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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
Subjective Ordering and Working Memory in Alcoholic Korsakoff Patients Sjoerd Wiegersma Dieren a
a c
a
, Elke de Jong & Marijke van
b
University of Utrecht , Julianaoord, Laren
b
Neurological and Orthopedic Clinic , Julianaoord, Laren c
University of Utrecht, vakgroep Psychonomie , Heidelberglaan 2, Transitorium 2, De Uithof, 3508 CS, Utrecht, the Netherlands Published online: 04 Jan 2008.
To cite this article: Sjoerd Wiegersma , Elke de Jong & Marijke van Dieren (1991) Subjective Ordering and Working Memory in Alcoholic Korsakoff Patients, Journal of Clinical and Experimental Neuropsychology, 13:6, 847-853, DOI: 10.1080/01688639108405102 To link to this article: http://dx.doi.org/10.1080/01688639108405102
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
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This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sublicensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Clinical and Experimental Neuropsychology 1991, Vol. 13, NO. 6, pp. 847-853
0168-8634/91/1306-0847$3.00 0 Swets & Zeitlinger
Subjective Ordering and Working Memory in Alcoholic Korsakoff Patients* Sjoerd Wiegersma, Elke de Jong University of Utrecht
Downloaded by [Tufts University] at 13:51 02 December 2014
and Marijke van Dieren Neurological and Orthopedic Clinic, Julianaoord, Laren
ABSTRACT Frontal-lobe dysfunction of alcoholic Korsakoff patients was studied by presenting four tasks requiring short-term retention, as well as different degrees and types of control. Digit span forward was considered a measure of passive short-term retention; missing scan measures memory search and comparison, in addition to retention; and two subjective ordering tasks measure active generation of responses in addition to the processes in the other two tasks. The results showed no evidence of reduced performance for any of these tasks, when compared with performance of control subjects. The hypothesis that Korsakoff patients have a frontal-lobe dysfunction in addition to their amnesia needs some qualification because of these results: Frontal-lobe function specific to the ordering of verbal responses seems to be intact in Korsakoff patients.
The cognitive disruption in alcoholic Korsakoff patients is characterized by amnesia as well as some cognitive deficits, which seem to be independent of the memory deficits (Squire, 1982). These deficits include problems with the division of attention, perseveration of responses, deficits in shifting attention and susceptibility to interference (Oscar-Berman, 1984), and suggest that some damage to the frontal lobes has occurred (Moscovitch, 1982). This study is directed at possible frontal-lobe involvement in the alcoholic Korsakoff syndrome. In a previous study with frontal-lobe patients we used four tasks which all required short-term retention of numbers and which differed in the degree and type of the control processes involved. These tasks were digit span forward, missing scan, randomization span, and randomization span visual. The first requires recall of aurally presented sequences of digits. The second requires the detection of the missing number in a randomly arranged sequence,
* Correspondence and reprint requests should be addressed to Dr. Sjoerd Wiegersma, University of Utrecht, vakgroep Psychonomie, Heidelberglaan 2, Transitorium 2, De Uithof, 3508 CS Utrecht, the Netherlands. Accepted for publication: December 26, 1990.
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made up of all the numbers minus one, of a set of numbers (1-3, 1-4, etc.). The other two tasks require the random production of short sequences, to be made of sets of numbers (1-3, 1-4, etc.), with the restriction of not repeating the same digits nor using counting orders. The latter two tasks are called subjective ordering tasks and showed deficits in frontal-lobe patients, whereas the former two tasks showed almost intact performance when compared with control subjects (Wiegersma, van der Scheer, & Hijman, 1990). These results were explained by a deterioration in an active generation component of subjective ordering, while the short-term retention and comparison components were supposed to remain intact as shown by the intact performance at digit span forward and missing scan. Such results can be explained by a theoretical framework, in which a working memory is built up of a passive short-term retention component and an active control component, the latter being selectively deficient in frontal-lobe patients (Baddeley, 1986; Norman & Shallice, 1986). Since Korsakoff patients show so many signs of the frontal-lobe syndrome, it seemed worthwhile studying these patients with the same set of tasks. The short-term retention component is relatively intact in amnesia (e.g., Baddeley & Warrington, 1970). being somewhat lower than normal, but still within the normal range (Parkinson, 1982). Hence, if alcoholic Korsakoffs suffer from a frontal-lobe syndrome with relatively intact short-term retention, they should be selectively impaired in the subjective ordering tasks, with relatively unimpaired digit span. As to the missing scan, predictions are less clear. If memory comparison processes are involved in the disorder, performance on this task should be impaired. If only the response generation component of subjective ordering suffers from the disorder, then missing scan performance should remain intact in the patients.
