA Hospitals; (2) 10 male left-hemisphere, brain-damaged controls from the aphasia ward; (3) 10 male alcoholic controls from the medical, surgical or psychiatric wards, with no clinical signs of Korsakoff's disease; and (4) a normal control group consisting of 11 staff members or neurologically intact hospital patients. The Wechsler Adult Intelligence Scale and four subtests of the Wechsler Memory Scale (information, orientation, digit span and paired-associate learning) were given to the Korsakoff patients to insure that their I.Q.'s and digit spans were within normal range; the mean I.Q. for this group was 104 (range, 95-123). In addition performance I.Q. scores were obtainable from 8 of the 10 aphasics (mean 91, range 66-103). Portions of the Wechsler Memory Scale also were given to all but one of the alcoholics (discharged early) to substantiate the clinical evaluation of no memory impairment; their scores are compared to those of the Korsakoffs in Table 1. The mean age of the Korsakoffs was 53 yr (range 42-66), and the etiology of the syndrome was Table 1. Comparison of Korsakoffs and alcoholic controls on subtests of the Wechsler Memory Scale SUBTESTS Informat ion

Orientation

Paired Associates

Alcoholics

5,2

4.9

9.2

6.9

5.0

Korsakoffs

2.6*

2.9"

6.7

7.0

4.2

Groups

Digit s p a n Forward Backward

*Significantly different from alcoholic controls (Mann-Whitney U-test, P < 0.01). associated with chronic alcoholism. All of the brain damaged controls (aphasics) had good to moderately good verbal comprehension; the projected site of lesion was predominantly frontal in eight patients (six due to vascular disease; one tumor; one head trauma), predominantly posterior in one patient (vascular disease), and mixed in one patient (vascular disease). The mean age of the aphasic group was 49 yr (range 38-61). The mean age of the alcoholic group was 46 yr (range 31-54). The mean age of the normal group was 26 yr (range 20-45). Since the mean ages differed among the groups of subjects, comparisons were made within groups, based upon ranks of performance (total errors) and age, using the Spearman rank order correlation test. There were no significant correlations between age and performance within any of the groups; correlations ranged between r = 0-115 and r = 0"291. Procedure

Subjects were given a series of 12 two-choice visual discrimination problems. Each problem was presented for one training trial and four test trials. On the training trial of a problem, the two stimuli differed atong the dimensions of color, size, form and position. For example, a large red X on the left might be paired with a small blue T on the right. The subject was required to guess which of the two stimuli was the one (preselected by the experimenter) to be correct, and following his choice, was told "correct" or "incorrect" according to a prearranged order. A response made by the subject might be on the basis of a single dimen-

STIMULUS-PREFERENCE AND MEMORY FACTORS IN KORSAKOFF'S SYNDROME

10l

sion (e.g. color) or some combination of dimensions (e.g. color and size). Therefore, the four separate test trials which followed were designed to determine which, if any, of the four dimensions had been most relevant to the subject on the training trial. As can be seen in Fig. 1, this was done by presenting on each

Training trial

Test trials

FIG. 1. Examples of stimuli used in the training trial and test trials. An arrow over the correct training stimulus was used in the memory-aid condition. On test trials, each card contained only one relevant dimension (large, dark, X and left, respectively, for these four trials). test trial, only one of the four pairs of relevant training cues at a time, and excluding the other three. For example, if a large dark-colored X on the left was the correct stimulus of a training pair (and the small light-colored T on the right was incorrect), the subject would perform perfectly on the first test trial if he were to choose large but not small (when given a choice of two different-sized black squares in relative u p down positions). Perfect performance on test trials two, three and four, respectively, would require selection of the dark color but not the light one (when given a choice of a dark and a light square of identical sizes in up-down positions); X and not T (when given a choice of those two letters, equal sizes, black and in u p down positions); and left, not right (when given the choice of a black square on the left, and an identical black square on the right). The entire series of 12 problems was presented twice. In a standard condition, the training pair was removed from the subject's view during test trials; in a memory-aid condition [9], training stimuli were present throughout a problem, and the correct one was marked clearly with an arrow. One measure of retention could be obtained by comparing performance on standard problems with performance on memoryaid problems. In addition, since for any single problem, test-trials one and two were closer in time to the training trial than test-trials three and four, a second estimate of retention could be obtained by comparing the number of errors made on the first two test trials with errors made on the last two; this measure was especially relevant in standard problems, where training stimuli were absent during test trials. All test trials were arranged such that cues from each dimension appeared equally often as first, second, third and fourth choices, and the entire procedure was preceded by a series of four practice problems to insure that subjects understood the instructions. Estimates of dimensional and cue preferences also were obtained. Prior to the start of this study, all of

