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Cued recall in anterograde amnesia
BRAIN
AND
LANGUAGE
15,
70-81 (1982)
Cued Recall in Anterograde Amnesia C. DOUGLASWETZEL AND LARRY R. SQUIRE Veterans
Administration
Medical
Center, San Diego, and of Medicine, La Jolla
University
of California
School
After a single presentation of a word list, normal subjects exhibited better retention when prompted with semantic cues than with rhyme or letter cues. Alcoholic Korsakoff patients, patients receiving electroconvulsive therapy (ECT), and the patient N.A. exhibited impaired retention and, unlike control subjects, did not exhibit an advantage of semantic cues over letter and rhyme cues. Two experimental manipulations designed to equate the level of performance of amnesics and controls indicated that these amnesias could be understood as a reflection of weak memory strength that results from deficiencies in initial learning and retention. In addition, alcoholic Korsakoff patients appeared to have greater difficulty utilizing semantic cues than patients receiving ECT or patient N.A.
Analysis of the amnesic syndrome has provided useful information about normal human memory and its neurological organization. The available evidence suggests that amnesia is not a unitary disorder, so that different amnesias might reflect disorders in different aspects of memory function (Huppert & Piercy, 1979; Squire, 1981a). In addition, the alcoholic Korsakoff syndrome seems to include certain features not exhibited by other forms of amnesia that have been studied (Zangwill, 1977; Squire & Cohen, 1981, 1982). One way that patients with Korsakoff syndrome might be distinct is in their apparently deficient use of deeper, more elaborative encoding strategies (Butters & Cermak, 1980). Although the use of meaningful semantic encoding strategies leads to superior recall in normal individuals, such strategies are employed less often than normal by Korsakoff patients. Moreover, procedures that induce normal This research was supported by the Medical Research Service of the Veterans Administration, by an NIMH Fellowship (USPHS 1 T32 NS-07086-01) and by NIMH Grant MH24600. We thank the staffs of Mesa Vista, San Luis Rey, Centre City, Mercy, and Vista Hill Hospials for their full cooperation, Joy Beck for assistance, and Drs. Neal Cohen and Lynn Nadel for helpful comments. Dr. Douglas Wetzel is now at Navy Personnel Research & Development Center, San Diego, CA 92152. Address reprint requests to Larry R. Squire, Ph.D., Veterans Administration Medical Center, 3350 La Jolla Village Drive, San Diego, CA 92161. 70 0093-934X/82/010070-12$02.00/0 Copyright All rights
0 1982 by Academic Press, Inc. of reproduction in any form reserved.
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IN AMNESIA
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subjects to encode semantically are not always effective with Korsakoff patients, though they can be with other forms of amnesia that have been evaluated (Wetzel & Squire, 1980). In the study of amnesia, the effectiveness of cues given at retention testing has been of interest because such cues can often have a marked facilitatory effect on performance (Warrington & Weiskrantz, 1970; Squire, Wetzel, & Slater, 1978). Prompting memory with meaningful semantic cues produces better recall in normal individuals than prompting with nonsemantic cues, e.g., rhymes. In the case of alcoholic Korsakoff patients, however, semantic cuing is sometimes no more beneficial than rhyme cuing (Cermak, Butters, & Gerrein, 1973). It is not yet clear if such a deficit is present in other forms of amnesia. STUDY
1
The first study asked whether patients receiving ECT and the patient N.A. might fail to benefit in the normal way from semantic cues given at retention testing, and whether any deficit exhibited by these patients could be mimicked in the performance of control subjects tested long after learning. When a long retention inverval is used to equate the performance of control subjects to that of amnesic patients, it is not necessary to suppose that this level of performance has been achieved in the same way by both groups. This method simply provides a way of examining a pattern of recall at different levels of performance. Thus, apparent deficits in the use of semantic cues might have more to do with the strength of memory than with the ability to process semantic information. The amnesia associated with ECT is a relatively circumscribed, transient deficit that recovers gradually after treatment (Squire, 198lb). By 90 min after treatment, patients can perform normally on conventional tests of intellectual ability. Yet at this time they are deficient at acquiring new information and at recalling information that was acquired during the few years prior to treatment. The patient N.A. has been described in detail previously (Teuber, Milner, & Vaughan, 1968; Squire & Slater, 1978). Since 1960, he has exhibited persistent and strikingly circumscribed anterograde amnesia for verbal material. Methods Subjects read aloud a list of words and later were tested of cues: the semantic category of the target word, the initial and a rhyme for the target word.
for retention with three types two letters of the target word,
Patients ECT und depressed patienrs. Eighteen patients scribed bilateral ECT for the relief of depressive units of five local hospitals. Eight of the patients
(10 female, 8 male) who had been preillness were tested on the psychiatric had received ECT previously, but none
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AND SQUIRE
during the prior 2 years. ECT was given on Monday, Wednesday, and Friday with a Medcraft machine (140-160 V for 0.6-0.75 set) following medication with sodium methohexital, succinylcholine, and atropine. The electrodes were positioned bitemporally. The attending physician described each treatment as having produced a grand ma1 seizure, modified by the relaxant medication. Patients were tested on two different occasions, 90-120 min after the second, third, fourth, or fifth treatment in the series. For comparison to the ECT patients, 36 depressed psychiatric inpatients were also tested (13 males, 23 female). They were matched to the ECT patients with respect to age (40.5 vs. 42.7 for the ECT group) and years of education (13.6 vs. 12.5 for the ECT group). Three control subjects had received ECT more than 2 years previously. Case N.A. and controls. This individual became amnesic in 1960 at the age of 22 as the result of a penetrating brain injury with a miniature fencing foil (Teuber et al., 1968). In 1975 he scored well above average (124) on the Wechsler Adult Intelligence Scale (WARS). His Wechsler Memory Quotient is 27 points below his IQ. His verbal memory is considerably more impaired than his nonverbal memory, and he continues to exhibit a marked deficit in paired-associate learning and delayed recall (Squire & Slater, 1978). Computerized tomography has identified a lesion in the left thalamic region, in a position corresponding to the dorsomedial nucleus (Squire & Moore, 1979). In the present study, N.A.‘s performance was compared to that of 51 normal men, matched to him with respect to age (controls, 36.2; N.A., then 38). years of education (controls, 14.8; N.A., 13), WAIS subtest scores for information (controls, 22.3; N.A., 22), and for vocabulary (controls, 61.2; N.A., 66).