METHOD Design The four experimental tasks mentioned above were presented to alcoholic Korsakoff patients and normal control subjects. The tasks were presented in a pseudo-random order, such that all four tasks occurred equally in each position. After completion of these four tasks, all subjects performed five Word Fluency tasks, also in random orders. These tasks were added. because they require the production of sequences as in the subjective ordering tasks, but are different from these in that they require retrieval from long-term memory. Since the subjective ordering tasks are supposed to be short-term memory tasks, Korsakoff patients who suffer from amnesia should be more severely impaired at the Word Fluency tasks than at the subjective ordering tasks. Subjects Sixteen Korsakoff patients of the ‘Neurologische en Orthopedische Kliniek Julianaoord’ at Laren, the Netherlands, participated.The diagnosis ‘Korsakoff Syndrome’ was established by using the following criteria. Intelligence was within the normal range, considering age and education (mean WAIS-IQ was 95.2; range 79-1 14). Deficits of long-term memory were measured with Rey’s Verbal Learning Test. Mean total recall score over five trials was 19.3 (range: 10-31; 11 patients scored in the f i i t decile of the normative distribution
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of healthy subjects). Mean delayed recall after 20 min was 1.0 (range 0-5), and mean delayed recognition was 9.8 (range 2-14). The frontal-lobe patients of the previous experiment (Wiegersma, van der Scheer, & Hijman, 1990) scored considerably higher on these measures: 37.0 for total recall, 7.8 for delayed recall, and 12.8 for delayed recognition. Rey (1964, pp. 150-151) gives normative values for healthy manual laborers for total recall (57.7) and delayed recognition (14.5). For the intellectual professions the norms are 61.6 and 14.9 respectively. The story of Binet-Bobertag showed a mean recall score of 9.1 (range 2-14). One subject, scoring high (14) at this test, was nevertheless admitted, since she was very low at all parts of Rey's Verbal Learning Test (total recall: 10; delayed recall: 1; delayed recognition: 2). All subjects showed alcohol abuse in the recent past. Cases caused by different etiology (tumour, trauma, etc.) were excluded. Sixteen control subjects were matched to the patients with respect to sex, age, and education. There were 10 women and six men in each group. Mean age was 53.6 years (range 33-67) for the patients and 54.6 years (range 37-67) for the controls. For the estimation of education we used a seven-point scale as presented by the Manual of the Groninger Intelligentie Test (Luteijn & Van der Ploeg, 1983). Median education was 4.0 (range 2-5) for Korsakoffs and 4.0 (range 2-6) for controls. Procedures All four experimental tasks involve short-term retention and make use of numbers. The tasks differ in the degree that control processes are required and in the type of control processes. One practice trial at level three was given in each task before testing started. There was one trial at each level as long as the subject was correct. In the case of failure, an additional trial at the same level was presented. Testing in all tasks was finished when the subject also failed at the second trial.
Digit span forward. Subsets of the numbers 1-12 were aurally presented at a rate of one number per second, for immediate recall by the subject. The first sequence consisted of three numbers, the second of four, etc. Free recall was allowed, in order to make the task more comparable to the other tasks (Buschke, 1963). There was one sequence for each level, except when an error was made. In that case, a second opportunity at the same level was given with a new sequence. The subject earned three points if the first level of three numbers was successfully completed, one additional point for each correct first trial at a higher level and 0.5 point if only a second trial was correct. If both trials of one level were wrong, testing was finished.
Missing
scan. Random sequences of n-1 numbers, randomly selected from sets of n numbers, were presented at a rate of one per second. Set size ( n ) was gradually increased from three (numbers 1-3). through four (numbers 1-4), etc., until the subject failed to mention the missing number. The set of possible numbers was given by oral instruction and visually presented to the subject on a card (in this way: 1-3 or 1-4, etc.) which remained visible to the subject until the trial was completed., Scoring was as for digit span.
