BRAIN
AND
Different
LANGUAGE
6,
179-191 (1978)
Patterns
STEVEN Mantejiore
of Mnemonic Deficits Amnestic Syndromes MATTIS
AND RICHARD
in Two Organic
KOVNER
Hospital and Medical Center and the Albert Einstein College of Medicine AND ERICH
GOLDMEIER
Veterans Administration
Health Care Facility
A recall and recognition memory study of Korsakoff and post-herpes encephalitis patients employing percentage correct recall and the statistic d’ derived from signal detection theory supports Lhermitte’s contention that these two patient groups represent two distinct organic amnesia syndromes. Post-herpes encephalitis patients show little evidence of encoding and storage of information. In contrast recognition memory of Korsakoff and normal control subjects was essentially similar for truly novel information. Recognition memory for English words was markedly impaired for Korsakoff patients and worsened with increased semantic organization of the material. In light of our findings it would seem advisable to utilize homogeneous groups, with respect to brain pathology, when studying memory processes in organic patients.
While there is general agreement that amnesic patients demonstrate severely deficient recall of recent events there are significant differences among investigators as to which specific defects in the processing of information are causal to the memory disorder. These differences probably reflect the various methods employed to measure encoding, storage, and retrieval in addition to important variation in the composition of amnesic groups studied. Butters and his co-workers in a series of experiments investigating recall, recognition, and language versus nonlanguage processes in alcoholic Korsakoff patients conclude that the amnesic disorder primarily reflects distortion in the semantic encoding of information (Butters & Cermak, 1974; Cermak, Butters, & Moreines, 1974; Cermak & Butters, 1972). Warrington and colleagues report results for a mixed amnesic group (comprising patients with differing pathology and presumably different The authors thank Mr. Raymond Pass for his help in preparing the stimuli. Requests for reprints should be sent to Dr. Steven Mattis, Department of Neurology, Montefiore Hospital, Bronx, New York 10467. 179
0093-934x178/0062-0179$02.00/O Copyright 0 1978 by Academic Press, Inc. All rights of reproduction in any form reserved.
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MATTIS,
KOVNER,
AND GOLDMEIER
sites of effective lesions) consonant with the inference that amnesic patients suffer essentially from a disruption in self-directed retrieval, due to pronounced susceptibility to interference (Warrington & Weiskrantz, 1974). Mimer, in studies on large numbers of patients with surgical hippocampal lesions, has inferred a failure of consolidation to be the major factor in the amnesic syndrome (Milner, 1966). Although it is widely recognized that an amnesic syndrome is produced by lesions that focus on two topographically separate but interconnected brain areas, the medial diencephalon and hippocampus, there is no general agreement as to the functional significance of different lesion locations. Warrington and Weiskrantz (1974) observe that the memory performance of patients with medial temporal lobe (hippocampal) damage is comparable to that of patients with damage centering in mamillo-thalamic regions of the diencephalon and that “therefore one need not consider other possible differences among these classes of patients.” Conversely, Lhermitte and Signoret (1972) and Cermak (1976) note very significant differences in memory performance of patients with primary pathology in each area and conclude that the mammillo-thalamic-hippocampal circuit may not be a unitary system with regard to memory processes. The present study further investigates the possibility that different brain lesions may produce differing verbal memory deficits and attempts to elucidate which mnemonic subprocesses may be affected. Recognition and recall memory in a group of alcoholic Korsakoff patients with damage centering in the medial diencephalon (Victor, Adams, & Collins, 1971) is contrasted with post-herpes encephalitis patients whose residual lesions focus on medial temporal lobes (hippocampi) and orbital frontal cortex (Drachman & Adams, 1962). The study utilizes a verbal list learning paradigm that presents lists that vary as a function of the accessibility of the material to semantic encoding. The paradigm seeks to contrast the amount of material stored to that recalled by presenting intermittent memory probes between recall trials and attempts to maximize recall efficiency by providing a “boost” to those target items that are below recall threshold for a given trial. METHODS
Subjects Five amnesic patients were utilized as subjects, three alcoholic Korsakoff and two post-herpes encephalitis patients. Four of these reside at the Veterans Administration Health Care Facility, Montrose, New York, and the last, afemale post-encephalitis patient, resides at home and has been followed as an outpatient by the Neuropsychology Division at Montefiore Hospital and Medical Center for the last 4 years. All amnesic patients presented clinically with a stable, dense memory deficit which included disorientation in time and place, inability to recall daily personal or important current events, and some degree of retrograde amnesia. Five normal control group subjects were paid volunteers matched with the amnesic subjects
MNEMONIC
DEFICITS
181
for age, Full Scale WAIS IQ, and sex. The mean IQs and ages were 106 (range: 102 to 109) and 59 years (range: 57 to 60) for the post-herpes encephalitis group, 104 (range: 99 to 108) and 59 years (range: 5 1 to 68) for the alcoholic Korsakoff group, and 110 (range: 104 to 116) and 58 years (range: 53 to 64) for the normal control group. Immediate memory span, as estimated by the Digit-Span subtest of the WAIS, was above the mean for every amnesic subject and was comparable to that ofthe normal controls (mean scale score of 13 vs. mean scaled score of 12, respectively).
Design Two short-term verbal memory paradigms were used. The first consisted of modified free recall with recognition probes. Recall trials incorporated the device of selective reminding with extended recall (Buschke, 1973) which attempts to maximize performance both by expanding the time frame allowed for recall and by reminding the subject of list items below recall threshold on a given trial. The second paradigm employed a standard recognition memory design. Within each memory paradigm four types of 20-word learning lists were utilized, designed to differ in their accessibility to semantic encoding strategies; categorized and mixed English words, nonsense hexagrams, and Persian words. The categorized and mixed English word lists were derived from standardized compilations (Battig & Montague, 1969; Carroll, Davies, & Richman, 1971). For the categorized lists both the 20 target and 20 distractor items were selected from high, medium, and low frequency words within the same category. The mixed lists contained words each selected from a different category with target and distractor item pairs selected from the same category and matched for frequency within that category. The categorized and mixed English lists (target and distractor) were constructed so as to have the same range and mean word frequency. Each item on the nonsense lists was composed of two CVC trigrams with known association values to English words (Archer, 1960). The target and distractor items were matched for associative values of the trigrams, but the associative values ofthe resulting hexagrams are not known. Examples ofCVCCVC nonsense hexagrams are HUMROW and PUFMAX. The Persian word lists were composed of two-syllable words from an English-Persian reader. Examples of these words are BG-ZORG and TAH-ZEE. Each subject participated in the same eight learning tasks, i.e., 4 word lists x 2 recall paradigms. Two tests were given each day, separated by a I-hr lunch break, on 4 successive days. The order of list presentation was randomized for the experimental subjects. Each normal control subject was yoked to an amnesic subject and followed their sequence of learning conditions.