102

MARLENE OSCAR-BERMAN a n d INA SAMUELS

the subjects were run through LEVINE'S[10] blank-trials testing procedure in order to determine hierarchies of hypotheses or response strategies in two-choice visual discrimination problems employing the same dimensions and cues as in the present study (see [7] for more detail on that procedure~. The two hypotheses used most frequently by an individual subject in the Levinian tasks defined that subject's preferred dimensions (PD), and the two strategies used least frequently were defined as non-preferred (NPD). We were interested in determining on test trials of the present study, whether or not Korsakoff subjects would make significantly fewer errors on preferred dimensions than on non-preferred dimensions (as compared to controls). For example, if a subject's hierarchy or responses had been found by the Levinian procedure to be form first, color second, size third and position fourth, would he be more accurate on test trials involving form or color (PD) than on size or position (NPD)? Preference for cues were determined from a subject's initial choices on the training trials of the present study. Since on a randomly selected half of the training trials, a subject was told that his initial responses were correct, these choices were defined as responses to his preferred cues (PC); on the remaining training trials, where the subject was informed that his initial choices were incorrect, the positive stimuli were designated as the non-preferred cues (NPC). Cue preferences measured this way were compared with performance on test trials, in order to determine relative accuracy with preferred and non-preferred cues. For example, if a subject initially chose the large, dark X on the left (whether or not it was the correct stimulus), would he be more likely on test trials to select large, dark, X and left (PC's) than small, light, T and right (NPC's)? RESULTS E a c h o f the m a j o r d e p e n d e n t v a r i a b l e s ( d i m e n s i o n preferences, cue p r e f e r e n c e s a n d r e t e n t i o n scores) was s u b j e c t e d to s e p a r a t e analyses o f v a r i a n c e in w h i c h G r o u p effects c o u l d be assessed. Significant m a i n effects o f g r o u p s w e r e o b t a i n e d in all cases, p e r m i t t i n g s u b s e q u e n t i n t e r g r o u p c o m p a r i s o n s w i t h i n d e p e n d e n t t-tests. C h a n g e s w i t h i n g r o u p s (difference scores) w e r e assessed by m e a n s o f c o r r e l a t e d t-tests.

Dimensional analyses F i g u r e 2 a n d T a b l e 2 s h o w the m e a n n u m b e r o f e r r o r s c o m p i l e d by the f o u r g r o u p s o n t h e p r e f e r r e d a n d n o n - p r e f e r r e d d i m e n s i o n s . F o r t h e s t a n d a r d c o n d i t i o n , the K o r s a k o f f Norrnals

• ........

Aphasics

× ........

• x

Alcoholics

g . . . .

m

Korsokofffs ~tandard

Memory - aid condition

condition

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°i

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PD

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.

.

.

.

.

.