Randomization span. Subjects had to select responses from sets of numbers (1-3,1-4, etc.) in a self-chosen ordering, with the restrictions of avoiding repetition and counting forward or backward. A randomly selected number to start with was provided by the experimenter. If the patient or control subject produced a sequence with three or more numbers in counting order forward (e.g., 5, 6 . 7 or 2, 3 and 5, 6) or four or more numbers backward (e.g., 1 0 , 9 , 8 , 7 ) an additional opportunity was given at the same level, after repetition of the instructions. If the subject failed in the second trial, a third opportunity was given at that level. This was done to make sure that failure in the patients was not due to forgetting the instructions. The set of numbers allowed remained visually available on a card (1 -3,
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SJOERD WIEGERSMA ET AL.
1-4, etc.) during production of the sequence as in the missing item task. The rate of production was self-placed. Scoring was as for digit span and missing scan. Subjects got 0.5 point for a level where one of the added trials was correct.
Randomization span visual. This task is identical to the randomization task, except that all admitted alternatives are presented to the subject in a different visual arrangement. Vocal responses were required. A comparable task, but requiring pointing responses rather than vocal responses, has been used by Petrides and Milner (1982) and Wiegersma, van der Scheer, and Hijman (1990) in studying frontal-lobepatients. Vocal responses were preferred in the present study in order to minimize possible confounding with spatial factors. The subject selects one of n alternativenumbers (1-3. 1-4, etc.) from sheets of paper, while the
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experimenter turns them over at a rate determined by the speed of production of the subject. Instructions and scoring were as in the randomization task. Word-Fluency Tasks The subject produces as many words of a semantic category (animals or professions) or beginning with certain letters (M, S, or K) as possible in 1 minute for each of the five categories.
RESULTS The results at the experimental tasks are presented in Table 1. An analysis of variance with repeated measures over tasks showed that there was no significant effect of group (F < l), nor of the interaction of group and task (F c 1). Only the main effect of task showed statistical significance (F (3,90) = 33.12, p < .001). Neither age nor educational level showed significant product-moment correlations with any of the four experimental tasks. Although direct comparison of experiments is difficult because of small procedural differences, we also give the values of the frontal-lobe patients in Wiegersma, van der Scheer, and Hijman (1990): 5.4 (digit span), 8.7 (missing scan), 5.3 (randomization), and 4.9 (randomization visual). The frontal-lobe patients generally scored lower, but especially so on the subjective ordering tasks. The control subjects in the present experiment score lower on subjective ordering than those in the previous experiment, probably because they are older. An aging effect on subjective ordering has been shown by Wiegersma and Meertse (1990).
Table 1. Means (standard deviations) of the spans of alcoholic Korsakoff patients and normal controls for the four experimental tasks. DS = digit span, MS = missing scan, R = randomization span, R V = randomization span visual. Group Patients Controls
DS
MS
R
RV
6.0 (1.6) 6.0 (1.2)
9.4 (2.3) 9.8 (2.1)
6.6 (2.6) 6.8 (2.0)
5.9 (1.9) 6.1 (1.9)
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Table 2. Means (standard deviations) of Korsakoff patients and normal controls for the Word Fluency tasks. Group
Animals
Professions
M
S
K
Patients Controls
15.2 (3.7) 22.6 (5.4)
12.9 (4.9) 16.1 (5.4)
12.4 (5.3) 15.1 (5.9)
11.4 (4.5) 15.3 (4.6)
11.7 (4.3) 16.8 (6.1)
The results at the Word-Fluency tasks are presented in Table 2. There was a significant main effect of group ( F (1,30) =9.77, p < . O l ) and of task ( F (4,120) = 15.84, p < .OOl). The interaction effect of group and task was not significant.