Procedure Modijied free recall with recognition probes paradigm. A 20-word target list was read to each subject at the rate of one word every 2 sec. To insure initial correct reception ofthe verbal stimuli the patient repeated each word on the “target” list as it was read, on the first trial only. After presentation ofthe whole list the subject was asked to recall it in any order and then was vigorously encouraged to continue his recall. At the point at which the subject gave up he was reminded of those list items he had missed on that trial. He was then asked to recall the entire list again, thus beginning the next trial. Each time a target word was recalled the subject was told he was correct. Ifthe subject intruded a word not on the target list he was told that it was incorrect. A recognition probe was inserted at three points during recall (on trials 4, 8, and 12), after the subject had exhausted his recall but before he had been reminded of the target words he had left out. He was then read a list of 40 words and was asked to respond “yes” or “no” as to whether each word in question belonged to the target list he was in the process ofleaming. The subject was immediately informed after each judgment whether or not he was correct. After
182
MATTIS,
KOVNER,
AND GOLDMEIER
completion of each recognition probe selective reminding was instituted for the recall trial completed just prior to that probe, thus beginning the next recall trial. Standard recognition paradigm. The subject was read a list of 20 words at the rate of one every 2 set and, again, repeated each word as it was read. This constituted presentation of the target or “original” list. Thereafter, the subject was read a list of 40 words half of which were target and half distractor items. After presentation of each item the subject was asked to make a “yes/no” decision as to whether or not the word belonged to the original target list and was immediately informed if he was correct or not. The same 40 words, in random order, were presented on each of 12 trials.
Data Tabulation An adjusted percentage correct measure was computed for each recall trial. Intrusions were noted and subtracted from the total number of target items correctly recalled, and this was then divided by the total number of target items. This correction was made for the English words only because it was observed that the Korsakoff group made a significant number of intrusions from the same category as the target items on the categorized list even before the distractor list had been presented on the first probe. By this correction we hoped to avoid confounding true recall of the target list with non-list-specific generation of items by category, a process which has been found to be intact in amnesic patients (Baddeley & Warrington, 1973). To obtain an unbiased measure of recognition memory performance the statistic d’, derived from signal detection theory, was computed for each recognition probe and trial. The utility of d’ is that it is not affected by changes in a subject’s response criteria. For this reason it has been shown to be a better measure of recognition memory performance (trace strength) than
Normal
Normal
Control
Post
Control
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Kormakoff
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4.0
30 ‘u 1
21)
c 11)
N.C. Categorized
K.
P.E. Words
N.C.
K. Mtxed
P.E. Words
FIG. 1. Mean group memory performance on categorized and mixed English word lists in terms of d’ and adjusted percentage correct recall averaged over three recall trials (4,8, and 12) or three recognition probes (1,2, and 3). The line that crosses the figure defines the point above which all d’ values differ significantly from chance at the .05 level and refers to d’ only.
MNEMONIC Normal
Normd
Control
COX.t-1
Korcuskoff
Koreakorf Post
183
DEFICITS
Poet
Enoephalltic
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too
4.0
'a ii Is ;
3.0 2.31
2.0
1.0
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P.E. Peraan
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I
FIG. 2. Mean group memory performance on nonsense hexagram and Persian word lists in terms ofd’ and percentage correct recall averaged over three recall trials (4,8, and 12) or three recognition probes (1,2, and 3). The line that crosses the figure defines the point above which all d’ values differ significantly from chance at the .05 level and refers to d’ only. percentage correct measures corrected for guessing (Banks, 1970). The d’ was computed from the proportion of “yes” responses to items that belonged to the original target list (hits) and the proportion of”yes” responses to items that belonged to the distractor list (false alarms). A d’ of 3.92 represents perfect performance in this design, i.e., 100% hits, 0% false alarms, whereas ad’ of 0 represents perfect guessing, i.e., an equal proportion of hits and false alarms. All statistical comparisons were made with one-tailed Mann-Whitney U tests (Siegel, 1956).
RESULTS
Recall with Recognition Probes Memory Paradigm Figures 1 and 2 present, simultaneously, both measures of memory performance utilized in the recall with recognition probes paradigm, i.e., percentage correct recall adjusted for intrusions (see procedure), and d’. The levels on each measure for each amnesic and normal control group represent averages of three recall trials, or three recognition probes introduced during recall, for each “word list” at comparable points in learning. The crossing line at d’ = 0.8, on each figure, defines a confidence limit above which any d’ represents better than chance discrimination between target and distractor items, at the .05 level (Marascuilo, 1970).
184
MATHS,
KOVNER,
AND GOLDMEIER
Korsakoff and control groups show above chance averaged’ levels on each list condition, while the post-encephalitis group’s averaged’ levels for each “word list” do not differ from chance. The post-encephalitis subjects, therefore, do not give evidence of any memory storage, as estimated by d’ , across all word lists. Considering recall it can be seen from the figures that the control group shows high recall for both English word lists but shows low level recall performance for the two “novel” word lists. Their respective overall recall percentages on categorized and mixed English words of 88 and 83% represent an average recall per trial of about 17 of the 20 target items. This is about 11 items above immediate memory span for this type of material (Hunter, 1973). The control group recall percentages of 22 and 19% for the nonsense hexagram and Persian word lists, respectively, represent an average recall level of about 4 of the 20 target items on a given trial. This is about one item above immediate span for this type of verbal stimulus (Hunter, 1973). In contrast, neither the Korsakoff nor postencephalitis groups display recall performance above immediate span for either real English words or “novel” verbal material. The direct TABLE
1
AVERAGEPERCENTAGECORRECTRECALLFORALLSTIMULION
TRIALS~,&AND
12
Average percentage correct Normal control
Korsakoff
Significance of group difference”
Categorized English word@ Trial 4 Trial 8 Trial 12
76 90 98
35 30 30
** ** **
Mixed Trial Trial Trial
67 a7 94
32 23 30
** ** **
Nonsense hexagrams Trial 4 Trial 8 Trial 12
13 24 31
3 8 8
NS * **
Persian Trial Trial Trial
14 17 26
8 10 10
NS NS NS
English word@ 4 8 12
words 4 8 12
a (*) p < .05; (**) p < .02; (NS) nonsignificant, p > .05. * Percentage correct adjusted for intrusions.