.

i

f, PD

FIG. 2. Mean errors for each of the groups on problems containing non-preferred dimensions (NPD) and preferred dimensions (PD). Performance on the standard condition is shown on the left half of the figure, and performance with memory aids is shown on the right. p a t i e n t s w e r e significantly w o r s e t h a n n o r m a l a n d a l c o h o l i c subjects o n b o t h N P D a n d P D p r o b l e m s ( P < 0.05). T h e a p h a s i c s w e r e also i n f e r i o r t o n o r m a l s o n b o t h types o f p r o b l e m s ( P < 0.05 o r better). N o n e o f t h e r e m a i n i n g g r o u p differences was significant.

STIMULUS-PREFERENCE AND MEMORY FACTORS IN KORSAKOFF'S SYNDROME

103

Table 2. Distribution of mean errors by all groups on Standard (top) and Memory-aid (bottom) conditions. (Scores of the groups in parentheses are significantly different from the adjacent scores, P _< 0 0 5 or better.) Dimensior~

Groups

NPD

Normals

98

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~8

Dill,

h~C

PC

Diff.

.91

- .36

1.00

1.18

.18

1.27

4.70(N)

5 . 0 0 (N)

.30

5.20(N)

4.50(N) 1.60

Alcoholics

2.10

2.00

- ,i0

2.50

Korsakof f8

5.40(N;AI)

4.20(N;AI)

-I,20(N)

5.90(NIAI) 3.70(N)

Normals I '~

"PD

Cuee

Aphaslcs

.00 1.70(N)

~ A:coUol~., .70 mu Korsakoffs

2.30(N)

.00 1.40

.00

.00

- .30

1.70(N)

.40

- .30

1.00

.90(N)

-I.40(N)

1.70(N)

,10

1.50(N)

Triale

1 & 2

3 & 4

°54

I.i0

5.50(10

1.30

1.30

2.80

1.50

3.10(N)

6.50(N;AI)

3.40(N)

4.20(N)

- .90 -2.20

,00 -

.30

-

.90

- .20

~,

1.64

- .70

.00 1.40(N)

Trials

.00 1.70(N) .50

1.00(N)

.00 1.40(N)

,60 2,20(N)

.00 - .30

.10 1.20(Nikl;kp)

Although all groups showed significant improvements (P < 0.05 or better) with memory aids, the Korsakoffs remained inferior to normals on N P D and PD problems (P's < 0.05) and the aphasics made more errors than normals on N P D problems (P < 0.05). When differences between N P D and PD performance were analyzed for the four groups, only the Korsakoff patients made significantly more errors on their non-preferred than on their preferred dimensions in both the standard (P < 0.05) and the memory-aid (P ----0.05) conditions.

Cue analyses Table 2 also shows the mean number of errors for the four groups on preferred and non-preferred cues. In general, the pattern of results resembled that obtained for the dimensional analysis. For both the standard and memory-aid conditions, Korsakoff and aphasic patients made more errors than normal controls on preferred as well as nonpreferred cues (all P's < 0.05). In addition, the Korsakoffs were inferior to alcoholics on PC problems of the standard condition (P < 0.05). All groups also showed improved performance on the memory-aid, as opposed to the standard condition (P < 0.05). However, when considering the difference between errors to preferred cues and errors to nonpreferred cues, group differences disappeared. In particular, the Korsakoffs (like the other groups) showed no greater tendency to err on N P C problems than on PC problems, with or without memory aids. This negative result is not surprising since preferred cues are equally distributed among preferred and non-preferred dimensions as a result of the stimulus randomization procedure employed. However, it underscores the fact that dimensional preferences are, overall, more influential in determining error incidence than are individual cue preferences across dimensions.

Analyses of retention Retention was measured by comparing performance on trials 1 and 2 (early test-trials) with performance on trials 3 and 4 (late test-trials). These results are presented in Fig. 3 and Table 2. As before, the inferior performance of the Korsakoff and aphasic groups is

104

MARLENEOSCAR-BERMANand INA SAMUELS Normals Aphasics Alcoholics Korsakoffs

• ........ x ........ • ~3 .

.

.

.