DISCUSSION We did not find evidence in Korsakoff patients for the pattern of results found in frontal-lobe patients. The Korsakoffs perform at about the same level as controls in all four experimental tasks. The Korsakoffs only needed a few more trials in the subjective ordering tasks, since they more readily seemed to forget the instruction not to count than the controls, probably due to their amnesia. However, provided that they obey the instructions in this respect, they seem to be able to do all tasks at a normal level. Hence, Korsakoff patients show no evidence of being worse when control processes relevant to active sequential ordering are required. In that respect, they differ from patients with frontal-lobe lesions (Wiegersma, van der Scheer, & Hijman, 1990). How can these negative results with subjective ordering be explained? We would not like to suggest that the frontal-lobe syndrome is absent in Korsakoff patients, since it has been supported by a variety of tasks as well as anatomical evidence (Moscovitch, 1982; Oscar-Berman, 1984). Rather, it should be concluded that there is something special with the frontal-lobe syndrome of these patients, wherein subjective ordering is preserved while at the same time several other indicators show the characteristic decline. What is so special about subjective ordering as compared to other tasks which indicate frontal-lobe dysfunction? Subjective ordering has been analyzed in earlier studies by using so-called randomization tasks (Wiegersma, 1982, 1984). It requires short-term retention, comparison of probe responses with previous responses available in short-term memory and the generation of one of the responses not produced so far. The present study suggests that all of these are intact in Korsakoff patients as contrasted with frontal-lobe patients, where short-term retention and comparison appeared to be intact, while only the spontaneous generation component was defective. Hence, the frontal-lobe syndrome of Korsakoff patients is special in that the spontaneous generation component of subjective ordering is intact.
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At this point it is of interest to make a comparison to the fluency tasks, which showed deficient performance in Korsakoff patients in our study as well as previous ones (Butters, 1985; Butters, Granholm, Salmon, Grant, & Wolfe. 1987). Although this task also involves spontaneous generation of a sequence of responses, this differs in one important aspect from the subjective ordering task. In subjective ordering, the response is selected from the set of pre-activated items in short-term memory, such that retrieval from long-term memory is not required during task performance. In the fluency task, however, such retrieval is required. In other respects, both tasks are quite similar: both require the active production of a sequence of non-repetitions in a self-determined order. Hence, the critical difference probably is in the retrieval of words from long-term memory, which is defective in Korsakoff patients. In summary, considerable overlap has been shown between the memory disorders in alcoholic Korsakoff amnesia and frontal-lobe patients (Moscovitch, 1982). This leads to the question of whether the frontal-lobe disorder is to some degree fundamental to the amnesia in Korsakoff patients or not. On the other hand, a primary amnesia may constitute certain characteristics of the frontal executive syndrome. For example, problems with retrieval and recognition may be responsible for perseveration and lack of selectivity (Goldberg & Bilder, 1986). The overlap of the executive frontal syndrome and amnesia needs differentiation by tasks which show intact performance in one and deficient performance in the other disorder. Subjective ordering seems to be one such task. Future comparisons of frontal with Korsakoff patients, using planning and sequential production tasks which depend on short-term rather than long-term retention, should further delineate the frontal involvement in the cognitive disorder of Korsakoff patients. Such studies could clear up the question about the possible causal relationships between the executive syndrome and the amnesia of Korsakoff patients. For now, the possibility seems to remain, that at least some frontal symptoms of Korsakoff patients are not distinctive characteristics of a frontal syndrome, and may rather be the secondary characteristics of their amnesia.
REFERENCES Baddeley, A. (1986). Working memory. Oxford: Clarendon Press. Baddeley, A.D., & Warrington, E.K. (1970). Amnesia and the distinction between longand short-termmemory. Journal of Verbal Learning and Verbal Behaviour, 9, 176-189. Buschke, H. (1 963). Retention in immediate memory estimated without retrieval. Science, 140, 56-57, Butters, N. (1985). Alcoholic Korsakoff's syndrome: Some unresolved issues concerning etiology, neuropathology,and cognitive deficits. Journal of Clinical and Experimental Neuropsychology, 7 , 181-210. Butters, N., Granholm. E., Salmon, D.P., Grant, I., & Wolfe, J. (1987). Episodic and semantic memory: A comparison of amnesic and demented patients. Journal of Clinical and Experimental Neuropsychology, 9,479-497. Goldberg, E.. & Bilder, R.M.(1986). Neuropsychological perspectives: Retrograde amnesia