MNEMONIC
DEFICITS
TABLE
185
2
AVERAGE d’ FORALL STIMULIONALLRECOGNITION PROBES Average d’ Normal control
Korsakoff
Significance of group difference”
3.30 3.54 3.78
1.31 1.30 0.30
* ** **
Mixed English words Probe 1 Probe 2 Probe 3
3.60 3.73 3.86
2.17 2.55 1.44
** NS **
Nonsense hexagrams Probe 1 Probe 2 Probe 3
2.68 2.58 2.88
1.01 1.50 1.66
** NS NS
Persian Probe Probe Probe
2.20 2.11 2.61
1.44 1.54 1.27
NS NS **
Categorized English words Probe 1 Probe 2 Probe
3
words 1 2 3
n (*) p < .05; (**) p < .02; (NS) nonsignificant, p > .05.
comparison in Figs. 1 and 2 of both measures of memory performance shows that the d’ statistic sets the Korsakoff group apart from the post-encephalitis group whereas percentage correct recall does not. Table 1 presents the percentage recall of Korsakoff and normal subjects for the recall trial just preceding each recognition probe. Table 2 presents the average d’ score for Korsakoff and normals for each recognition probe. In comparing the d’ and percentage correct recall measures of memory performance it should be noted that significant storage, as demonstrated by robust d’ levels, is not necessarily reflected in recall. This is true for the Korsakoff group on every type of verbal stimulus utilized but is also true for the control group for the “novel” stimuli. Figure 3 presents the average d’ scores for each group on every recognition probe introduced within the recall memory task. An examination of the curves shows that the separation of the two amnesic groups is consistent across probes on all word lists. Korsakoff patients, compared with the controls, show impairment of recognition memory on probes presented during recall for both English word lists. Conversely, control and Korsakoff groups demonstrate essentially similar d’ performance for analogous probes on both nonsense hexagram and Persian word
186
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AND GOLDMEIER -
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FIG. 3. Mean group memory performance in terms ofd’ for each of three recognition probes for each stimulus type. The line that crosses each graph defines the point above which all d’ values differ significantly from chance at the .05 level and refers to d’ only.
lists. On the categorized word list, the Korsakoffs show lower d’ scores than controls on each comparable probe. On the mixed English word list the groups differ significantly on probes 1 and 3 but not on probe 2. On both English word lists controls either remained at their initial high d’ score or increased d’ from first to third probe, whereas Korsakoffs showed a decrement in d’ on probe 3 as compared with probe 1. Standard Recognition Memory Paradigm
On the first recognition trial (see Fig. 4) the Korsakoff group displays significantly impaired average d’ levels, compared with the control group, on both English word lists (U = 0, p < .02). For the nonsense hexagram and Persian word lists, however, both Korsakoff and control groups are above chance on the first trial and do not differ significantly from each other (U = 4.5, p > .20; and U = 1.8, p > .05). With the exception of one borderline d’ value on trial 10 of the Persian word list the Korsakoff group quickly falls below chance and stays there for the remainder of the 12 trials on all four word lists. In contrast, the averaged’ scores of the control group remain relatively stable compared with their initial levels throughout the 12 recognition trials on all word lists.
MNEMONIC
187
DEFICITS
Recognition Probes versus Recognition Trials
The major procedural difference between recognition probes and recognition trials is the ratio of presentation of target to distractor items before a subject is required to discriminate between them. Prior to each recognition probe the subject hears each target item, in the absence of distractor items, four consecutive times, either by his own correct production of it on a recall trial or by the examiner reminding him of it if he does not recall it. In contrast, on all 12 recognition trials the subject is confronted with all 20 distractor items interspersed with all 20 target items each time. At recognition trial 3 and recognition probe 3 all subjects have been presented with distractor items twice on both paradigms. At the same point each subject has been exposed to the target item 14 times on the recall with probes paradigm (12 times during recall trials and twice during recognition probes 1 and 2), in addition to being exposed to distractor items twice (during recognition probes 1 and 2). The comparable point in the standard recognition paradigm, in terms of the prior number of times distractor items were presented, is trial 3. By trial 3 the subjects have been exposed to the distractor items two times and, to the target items, three times. By comparing subjects’ performance on recognition trial 3 versus Normal
Control
-
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-
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FIG. 4. Mean group memory performance in terms ofd’ for each of 12 standard recognition trials for each stimulus type. The line that crosses each graph defines the point above which all d’ values differ significantly from chance at the .05 level and refers to d’ only.
188
MATTIS,
KOVNER,
AND GOLDMEIER
TABLE MEAN
d’ DIFFERENCE BETWEEN
3
SCORES AND STATISTICAL COMPARISONS CONTROL AND KORSAKOFF GROUPS
Normal control
Korsakoff
Average d’ Word list Categorized English Mixed English Nonsense hexagram Persian
Average d’
DifferProbe 3 Trial 3 ence 3.78 3.86 2.88 2.61
2.66 3.18 1.25 0.69
DifferProbe 3 Trial 3 ence
1.12 0.68 1.63 1.92
0.30 1.44 1.66 1.27
0.57 0.45 0.41 0.50
-0.27 0.99 1.25 0.77
Significance of group difference” ** NS NS NS
u (w) p < .02; (NS) nonsignificant, p > .05.