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4

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FIG. 3. Mean errors for each of the groups on test trials 1 and 2, compared with errors on trials 3 and 4. Performance on the standard conditions is shown on the left half of the figure, and performance with memory aids is shown on the right. evident. Both of these groups were significantly inferior to the normal control group on early and on late trials, whether or not memory aids were employed (P < 0.05 in every case). The Korsakoffs also were inferior to the alcoholics on the later trials of the standard condition (P < 0.05). A comparison between the groups on the difference between errors made on early and late trials revealed that the Korsakoffs were the only subjects showing an abnormally high rise in error scores: in the standard condition, their increase in errors was greater than that of normals (P < 0.05), and in the memory-aid condition, their increase was greater than that of each of the other groups (P < 0.05 in every instance). DISCUSSION The present results indicate that mnemonic factors are critically involved in the transfer performance of all groups in the standard condition. When subjects are provided with memory aids, Korsakoffs and aphasics, as well as alcoholics and normal controls, show significant improvements in performance. While the absolute amount of savings is greatest for the Korsakoffs and aphasics, the percentage improvement from the standard to the memory-aid conditions does not differ significantly among groups. Although mnemonic factors affect the performance of all groups in the standard condition, deficits in retention are particularly evident in the case of the Korsakoff patients. When scores on early (1 and 2) and late (3 and 4) trials in the standard condition were compared, Korsakoffs were the only group to demonstrate an abnormally high increase in errors on later trials. This deterioration in performance as a function of the length of the retention interval, is consistent with the impairments in short-term memory previously reported for Korsakoff patients in a number of studies [3-5]. The data also support the suggestion that Korsakoff and aphasic patients have information-processing deficits which are independent of memory factors [11-14]. Even when subjects are provided with memory aids so that the information required for problem solution is fully available during testing, the Korsakoff and aphasic groups continue to

STIMULUS-PREFERENCE AND MEMORY FACTORS IN KORSAKOFF'S SYNDROME

105

show impairments on the transfer trials. The fact that aphasic and Korsakoff patients alike evidenced any impairment relative to normal control subjects may indicate the general sensitivity of the present task to the presence of brain damage; differences in patterns of errors, therefore, become of critical importance. In addition, it should be noted that performance by the alcoholic patients fell between that of the normals and the bona.fide neurological cases, implying as before (see [7, 11, 12]) that alcoholics may be approaching a Korsakoff condition not disclosed by standard clinical evaluations. Although the nature of the aphasics' deficit is ambiguous, the impairment of the Korsakoffs appears to involve a selective responsivity to certain stimulus attributes, and a disregard for the relevance of others. Thus, while aphasics (like normals and alcoholics) distributed their errors equally between preferred and non-preferred stimulus dimensions, Korsakoffs made significantly more errors on their non-preferred dimensions in both the standard and the memory-aid conditions. The selective focusing on preferred stimuli shown by the Korsakoff patients in this task in congruent with their performance on LV.VINE'S [10] hypothesis formation task [7]; stimulus dimensions which were utilized most frequently for hypothesis formation were also processed most effectively on transfer tests. These findings are consistent with the hypothesis that Korsakoff patients are limited in the amount of information they extract from multi-dimensional stimuli [6, 11]. The present findings also indicate the operation of an additional factor in the Korsakoff's impairment. As already noted, Korsakoff patients made significantly more errors on later than on earlier trials in the standard condition, a result attributable to their well-known impairments in short-term memory. However, Korsakoff patients continued to show higher error scores on later trials in the memory-aid condition, a finding which is not readily explicable in terms of memory deficits, since all the information necessary for solution is available during testing. Further, poorer performance on later trials is not related to stimulus preferences, since preferred and non-preferred dimensions and cues were randomized over trials. Although the Korsakoff's difficulties on the later transfer trials of this task appear analogous to those described by CERUAI¢ and BUTTERS [3] indicating increased sensitivity to proactive interference, the reasons for this effect remain unclear. Perhaps susceptibility to proactive interference is related to what TALLAND [I] has called "premature closure of activation", whereby Korsakoffs make responses prematurely, prior to receiving and/or retrieving all the relevant information necessary for problem solution (see also [12]). REFERENCES 1. TALLAND,G. A. DerangedMemory. Academic Press, New York, 1965. 2. SAMUELS,I., BUTTERS,N., GOODGLASS,H. and BRODY,B. A. A comparison of limbic and cortical damage in short-term visual and auditory memory. Neuropsychologia 9, 293-306, 1971. 3. CERMAK,L. S. and BLrrrERS,N. The role of interference and encoding in short-term memory deficits of Korsakoff patients. Neuropsychologia 10, 89-95, 1972. 4. WARRINGTON, E. K. and WEISKRAN'rZ,T. An analysis of short-term and long-term memory defects in man. In The Physiological Basis of Memory, J. A. DEUTCH(Editor). pp. 365-395, Academic Press, New York, 1973. 5. KINSBOURNE, M. and WooD, F. Short-term memory processes and the amnesic syndrome. In Short Term Memory, D. DEtrrcrI and J. A. DEUTCI-I(Editors). Academic Press, New York, 1975. 6. GLOSSER,G., BOTrERS,N. and SAMUELS,I. Failures in information processing in patients with Korsakoff's syndrome. Neuropsychologia (to be published). 7. OSCAR-BERMAN,M. Hypothesis testing and focusing behavior during concept formation by amnesic Korsakoff patients. Neuropsychologia 11, 191-198, 1973. 8. HousE, B. J. and ZEAMAN,D. Miniature experiments in the discrimination learning of retardates. In Advances in Child Development and Behavior, Vol. 1. Academic Press, New York, 1963.