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and executive deficits. In L.W. Poon (Ed.), Handbook for clinical memory assessment of older adults (pp. 55-68). Hyattsville: American Psychological Association. Luteijn, F., & Van der Ploeg, F.A.E. (1 983). Groninger Intelligentie Test. Lisse, Netherlands: Swets & Zeitlinger. Moscovitch, M. (1982). Multiple dissociations of functions in amnesia. In L.S. Cermak (Ed.), Human memory and amnesia (pp. 337-370). Hillsdale, NJ: Erlbaum. Oscar-Berman, M. (1984). Comparative neuropsychology and alcoholic Korsakoff disease. In L.R. Squire & N. Butters (Eds.), Neuropsychology of memory (pp. 194-202). New York: Guilford. Norman, D.A., & Shallice, T. (1 986). Attention to action: Willed and automatic control of behavior. In R.J. Davidson, G.E. Schwartz, & D. Shapiro (Eds.), Consciousness and se®ulation: Advances in research, 4 (pp. 1-18). New York: Plenum. Parkinson, S.R. (1982). Performance deficits in short-term memory tasks: A comparison of amnesic Korsakoff patients and the aged. In L.S. Cermak (Ed.), Human memory and amnesia (pp. 77-96). Hillsdale, NJ: Erlbaum. Petrides, M., & Milner, B. (1982). Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia, 20, 249-262. Rey, A. (1964). L'Examen clinique enpsychologie. Paris: Presses Universitaires de France. Squire, L.R. (1982). Comparisons between forms of amnesia: Some deficits are unique to Korsakoff's syndrome. Journal of Experimental Psychology: Leurning, Memory and Cognition, 8 , 560-571. Wiegersma, S. (1982). A control theory of sequential response production. Psychological Research, 4 4 , 175-188. Wiegersma, S. (1984). Acoustic and semantic similarity effects on repetition avoidance in produced sequences. Memory and Cognition, 12, 190-194. Wiegersma, S., van der Scheer, E., & Hijman, R. (1990). Subjective ordering, short-term memory, and the frontal lobes. Neuropsychologiu, 28, 95-98. Wiegersma, S., & Meertse, K. (1990). Subjective ordering, working memory, and aging. Experimental Aging Research, 16, 73-77.
Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19
Subjective Ordering and Working Memory in Alcoholic Korsakoff Patients Sjoerd Wiegersma Dieren a
a c
a
, Elke de Jong & Marijke van
b
University of Utrecht , Julianaoord, Laren
b
Neurological and Orthopedic Clinic , Julianaoord, Laren c
University of Utrecht, vakgroep Psychonomie , Heidelberglaan 2, Transitorium 2, De Uithof, 3508 CS, Utrecht, the Netherlands Published online: 04 Jan 2008.
To cite this article: Sjoerd Wiegersma , Elke de Jong & Marijke van Dieren (1991) Subjective Ordering and Working Memory in Alcoholic Korsakoff Patients, Journal of Clinical and Experimental Neuropsychology, 13:6, 847-853, DOI: 10.1080/01688639108405102 To link to this article: http://dx.doi.org/10.1080/01688639108405102
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
Downloaded by [Tufts University] at 13:51 02 December 2014
This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sublicensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Clinical and Experimental Neuropsychology 1991, Vol. 13, NO. 6, pp. 847-853
0168-8634/91/1306-0847$3.00 0 Swets & Zeitlinger
Subjective Ordering and Working Memory in Alcoholic Korsakoff Patients* Sjoerd Wiegersma, Elke de Jong University of Utrecht
Downloaded by [Tufts University] at 13:51 02 December 2014
and Marijke van Dieren Neurological and Orthopedic Clinic, Julianaoord, Laren
ABSTRACT Frontal-lobe dysfunction of alcoholic Korsakoff patients was studied by presenting four tasks requiring short-term retention, as well as different degrees and types of control. Digit span forward was considered a measure of passive short-term retention; missing scan measures memory search and comparison, in addition to retention; and two subjective ordering tasks measure active generation of responses in addition to the processes in the other two tasks. The results showed no evidence of reduced performance for any of these tasks, when compared with performance of control subjects. The hypothesis that Korsakoff patients have a frontal-lobe dysfunction in addition to their amnesia needs some qualification because of these results: Frontal-lobe function specific to the ordering of verbal responses seems to be intact in Korsakoff patients.
The cognitive disruption in alcoholic Korsakoff patients is characterized by amnesia as well as some cognitive deficits, which seem to be independent of the memory deficits (Squire, 1982). These deficits include problems with the division of attention, perseveration of responses, deficits in shifting attention and susceptibility to interference (Oscar-Berman, 1984), and suggest that some damage to the frontal lobes has occurred (Moscovitch, 1982). This study is directed at possible frontal-lobe involvement in the alcoholic Korsakoff syndrome. In a previous study with frontal-lobe patients we used four tasks which all required short-term retention of numbers and which differed in the degree and type of the control processes involved. These tasks were digit span forward, missing scan, randomization span, and randomization span visual. The first requires recall of aurally presented sequences of digits. The second requires the detection of the missing number in a randomly arranged sequence,
* Correspondence and reprint requests should be addressed to Dr. Sjoerd Wiegersma, University of Utrecht, vakgroep Psychonomie, Heidelberglaan 2, Transitorium 2, De Uithof, 3508 CS Utrecht, the Netherlands. Accepted for publication: December 26, 1990.