recognition probe 3 we can estimate the effect of additional target item presentations on recognition memory while holding the frequency of presentation of distractor items constant. For each subject the d’ obtained on recognition trial 3 was subtracted from the d’ value obtained on recognition probe 3 on each word list. The resulting distribution of d’ difference scores was analyzed for each word list separately. Table 3 presents the mean d’ difference scores and the statistical comparisons between the control and Korsakoff groups. For the mixed English, nonsense hexagram, and Persian word lists, both groups appear to have benefited similarly from repeated presentation of target items alone. That is, both groups displayed statistically indistinguishable increments in d’ on recognition probe 3 relative to recognition trial 3 on these word lists. On the categorized word list, in contrast, a significant difference is found between both groups. The controls show the same superiority on probe 3 compared with trial 3 that they demonstrate on the other lists. The Korsakoff group, however, does not show the same superiority ind’ on recognition probe 3 of the categorized list that they show in the other three list conditions. The distribution of difference scores on the categorized English word Iist for each group does not overlap. Korsakoff d’ differences (recognition probe 3 minus recognition trial 3) range from - .46 to . 11 whereas control group d’ differences range from .31 to 2.39. DISCUSSION
The observation that alcoholic Korsakoff patients can store considerable amounts of information while post-encephalitis patients show no significant memory processing beyond the awareness of immediate attention confirms the findings of Lhermitte and Signoret (1972) and extends them to verbal stimuli. The inability of the post-encephalitis
MNEMONIC
DEFICITS
189
subjects to store any of the widely varying types of verbal material utilized in this study, in comparison with their relatively normal competence in other cognitive skills such as concept manipulation (Lhermitte & Signoret, 1972; Cermak, 1976), allows characterization of their amnesic syndrome as a relatively isolated memory defect similar to that described for patients with extensive hippocampal lesions (Penfield & Milner, 1958). Since the lesions producing the post-encephalitis memory disorder are presumed to be mainly hippocampal (Drachman & Arbit, 1966), our results support the contention that these medial temporal lobe structures are crucially concerned with consolidation and may function as holding areas for new information from which more extensive, long-term encoding may proceed. Our data also allow some inferences about the nature of the Korsakoff memory defect. The strength of memory traces, as estimated by d’ scores, is predominantly comparable for Korsakoff and control groups on the novel word lists, strongly suggesting that, in the absence of any prior experience with agiven event, both groups process this “new” information in a similarly efficient manner. Thus, when the utility of previously stored material as an aid in coding and organizing target events is negligible, trace strength per se does not appear to be significantly impaired by the medial diencephalic lesions presumed present in the Korsakoff patient. It is when encountering a given event with which they have had prior experience, and for which they have established a network of associations, that the groups differ in their ability to utilize this network of associations to encode and store the event effectively. When one considers that the real English word lists are more familiar and of higher frequency of usage than the nonsense hexagrams and Persian lists these findings appear similar to those obtained by Huppert and Piercy (1976), who found recognition memory in Korsakoff patients for “familiar” stimuli and high frequency words inferior to their retention of “unfamiliar” stimuli and low frequency words. In their study, sets of target and distractor items were selected from a pool of stimuli to which there had been prior controlled exposure. The Korsakoff group had particular difficulty discriminating between such items. They apparently recognized both sets as having been previously experienced but were unable to establish a new context for the equally “familiar” stimuli. The authors suggested, therefore, that “the primary defect in amnesia may concern contextual memory rather than memory for items as such.” (Huppert & Piercy, 1976, p. 20). However, postulating a disorder in contextual memory as the primary defect does not fully account for our data. In our study all lists presenting real English words (categorized or mixed, target and distractor) were matched for range and mean frequency of usage. All real word lists were therefore presumed to be equally familiar prior to presentation and the contextual parameters were procedurally identical for all lists. Yet the Korsakoff patients demonstrated greater
190
MAlTIS,
KOVNER,
AND
GOLDMEIER
impairment relative to controls in recognition memory on the categorized as compared to the mixed English word list. Considering both the novel and English word lists, our findings indicate that, when prior familiarity is equal for both groups, the Korsakoff patients demonstrate a relative decrease in d’ as compared to controls as the intrinsic semantic organization of the word list increases. This supports the position of Butters and colleagues who have emphasized the role of defective semantic encoding in the Korsakoff amnesia. Our data also lead to the speculation that for the Korsakoff patient presentation of a familiar item may stimulate not only the target item in long-term storage but also its strong associates, and repeated presentation increases trace strength of both the target item and its associates by constant amounts. Thus, initially trace strength of the target item is proportionally greater than that of its associates so that the target is discriminable. Successive presentation over recall trials results in increased trace strength for both target and its associates. Assuming that trace strength has an upper limit, eventually target and distractor items would fall below the just noticeable difference necessary for discrimination. This speculation would account for the Korsakoff’s better recognition memory for the mixed as compared to the categorized list and for the decline across probes on both lists. The finding that development of interference during recognition memory performance in Korsakoff patients is heavily dependent on verbal stimulus type and design of the memory task makes attempts to explain this amnesic syndrome in terms of generalized interference phenomena tenuous. Overall, the present data suggest that Korsakoff patients evidence a basic disturbance in the relationship between items in their semantic associational network, an inability to construct efficient programs for entering the network in sequence (only at specific points), or both. Although it is recognized that the small samples of amnesic patients utilized in this study may not be entirely representative of either pathological type and that there may be some degree of overlap in lesioned brain areas across the two syndromes (Victor et al., 1971), it is significant that our data lend support to the possibility that differing brain lesions may produce behaviorally differentiable memory defects. Until this possibility is further clarified it would seem advisable to utilize homogeneous amnesic groups, with respect to brain pathology, when studying memory functions in organic populations. REFERENCES Archer,
E. J. 1960. Reevaluations Psychological
Monographs,
of the meaningfulness of all possible cvc trigrams. 74, I-23.
Baddeley, A. D., & Warrington, E. K. 1973. Memory coding in amnesia. Neuropsychologia, 11, 159-165.
MNEMONIC
DEFICITS
Banks, W. P. 1970. Signal detection theory and human memory. Psychological
191 Bulletin,
74,
81-99.
Battig, W. F., & Montague, W. W. 1969. Category norms for verbal items in fifty-six categories. Journal of Experimental Psychology Monographs, 80, l-46. Buschke, H. 1973. Selective reminding for analysis of memory and learning. Journal of Verbal Learning and Verbal Behavior, 12, 543-550. Butters, N., & Cermak, L. S. 1974. The role of cognitive factors in the memory disorders of alcoholic patients with the Korsakoff syndrome. Annals of the New York Academy of Sciences, 233, 61-75. Carroll, J. B., Davies, P., & Richman, L. 1971. The American heritage wordfrequency book. Boston: Houghton-Mifflin, Cermak, L. S. 1976. The encoding capacity of a patient with amnesia due to encephalitis. Neuropsychologia, 14, 311-326. Cermak, L. S., & Butters, N. 1972. The role of interference and encoding in the short-term memory deficits of Korsakoff patients. Neuropsychologia, 10, 89-96. Cermak, L. S., Butters, N., & Moreines, J. 1974. Some analyses ofthe verbal encoding deficit of alcoholic Korsakoff patients. Brain and Language, 1, 141- 150. Drachman, D. A., & Adams, R. D. 1962. Acute herpes simplex and inclusion body encephalitis. Archives of Neurology, 7, 45-63. Drachman, D. A., & Arbit, J. 1966. Memory and the hippocampal complex. Archives of Neurology, 15, 52-62. Hunter, I. M. L. 1973. Memory. Baltimore: Penguin Books. Huppert, F. A., & Piercy, M. 1976. Recognition memory in amnesic patients: Effect of temporal context and familiarity of material. Cortex, 12, 3-20. Lhermitte, F., & Signoret, J. L. 1972. Analyse neuropsychologique et differentiation des syndromes amnesiques. Revue Neurologique, 126, 161-178. Marascuilo, L. A. 1970. Extension of the significance test for one-parameter signal detection hypotheses. Psychometrika, 35, 237-243. Mimer, B. 1966. Amnesia following operation on the temporal lobes. In C. W. M. Whitty & 0. L. Zangwill (Eds.), Amnesia. London: Butterworth. Penfield, W., & Milner, B. 1958. Memory deficit produced by bilateral lesions in the hippocampal zone. Archives of Neurology and Psychiatry, 79, 475-497. Siegel, S. 1956. Nonparametric methods for the behaviorul sciences. New York: McGraw-Hill. Victor, M., Adams, R. D., & Collins, G. H. 1971. The Wernicke-Korsakoff syndrome. Philadelphia: F. A. Davis. Warrington, E. K., & Weiskrantz, L. 1974. The effect of prior learning on subsequent retention in amnesic patients. Neuropsychologia, 12, 419-428.