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9. EIMAS,P. D. Effects of memory aids on hypothesis behavior and focusing in young children and adults. J. exp. ChildPsyehol. 10, 319-336, 1970. 10. LEVINE, M. Hypothesis behavior by humans during discrimination learning. J. exp. Psychol. 71, 331388, 1966. t 1. OSCAR-BERMAN,M., GOODGLASS,U. and CHERLOW, D. G. Perceptual laterality and iconic recognition of visual materials by Korsakoff patients and normal adults. J. comp. physiol. Psyehol. 82, 316-321, 1973. 12. OSCAR-BERMAN, M., SAHAKIAN,B. J. and WIKMARK, G. Spatial probability learning by alcoholic Korsakoff patients. J. exp. Psychol.: Human Memory and Learning 2, 215-222, 1976. 13. EISEr~SON,J. Adult Aphasia. Appleton-Century-Crofts, New York, 1973. 14. PIERCY, M. The effects of cerebral lesions on intellectual function: a review of current research trends. Brit. J. Psychiat. 110, 310-352, 1964.

R~sum~ : On a compar~ des malades avec syndrome de Korsakoff des aphasiques et des sujets de contr~le sans atteinte neurologique sur une ~preuve c r ~ e pour juger des effets de preference de stimulus sur l'apprentissage et la r~tention de discrimination visuelle. Bien que les groupes de Korsakoff comme les groupes aphasiques commettent plus d'erreurs dans cette ~preuve que les contr6les, les 2 groupes avec l~sion c~r~brale montraient des types diff~rents de r~ponse : 1 ° les malades avec syndrome de Korsakoff commettent plus d'erreurs sur les dimensions du stimulus non pr~f~r~es que sur celles pr~f~r~es, ce que ne font pas les aphasiques. 2 ° Ce sont seulement les Korsakoffs qui commettent significativement plus d'erreurs sur les derniers essais que sur les premiers. Ces r~sultats sont en faveur des suggestions ant~rieures selon lesquelles la maladie de Korsakoff peut affecter le fonetionnement cogni tif, ind~pendamment de la r~tention.

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