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made up of all the numbers minus one, of a set of numbers (1-3, 1-4, etc.). The other two tasks require the random production of short sequences, to be made of sets of numbers (1-3, 1-4, etc.), with the restriction of not repeating the same digits nor using counting orders. The latter two tasks are called subjective ordering tasks and showed deficits in frontal-lobe patients, whereas the former two tasks showed almost intact performance when compared with control subjects (Wiegersma, van der Scheer, & Hijman, 1990). These results were explained by a deterioration in an active generation component of subjective ordering, while the short-term retention and comparison components were supposed to remain intact as shown by the intact performance at digit span forward and missing scan. Such results can be explained by a theoretical framework, in which a working memory is built up of a passive short-term retention component and an active control component, the latter being selectively deficient in frontal-lobe patients (Baddeley, 1986; Norman & Shallice, 1986). Since Korsakoff patients show so many signs of the frontal-lobe syndrome, it seemed worthwhile studying these patients with the same set of tasks. The short-term retention component is relatively intact in amnesia (e.g., Baddeley & Warrington, 1970). being somewhat lower than normal, but still within the normal range (Parkinson, 1982). Hence, if alcoholic Korsakoffs suffer from a frontal-lobe syndrome with relatively intact short-term retention, they should be selectively impaired in the subjective ordering tasks, with relatively unimpaired digit span. As to the missing scan, predictions are less clear. If memory comparison processes are involved in the disorder, performance on this task should be impaired. If only the response generation component of subjective ordering suffers from the disorder, then missing scan performance should remain intact in the patients.
METHOD Design The four experimental tasks mentioned above were presented to alcoholic Korsakoff patients and normal control subjects. The tasks were presented in a pseudo-random order, such that all four tasks occurred equally in each position. After completion of these four tasks, all subjects performed five Word Fluency tasks, also in random orders. These tasks were added. because they require the production of sequences as in the subjective ordering tasks, but are different from these in that they require retrieval from long-term memory. Since the subjective ordering tasks are supposed to be short-term memory tasks, Korsakoff patients who suffer from amnesia should be more severely impaired at the Word Fluency tasks than at the subjective ordering tasks. Subjects Sixteen Korsakoff patients of the ‘Neurologische en Orthopedische Kliniek Julianaoord’ at Laren, the Netherlands, participated.The diagnosis ‘Korsakoff Syndrome’ was established by using the following criteria. Intelligence was within the normal range, considering age and education (mean WAIS-IQ was 95.2; range 79-1 14). Deficits of long-term memory were measured with Rey’s Verbal Learning Test. Mean total recall score over five trials was 19.3 (range: 10-31; 11 patients scored in the f i i t decile of the normative distribution
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of healthy subjects). Mean delayed recall after 20 min was 1.0 (range 0-5), and mean delayed recognition was 9.8 (range 2-14). The frontal-lobe patients of the previous experiment (Wiegersma, van der Scheer, & Hijman, 1990) scored considerably higher on these measures: 37.0 for total recall, 7.8 for delayed recall, and 12.8 for delayed recognition. Rey (1964, pp. 150-151) gives normative values for healthy manual laborers for total recall (57.7) and delayed recognition (14.5). For the intellectual professions the norms are 61.6 and 14.9 respectively. The story of Binet-Bobertag showed a mean recall score of 9.1 (range 2-14). One subject, scoring high (14) at this test, was nevertheless admitted, since she was very low at all parts of Rey's Verbal Learning Test (total recall: 10; delayed recall: 1; delayed recognition: 2). All subjects showed alcohol abuse in the recent past. Cases caused by different etiology (tumour, trauma, etc.) were excluded. Sixteen control subjects were matched to the patients with respect to sex, age, and education. There were 10 women and six men in each group. Mean age was 53.6 years (range 33-67) for the patients and 54.6 years (range 37-67) for the controls. For the estimation of education we used a seven-point scale as presented by the Manual of the Groninger Intelligentie Test (Luteijn & Van der Ploeg, 1983). Median education was 4.0 (range 2-5) for Korsakoffs and 4.0 (range 2-6) for controls. Procedures All four experimental tasks involve short-term retention and make use of numbers. The tasks differ in the degree that control processes are required and in the type of control processes. One practice trial at level three was given in each task before testing started. There was one trial at each level as long as the subject was correct. In the case of failure, an additional trial at the same level was presented. Testing in all tasks was finished when the subject also failed at the second trial.