AND
Different
LANGUAGE
6,
179-191 (1978)
Patterns
STEVEN Mantejiore
of Mnemonic Deficits Amnestic Syndromes MATTIS
AND RICHARD
in Two Organic
KOVNER
Hospital and Medical Center and the Albert Einstein College of Medicine AND ERICH
GOLDMEIER
Veterans Administration
Health Care Facility
A recall and recognition memory study of Korsakoff and post-herpes encephalitis patients employing percentage correct recall and the statistic d’ derived from signal detection theory supports Lhermitte’s contention that these two patient groups represent two distinct organic amnesia syndromes. Post-herpes encephalitis patients show little evidence of encoding and storage of information. In contrast recognition memory of Korsakoff and normal control subjects was essentially similar for truly novel information. Recognition memory for English words was markedly impaired for Korsakoff patients and worsened with increased semantic organization of the material. In light of our findings it would seem advisable to utilize homogeneous groups, with respect to brain pathology, when studying memory processes in organic patients.
While there is general agreement that amnesic patients demonstrate severely deficient recall of recent events there are significant differences among investigators as to which specific defects in the processing of information are causal to the memory disorder. These differences probably reflect the various methods employed to measure encoding, storage, and retrieval in addition to important variation in the composition of amnesic groups studied. Butters and his co-workers in a series of experiments investigating recall, recognition, and language versus nonlanguage processes in alcoholic Korsakoff patients conclude that the amnesic disorder primarily reflects distortion in the semantic encoding of information (Butters & Cermak, 1974; Cermak, Butters, & Moreines, 1974; Cermak & Butters, 1972). Warrington and colleagues report results for a mixed amnesic group (comprising patients with differing pathology and presumably different The authors thank Mr. Raymond Pass for his help in preparing the stimuli. Requests for reprints should be sent to Dr. Steven Mattis, Department of Neurology, Montefiore Hospital, Bronx, New York 10467. 179
0093-934x178/0062-0179$02.00/O Copyright 0 1978 by Academic Press, Inc. All rights of reproduction in any form reserved.
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sites of effective lesions) consonant with the inference that amnesic patients suffer essentially from a disruption in self-directed retrieval, due to pronounced susceptibility to interference (Warrington & Weiskrantz, 1974). Mimer, in studies on large numbers of patients with surgical hippocampal lesions, has inferred a failure of consolidation to be the major factor in the amnesic syndrome (Milner, 1966). Although it is widely recognized that an amnesic syndrome is produced by lesions that focus on two topographically separate but interconnected brain areas, the medial diencephalon and hippocampus, there is no general agreement as to the functional significance of different lesion locations. Warrington and Weiskrantz (1974) observe that the memory performance of patients with medial temporal lobe (hippocampal) damage is comparable to that of patients with damage centering in mamillo-thalamic regions of the diencephalon and that “therefore one need not consider other possible differences among these classes of patients.” Conversely, Lhermitte and Signoret (1972) and Cermak (1976) note very significant differences in memory performance of patients with primary pathology in each area and conclude that the mammillo-thalamic-hippocampal circuit may not be a unitary system with regard to memory processes. The present study further investigates the possibility that different brain lesions may produce differing verbal memory deficits and attempts to elucidate which mnemonic subprocesses may be affected. Recognition and recall memory in a group of alcoholic Korsakoff patients with damage centering in the medial diencephalon (Victor, Adams, & Collins, 1971) is contrasted with post-herpes encephalitis patients whose residual lesions focus on medial temporal lobes (hippocampi) and orbital frontal cortex (Drachman & Adams, 1962). The study utilizes a verbal list learning paradigm that presents lists that vary as a function of the accessibility of the material to semantic encoding. The paradigm seeks to contrast the amount of material stored to that recalled by presenting intermittent memory probes between recall trials and attempts to maximize recall efficiency by providing a “boost” to those target items that are below recall threshold for a given trial. METHODS
Subjects Five amnesic patients were utilized as subjects, three alcoholic Korsakoff and two post-herpes encephalitis patients. Four of these reside at the Veterans Administration Health Care Facility, Montrose, New York, and the last, afemale post-encephalitis patient, resides at home and has been followed as an outpatient by the Neuropsychology Division at Montefiore Hospital and Medical Center for the last 4 years. All amnesic patients presented clinically with a stable, dense memory deficit which included disorientation in time and place, inability to recall daily personal or important current events, and some degree of retrograde amnesia. Five normal control group subjects were paid volunteers matched with the amnesic subjects
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for age, Full Scale WAIS IQ, and sex. The mean IQs and ages were 106 (range: 102 to 109) and 59 years (range: 57 to 60) for the post-herpes encephalitis group, 104 (range: 99 to 108) and 59 years (range: 5 1 to 68) for the alcoholic Korsakoff group, and 110 (range: 104 to 116) and 58 years (range: 53 to 64) for the normal control group. Immediate memory span, as estimated by the Digit-Span subtest of the WAIS, was above the mean for every amnesic subject and was comparable to that ofthe normal controls (mean scale score of 13 vs. mean scaled score of 12, respectively).
Design Two short-term verbal memory paradigms were used. The first consisted of modified free recall with recognition probes. Recall trials incorporated the device of selective reminding with extended recall (Buschke, 1973) which attempts to maximize performance both by expanding the time frame allowed for recall and by reminding the subject of list items below recall threshold on a given trial. The second paradigm employed a standard recognition memory design. Within each memory paradigm four types of 20-word learning lists were utilized, designed to differ in their accessibility to semantic encoding strategies; categorized and mixed English words, nonsense hexagrams, and Persian words. The categorized and mixed English word lists were derived from standardized compilations (Battig & Montague, 1969; Carroll, Davies, & Richman, 1971). For the categorized lists both the 20 target and 20 distractor items were selected from high, medium, and low frequency words within the same category. The mixed lists contained words each selected from a different category with target and distractor item pairs selected from the same category and matched for frequency within that category. The categorized and mixed English lists (target and distractor) were constructed so as to have the same range and mean word frequency. Each item on the nonsense lists was composed of two CVC trigrams with known association values to English words (Archer, 1960). The target and distractor items were matched for associative values of the trigrams, but the associative values ofthe resulting hexagrams are not known. Examples ofCVCCVC nonsense hexagrams are HUMROW and PUFMAX. The Persian word lists were composed of two-syllable words from an English-Persian reader. Examples of these words are BG-ZORG and TAH-ZEE. Each subject participated in the same eight learning tasks, i.e., 4 word lists x 2 recall paradigms. Two tests were given each day, separated by a I-hr lunch break, on 4 successive days. The order of list presentation was randomized for the experimental subjects. Each normal control subject was yoked to an amnesic subject and followed their sequence of learning conditions.
Procedure Modijied free recall with recognition probes paradigm. A 20-word target list was read to each subject at the rate of one word every 2 sec. To insure initial correct reception ofthe verbal stimuli the patient repeated each word on the “target” list as it was read, on the first trial only. After presentation ofthe whole list the subject was asked to recall it in any order and then was vigorously encouraged to continue his recall. At the point at which the subject gave up he was reminded of those list items he had missed on that trial. He was then asked to recall the entire list again, thus beginning the next trial. Each time a target word was recalled the subject was told he was correct. Ifthe subject intruded a word not on the target list he was told that it was incorrect. A recognition probe was inserted at three points during recall (on trials 4, 8, and 12), after the subject had exhausted his recall but before he had been reminded of the target words he had left out. He was then read a list of 40 words and was asked to respond “yes” or “no” as to whether each word in question belonged to the target list he was in the process ofleaming. The subject was immediately informed after each judgment whether or not he was correct. After
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completion of each recognition probe selective reminding was instituted for the recall trial completed just prior to that probe, thus beginning the next recall trial. Standard recognition paradigm. The subject was read a list of 20 words at the rate of one every 2 set and, again, repeated each word as it was read. This constituted presentation of the target or “original” list. Thereafter, the subject was read a list of 40 words half of which were target and half distractor items. After presentation of each item the subject was asked to make a “yes/no” decision as to whether or not the word belonged to the original target list and was immediately informed if he was correct or not. The same 40 words, in random order, were presented on each of 12 trials.
Data Tabulation An adjusted percentage correct measure was computed for each recall trial. Intrusions were noted and subtracted from the total number of target items correctly recalled, and this was then divided by the total number of target items. This correction was made for the English words only because it was observed that the Korsakoff group made a significant number of intrusions from the same category as the target items on the categorized list even before the distractor list had been presented on the first probe. By this correction we hoped to avoid confounding true recall of the target list with non-list-specific generation of items by category, a process which has been found to be intact in amnesic patients (Baddeley & Warrington, 1973). To obtain an unbiased measure of recognition memory performance the statistic d’, derived from signal detection theory, was computed for each recognition probe and trial. The utility of d’ is that it is not affected by changes in a subject’s response criteria. For this reason it has been shown to be a better measure of recognition memory performance (trace strength) than
Normal
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FIG. 1. Mean group memory performance on categorized and mixed English word lists in terms of d’ and adjusted percentage correct recall averaged over three recall trials (4,8, and 12) or three recognition probes (1,2, and 3). The line that crosses the figure defines the point above which all d’ values differ significantly from chance at the .05 level and refers to d’ only.
MNEMONIC Normal
Normd
Control
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Korcuskoff
Koreakorf Post
183
DEFICITS
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FIG. 2. Mean group memory performance on nonsense hexagram and Persian word lists in terms ofd’ and percentage correct recall averaged over three recall trials (4,8, and 12) or three recognition probes (1,2, and 3). The line that crosses the figure defines the point above which all d’ values differ significantly from chance at the .05 level and refers to d’ only. percentage correct measures corrected for guessing (Banks, 1970). The d’ was computed from the proportion of “yes” responses to items that belonged to the original target list (hits) and the proportion of”yes” responses to items that belonged to the distractor list (false alarms). A d’ of 3.92 represents perfect performance in this design, i.e., 100% hits, 0% false alarms, whereas ad’ of 0 represents perfect guessing, i.e., an equal proportion of hits and false alarms. All statistical comparisons were made with one-tailed Mann-Whitney U tests (Siegel, 1956).
RESULTS
Recall with Recognition Probes Memory Paradigm Figures 1 and 2 present, simultaneously, both measures of memory performance utilized in the recall with recognition probes paradigm, i.e., percentage correct recall adjusted for intrusions (see procedure), and d’. The levels on each measure for each amnesic and normal control group represent averages of three recall trials, or three recognition probes introduced during recall, for each “word list” at comparable points in learning. The crossing line at d’ = 0.8, on each figure, defines a confidence limit above which any d’ represents better than chance discrimination between target and distractor items, at the .05 level (Marascuilo, 1970).
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Korsakoff and control groups show above chance averaged’ levels on each list condition, while the post-encephalitis group’s averaged’ levels for each “word list” do not differ from chance. The post-encephalitis subjects, therefore, do not give evidence of any memory storage, as estimated by d’ , across all word lists. Considering recall it can be seen from the figures that the control group shows high recall for both English word lists but shows low level recall performance for the two “novel” word lists. Their respective overall recall percentages on categorized and mixed English words of 88 and 83% represent an average recall per trial of about 17 of the 20 target items. This is about 11 items above immediate memory span for this type of material (Hunter, 1973). The control group recall percentages of 22 and 19% for the nonsense hexagram and Persian word lists, respectively, represent an average recall level of about 4 of the 20 target items on a given trial. This is about one item above immediate span for this type of verbal stimulus (Hunter, 1973). In contrast, neither the Korsakoff nor postencephalitis groups display recall performance above immediate span for either real English words or “novel” verbal material. The direct TABLE
1
AVERAGEPERCENTAGECORRECTRECALLFORALLSTIMULION
TRIALS~,&AND
12
Average percentage correct Normal control
Korsakoff
Significance of group difference”
Categorized English word@ Trial 4 Trial 8 Trial 12
76 90 98
35 30 30
** ** **
Mixed Trial Trial Trial
67 a7 94
32 23 30
** ** **
Nonsense hexagrams Trial 4 Trial 8 Trial 12
13 24 31
3 8 8
NS * **
Persian Trial Trial Trial
14 17 26
8 10 10
NS NS NS
English word@ 4 8 12
words 4 8 12
a (*) p < .05; (**) p < .02; (NS) nonsignificant, p > .05. * Percentage correct adjusted for intrusions.