Digit span forward. Subsets of the numbers 1-12 were aurally presented at a rate of one number per second, for immediate recall by the subject. The first sequence consisted of three numbers, the second of four, etc. Free recall was allowed, in order to make the task more comparable to the other tasks (Buschke, 1963). There was one sequence for each level, except when an error was made. In that case, a second opportunity at the same level was given with a new sequence. The subject earned three points if the first level of three numbers was successfully completed, one additional point for each correct first trial at a higher level and 0.5 point if only a second trial was correct. If both trials of one level were wrong, testing was finished.
Missing
scan. Random sequences of n-1 numbers, randomly selected from sets of n numbers, were presented at a rate of one per second. Set size ( n ) was gradually increased from three (numbers 1-3). through four (numbers 1-4), etc., until the subject failed to mention the missing number. The set of possible numbers was given by oral instruction and visually presented to the subject on a card (in this way: 1-3 or 1-4, etc.) which remained visible to the subject until the trial was completed., Scoring was as for digit span.
Randomization span. Subjects had to select responses from sets of numbers (1-3,1-4, etc.) in a self-chosen ordering, with the restrictions of avoiding repetition and counting forward or backward. A randomly selected number to start with was provided by the experimenter. If the patient or control subject produced a sequence with three or more numbers in counting order forward (e.g., 5, 6 . 7 or 2, 3 and 5, 6) or four or more numbers backward (e.g., 1 0 , 9 , 8 , 7 ) an additional opportunity was given at the same level, after repetition of the instructions. If the subject failed in the second trial, a third opportunity was given at that level. This was done to make sure that failure in the patients was not due to forgetting the instructions. The set of numbers allowed remained visually available on a card (1 -3,
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1-4, etc.) during production of the sequence as in the missing item task. The rate of production was self-placed. Scoring was as for digit span and missing scan. Subjects got 0.5 point for a level where one of the added trials was correct.
Randomization span visual. This task is identical to the randomization task, except that all admitted alternatives are presented to the subject in a different visual arrangement. Vocal responses were required. A comparable task, but requiring pointing responses rather than vocal responses, has been used by Petrides and Milner (1982) and Wiegersma, van der Scheer, and Hijman (1990) in studying frontal-lobepatients. Vocal responses were preferred in the present study in order to minimize possible confounding with spatial factors. The subject selects one of n alternativenumbers (1-3. 1-4, etc.) from sheets of paper, while the
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experimenter turns them over at a rate determined by the speed of production of the subject. Instructions and scoring were as in the randomization task. Word-Fluency Tasks The subject produces as many words of a semantic category (animals or professions) or beginning with certain letters (M, S, or K) as possible in 1 minute for each of the five categories.
RESULTS The results at the experimental tasks are presented in Table 1. An analysis of variance with repeated measures over tasks showed that there was no significant effect of group (F < l), nor of the interaction of group and task (F c 1). Only the main effect of task showed statistical significance (F (3,90) = 33.12, p < .001). Neither age nor educational level showed significant product-moment correlations with any of the four experimental tasks. Although direct comparison of experiments is difficult because of small procedural differences, we also give the values of the frontal-lobe patients in Wiegersma, van der Scheer, and Hijman (1990): 5.4 (digit span), 8.7 (missing scan), 5.3 (randomization), and 4.9 (randomization visual). The frontal-lobe patients generally scored lower, but especially so on the subjective ordering tasks. The control subjects in the present experiment score lower on subjective ordering than those in the previous experiment, probably because they are older. An aging effect on subjective ordering has been shown by Wiegersma and Meertse (1990).