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DEFICITS
TABLE
185
2
AVERAGE d’ FORALL STIMULIONALLRECOGNITION PROBES Average d’ Normal control
Korsakoff
Significance of group difference”
3.30 3.54 3.78
1.31 1.30 0.30
* ** **
Mixed English words Probe 1 Probe 2 Probe 3
3.60 3.73 3.86
2.17 2.55 1.44
** NS **
Nonsense hexagrams Probe 1 Probe 2 Probe 3
2.68 2.58 2.88
1.01 1.50 1.66
** NS NS
Persian Probe Probe Probe
2.20 2.11 2.61
1.44 1.54 1.27
NS NS **
Categorized English words Probe 1 Probe 2 Probe
3
words 1 2 3
n (*) p < .05; (**) p < .02; (NS) nonsignificant, p > .05.
comparison in Figs. 1 and 2 of both measures of memory performance shows that the d’ statistic sets the Korsakoff group apart from the post-encephalitis group whereas percentage correct recall does not. Table 1 presents the percentage recall of Korsakoff and normal subjects for the recall trial just preceding each recognition probe. Table 2 presents the average d’ score for Korsakoff and normals for each recognition probe. In comparing the d’ and percentage correct recall measures of memory performance it should be noted that significant storage, as demonstrated by robust d’ levels, is not necessarily reflected in recall. This is true for the Korsakoff group on every type of verbal stimulus utilized but is also true for the control group for the “novel” stimuli. Figure 3 presents the average d’ scores for each group on every recognition probe introduced within the recall memory task. An examination of the curves shows that the separation of the two amnesic groups is consistent across probes on all word lists. Korsakoff patients, compared with the controls, show impairment of recognition memory on probes presented during recall for both English word lists. Conversely, control and Korsakoff groups demonstrate essentially similar d’ performance for analogous probes on both nonsense hexagram and Persian word
186
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FIG. 3. Mean group memory performance in terms ofd’ for each of three recognition probes for each stimulus type. The line that crosses each graph defines the point above which all d’ values differ significantly from chance at the .05 level and refers to d’ only.
lists. On the categorized word list, the Korsakoffs show lower d’ scores than controls on each comparable probe. On the mixed English word list the groups differ significantly on probes 1 and 3 but not on probe 2. On both English word lists controls either remained at their initial high d’ score or increased d’ from first to third probe, whereas Korsakoffs showed a decrement in d’ on probe 3 as compared with probe 1. Standard Recognition Memory Paradigm
On the first recognition trial (see Fig. 4) the Korsakoff group displays significantly impaired average d’ levels, compared with the control group, on both English word lists (U = 0, p < .02). For the nonsense hexagram and Persian word lists, however, both Korsakoff and control groups are above chance on the first trial and do not differ significantly from each other (U = 4.5, p > .20; and U = 1.8, p > .05). With the exception of one borderline d’ value on trial 10 of the Persian word list the Korsakoff group quickly falls below chance and stays there for the remainder of the 12 trials on all four word lists. In contrast, the averaged’ scores of the control group remain relatively stable compared with their initial levels throughout the 12 recognition trials on all word lists.
MNEMONIC
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DEFICITS
Recognition Probes versus Recognition Trials
The major procedural difference between recognition probes and recognition trials is the ratio of presentation of target to distractor items before a subject is required to discriminate between them. Prior to each recognition probe the subject hears each target item, in the absence of distractor items, four consecutive times, either by his own correct production of it on a recall trial or by the examiner reminding him of it if he does not recall it. In contrast, on all 12 recognition trials the subject is confronted with all 20 distractor items interspersed with all 20 target items each time. At recognition trial 3 and recognition probe 3 all subjects have been presented with distractor items twice on both paradigms. At the same point each subject has been exposed to the target item 14 times on the recall with probes paradigm (12 times during recall trials and twice during recognition probes 1 and 2), in addition to being exposed to distractor items twice (during recognition probes 1 and 2). The comparable point in the standard recognition paradigm, in terms of the prior number of times distractor items were presented, is trial 3. By trial 3 the subjects have been exposed to the distractor items two times and, to the target items, three times. By comparing subjects’ performance on recognition trial 3 versus Normal
Control
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FIG. 4. Mean group memory performance in terms ofd’ for each of 12 standard recognition trials for each stimulus type. The line that crosses each graph defines the point above which all d’ values differ significantly from chance at the .05 level and refers to d’ only.
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MATTIS,
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AND GOLDMEIER
TABLE MEAN
d’ DIFFERENCE BETWEEN
3
SCORES AND STATISTICAL COMPARISONS CONTROL AND KORSAKOFF GROUPS
Normal control
Korsakoff
Average d’ Word list Categorized English Mixed English Nonsense hexagram Persian
Average d’
DifferProbe 3 Trial 3 ence 3.78 3.86 2.88 2.61
2.66 3.18 1.25 0.69
DifferProbe 3 Trial 3 ence
1.12 0.68 1.63 1.92
0.30 1.44 1.66 1.27
0.57 0.45 0.41 0.50
-0.27 0.99 1.25 0.77
Significance of group difference” ** NS NS NS
u (w) p < .02; (NS) nonsignificant, p > .05.
recognition probe 3 we can estimate the effect of additional target item presentations on recognition memory while holding the frequency of presentation of distractor items constant. For each subject the d’ obtained on recognition trial 3 was subtracted from the d’ value obtained on recognition probe 3 on each word list. The resulting distribution of d’ difference scores was analyzed for each word list separately. Table 3 presents the mean d’ difference scores and the statistical comparisons between the control and Korsakoff groups. For the mixed English, nonsense hexagram, and Persian word lists, both groups appear to have benefited similarly from repeated presentation of target items alone. That is, both groups displayed statistically indistinguishable increments in d’ on recognition probe 3 relative to recognition trial 3 on these word lists. On the categorized word list, in contrast, a significant difference is found between both groups. The controls show the same superiority on probe 3 compared with trial 3 that they demonstrate on the other lists. The Korsakoff group, however, does not show the same superiority ind’ on recognition probe 3 of the categorized list that they show in the other three list conditions. The distribution of difference scores on the categorized English word Iist for each group does not overlap. Korsakoff d’ differences (recognition probe 3 minus recognition trial 3) range from - .46 to . 11 whereas control group d’ differences range from .31 to 2.39. DISCUSSION
The observation that alcoholic Korsakoff patients can store considerable amounts of information while post-encephalitis patients show no significant memory processing beyond the awareness of immediate attention confirms the findings of Lhermitte and Signoret (1972) and extends them to verbal stimuli. The inability of the post-encephalitis
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subjects to store any of the widely varying types of verbal material utilized in this study, in comparison with their relatively normal competence in other cognitive skills such as concept manipulation (Lhermitte & Signoret, 1972; Cermak, 1976), allows characterization of their amnesic syndrome as a relatively isolated memory defect similar to that described for patients with extensive hippocampal lesions (Penfield & Milner, 1958). Since the lesions producing the post-encephalitis memory disorder are presumed to be mainly hippocampal (Drachman & Arbit, 1966), our results support the contention that these medial temporal lobe structures are crucially concerned with consolidation and may function as holding areas for new information from which more extensive, long-term encoding may proceed. Our data also allow some inferences about the nature of the Korsakoff memory defect. The strength of memory traces, as estimated by d’ scores, is predominantly comparable for Korsakoff and control groups on the novel word lists, strongly suggesting that, in the absence of any prior experience with agiven event, both groups process this “new” information in a similarly efficient manner. Thus, when the utility of previously stored material as an aid in coding and organizing target events is negligible, trace strength per se does not appear to be significantly impaired by the medial diencephalic lesions presumed present in the Korsakoff patient. It is when encountering a given event with which they have had prior experience, and for which they have established a network of associations, that the groups differ in their ability to utilize this network of associations to encode and store the event effectively. When one considers that the real English word lists are more familiar and of higher frequency of usage than the nonsense hexagrams and Persian lists these findings appear similar to those obtained by Huppert and Piercy (1976), who found recognition memory in Korsakoff patients for “familiar” stimuli and high frequency words inferior to their retention of “unfamiliar” stimuli and low frequency words. In their study, sets of target and distractor items were selected from a pool of stimuli to which there had been prior controlled exposure. The Korsakoff group had particular difficulty discriminating between such items. They apparently recognized both sets as having been previously experienced but were unable to establish a new context for the equally “familiar” stimuli. The authors suggested, therefore, that “the primary defect in amnesia may concern contextual memory rather than memory for items as such.” (Huppert & Piercy, 1976, p. 20). However, postulating a disorder in contextual memory as the primary defect does not fully account for our data. In our study all lists presenting real English words (categorized or mixed, target and distractor) were matched for range and mean frequency of usage. All real word lists were therefore presumed to be equally familiar prior to presentation and the contextual parameters were procedurally identical for all lists. Yet the Korsakoff patients demonstrated greater
190
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KOVNER,
AND
GOLDMEIER
impairment relative to controls in recognition memory on the categorized as compared to the mixed English word list. Considering both the novel and English word lists, our findings indicate that, when prior familiarity is equal for both groups, the Korsakoff patients demonstrate a relative decrease in d’ as compared to controls as the intrinsic semantic organization of the word list increases. This supports the position of Butters and colleagues who have emphasized the role of defective semantic encoding in the Korsakoff amnesia. Our data also lead to the speculation that for the Korsakoff patient presentation of a familiar item may stimulate not only the target item in long-term storage but also its strong associates, and repeated presentation increases trace strength of both the target item and its associates by constant amounts. Thus, initially trace strength of the target item is proportionally greater than that of its associates so that the target is discriminable. Successive presentation over recall trials results in increased trace strength for both target and its associates. Assuming that trace strength has an upper limit, eventually target and distractor items would fall below the just noticeable difference necessary for discrimination. This speculation would account for the Korsakoff’s better recognition memory for the mixed as compared to the categorized list and for the decline across probes on both lists. The finding that development of interference during recognition memory performance in Korsakoff patients is heavily dependent on verbal stimulus type and design of the memory task makes attempts to explain this amnesic syndrome in terms of generalized interference phenomena tenuous. Overall, the present data suggest that Korsakoff patients evidence a basic disturbance in the relationship between items in their semantic associational network, an inability to construct efficient programs for entering the network in sequence (only at specific points), or both. Although it is recognized that the small samples of amnesic patients utilized in this study may not be entirely representative of either pathological type and that there may be some degree of overlap in lesioned brain areas across the two syndromes (Victor et al., 1971), it is significant that our data lend support to the possibility that differing brain lesions may produce behaviorally differentiable memory defects. Until this possibility is further clarified it would seem advisable to utilize homogeneous amnesic groups, with respect to brain pathology, when studying memory functions in organic populations. REFERENCES Archer,
E. J. 1960. Reevaluations Psychological
Monographs,
of the meaningfulness of all possible cvc trigrams. 74, I-23.
Baddeley, A. D., & Warrington, E. K. 1973. Memory coding in amnesia. Neuropsychologia, 11, 159-165.
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Banks, W. P. 1970. Signal detection theory and human memory. Psychological
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Battig, W. F., & Montague, W. W. 1969. Category norms for verbal items in fifty-six categories. Journal of Experimental Psychology Monographs, 80, l-46. Buschke, H. 1973. Selective reminding for analysis of memory and learning. Journal of Verbal Learning and Verbal Behavior, 12, 543-550. Butters, N., & Cermak, L. S. 1974. The role of cognitive factors in the memory disorders of alcoholic patients with the Korsakoff syndrome. Annals of the New York Academy of Sciences, 233, 61-75. Carroll, J. B., Davies, P., & Richman, L. 1971. The American heritage wordfrequency book. Boston: Houghton-Mifflin, Cermak, L. S. 1976. The encoding capacity of a patient with amnesia due to encephalitis. Neuropsychologia, 14, 311-326. Cermak, L. S., & Butters, N. 1972. The role of interference and encoding in the short-term memory deficits of Korsakoff patients. Neuropsychologia, 10, 89-96. Cermak, L. S., Butters, N., & Moreines, J. 1974. Some analyses ofthe verbal encoding deficit of alcoholic Korsakoff patients. Brain and Language, 1, 141- 150. Drachman, D. A., & Adams, R. D. 1962. Acute herpes simplex and inclusion body encephalitis. Archives of Neurology, 7, 45-63. Drachman, D. A., & Arbit, J. 1966. Memory and the hippocampal complex. Archives of Neurology, 15, 52-62. Hunter, I. M. L. 1973. Memory. Baltimore: Penguin Books. Huppert, F. A., & Piercy, M. 1976. Recognition memory in amnesic patients: Effect of temporal context and familiarity of material. Cortex, 12, 3-20. Lhermitte, F., & Signoret, J. L. 1972. Analyse neuropsychologique et differentiation des syndromes amnesiques. Revue Neurologique, 126, 161-178. Marascuilo, L. A. 1970. Extension of the significance test for one-parameter signal detection hypotheses. Psychometrika, 35, 237-243. Mimer, B. 1966. Amnesia following operation on the temporal lobes. In C. W. M. Whitty & 0. L. Zangwill (Eds.), Amnesia. London: Butterworth. Penfield, W., & Milner, B. 1958. Memory deficit produced by bilateral lesions in the hippocampal zone. Archives of Neurology and Psychiatry, 79, 475-497. Siegel, S. 1956. Nonparametric methods for the behaviorul sciences. New York: McGraw-Hill. Victor, M., Adams, R. D., & Collins, G. H. 1971. The Wernicke-Korsakoff syndrome. Philadelphia: F. A. Davis. Warrington, E. K., & Weiskrantz, L. 1974. The effect of prior learning on subsequent retention in amnesic patients. Neuropsychologia, 12, 419-428.