Table 1. Means (standard deviations) of the spans of alcoholic Korsakoff patients and normal controls for the four experimental tasks. DS = digit span, MS = missing scan, R = randomization span, R V = randomization span visual. Group Patients Controls
DS
MS
R
RV
6.0 (1.6) 6.0 (1.2)
9.4 (2.3) 9.8 (2.1)
6.6 (2.6) 6.8 (2.0)
5.9 (1.9) 6.1 (1.9)
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Table 2. Means (standard deviations) of Korsakoff patients and normal controls for the Word Fluency tasks. Group
Animals
Professions
M
S
K
Patients Controls
15.2 (3.7) 22.6 (5.4)
12.9 (4.9) 16.1 (5.4)
12.4 (5.3) 15.1 (5.9)
11.4 (4.5) 15.3 (4.6)
11.7 (4.3) 16.8 (6.1)
The results at the Word-Fluency tasks are presented in Table 2. There was a significant main effect of group ( F (1,30) =9.77, p < . O l ) and of task ( F (4,120) = 15.84, p < .OOl). The interaction effect of group and task was not significant.
DISCUSSION We did not find evidence in Korsakoff patients for the pattern of results found in frontal-lobe patients. The Korsakoffs perform at about the same level as controls in all four experimental tasks. The Korsakoffs only needed a few more trials in the subjective ordering tasks, since they more readily seemed to forget the instruction not to count than the controls, probably due to their amnesia. However, provided that they obey the instructions in this respect, they seem to be able to do all tasks at a normal level. Hence, Korsakoff patients show no evidence of being worse when control processes relevant to active sequential ordering are required. In that respect, they differ from patients with frontal-lobe lesions (Wiegersma, van der Scheer, & Hijman, 1990). How can these negative results with subjective ordering be explained? We would not like to suggest that the frontal-lobe syndrome is absent in Korsakoff patients, since it has been supported by a variety of tasks as well as anatomical evidence (Moscovitch, 1982; Oscar-Berman, 1984). Rather, it should be concluded that there is something special with the frontal-lobe syndrome of these patients, wherein subjective ordering is preserved while at the same time several other indicators show the characteristic decline. What is so special about subjective ordering as compared to other tasks which indicate frontal-lobe dysfunction? Subjective ordering has been analyzed in earlier studies by using so-called randomization tasks (Wiegersma, 1982, 1984). It requires short-term retention, comparison of probe responses with previous responses available in short-term memory and the generation of one of the responses not produced so far. The present study suggests that all of these are intact in Korsakoff patients as contrasted with frontal-lobe patients, where short-term retention and comparison appeared to be intact, while only the spontaneous generation component was defective. Hence, the frontal-lobe syndrome of Korsakoff patients is special in that the spontaneous generation component of subjective ordering is intact.
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At this point it is of interest to make a comparison to the fluency tasks, which showed deficient performance in Korsakoff patients in our study as well as previous ones (Butters, 1985; Butters, Granholm, Salmon, Grant, & Wolfe. 1987). Although this task also involves spontaneous generation of a sequence of responses, this differs in one important aspect from the subjective ordering task. In subjective ordering, the response is selected from the set of pre-activated items in short-term memory, such that retrieval from long-term memory is not required during task performance. In the fluency task, however, such retrieval is required. In other respects, both tasks are quite similar: both require the active production of a sequence of non-repetitions in a self-determined order. Hence, the critical difference probably is in the retrieval of words from long-term memory, which is defective in Korsakoff patients. In summary, considerable overlap has been shown between the memory disorders in alcoholic Korsakoff amnesia and frontal-lobe patients (Moscovitch, 1982). This leads to the question of whether the frontal-lobe disorder is to some degree fundamental to the amnesia in Korsakoff patients or not. On the other hand, a primary amnesia may constitute certain characteristics of the frontal executive syndrome. For example, problems with retrieval and recognition may be responsible for perseveration and lack of selectivity (Goldberg & Bilder, 1986). The overlap of the executive frontal syndrome and amnesia needs differentiation by tasks which show intact performance in one and deficient performance in the other disorder. Subjective ordering seems to be one such task. Future comparisons of frontal with Korsakoff patients, using planning and sequential production tasks which depend on short-term rather than long-term retention, should further delineate the frontal involvement in the cognitive disorder of Korsakoff patients. Such studies could clear up the question about the possible causal relationships between the executive syndrome and the amnesia of Korsakoff patients. For now, the possibility seems to remain, that at least some frontal symptoms of Korsakoff patients are not distinctive characteristics of a frontal syndrome, and may rather be the secondary characteristics of their amnesia.
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