Materials A cued recall test was constructed using lists of 24 and 45 words. To allow repeated testing of subjects, several alternate forms were available for each list length. To select the words, a group of 62 hospital employees provided one-word answers to the cues used in the study (semantic category, initial two-letters, and rhyme; see Table 1). Frequently mentioned words were eliminated, and common nouns of four to seven letters were selected from the remainder. These data were also used to obtain a guessing correction for each cue used in the study. Recall probabilities were corrected with the formula (pU-pG)/(lpG), where pU is the observed (uncorrected) probability of correct recall and pG is the probability of obtaining a correct response by guessing (Green & Swets, 1966; Bahrick, 1970).
Procedure Prior to each word once for 4 10x 15-cm
presentation of a word list for learning, subjects were instructed to verbalize and to remember it in whatever manner they chose. Each word was presented set, with a 0.5~set interword interval. The words were printed individually on cards in 1.2~cm letters. The nature of the retention test was explained during
TABLE EXAMPLES
Information
type
Semantic (category) Graphic (2 letters) Phonemic (rhyme)
OF RETRIEVAL
1
CUES AND TARGET WORDS
Retrieval cue question
Target word
A type of BIRD ? Initial letters were DA ? Rhymes with MINE ?
CROW DANCE WINE
Note. All three cues were used once for each three words tested.
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a period of 45-60 set separating the end of the learning list from the presentation of the first retrieval cue. The learning word list was presented in a different random order for each subject. For retention testing, the experimenter asked for recall of each word from a fixed sequence of cues on a printed test. Each block of three words tested included a semantic-category, two-letter, and rhyme cue. In this way, successive blocks of cues in the test could equally sample the same average serial positions of the randomized learning list. Every cue was unique to only one word in the learning list. Subjects were asked to guess if they could not remember the target word. The 24-item list was given to a group of ECT patients (n = 9) and to a group of depressed control patients (n = 9). Similarly, the 4%item list was given to a different group of ECT patients (n = 9) and depressed control patients (n = 9). Each patient was tested twice on two nonconsecutive days with a different alternate form. The learning-retention interval was about 1 min. Two additional groups of depressed control patients (n = 9 each) were also given a 24-item or a 4%item learning list. Each of these patients was tested once after a retention interval of I day. The patient N.A. was given four alternate forms of the 24-item list and three alternate forms of the 4%item list. Retention was tested about 1 min after learning. His test sessions were spaced over a 4-month period. Twenty-four control subjects were tested once with the 24-item list, after retention intervals of 1 min, 1 day, and 7 days (n = 8 for each retention interval). Twenty-seven other control subjects were tested once with the 45item list, after retention intervals of 1 min. I day, and 7 days (n = 9 for each retention interval).
Results ECT. A 3 x 2 x 3 analysis of variance (ANOVA) was performed for the factors of patient group (ECT, I min; depressed, I min; depressed, I day), list length (24 vs. 45 items), and retrieval cue (category, letters, and rhyme). Overall, significantly’ greater recall was demonstrated with the short 24-item list than with the longer 45item list, F(1, 48) = 8.58 (Fig. 1). List length did not interact with any other factor (p’s > .3). Significant overall main effects were also obtained among the three patient groups, F(2, 48) = 18.19, and among the three retrieval cues, F(2, 96) = 19.36. The single significant interaction showed the ECT and depressed groups to differ in their responses to the three cues, F(4, 96) = 4.91. Tukey HSD studentized comparisons were performed on the nine means of the Groups x Cue interaction, collapsing list length (critical mean difference HSD = 0.136, df = 144). The depressed controls tested 1 min after learning recalled significantly better with the category cue than with either letter or rhyme cues. By contrast, ECT patients and controls tested 1 day after learning recalled about the same number of words in response to each cue. Thus the pattern of amnesic performance observed in patients receiving ECT was recapitulated in the performance of control subjects tested I day after learning. Case N.A. A 3 ~2x3 ANOVA was performed for the 51 control subjects. Significant main effects were obtained for the effect of retention interval, F(2, 45) = 49.3; list length, F( 1, 45) = 5.23, and for the effect of the three cues, F(2, 90) = 11.14. Recall of the 24and 45item lists was similar, and list length did not interact with other factors (p’s > .3). The only significant interaction indicated that differences among the three retrieval cues declined over the three retention intervals; Groups x Cue F(4, 90) = 4.24 (Fig. 2). That is, when tested 1 min after learning, category-cue recall was significantly greater than recall with letter or rhyme cues, but recall did not differ significantly among the three cues at 1 or 7 days after learning (HSD = 0.16, df = 135).
’ The level for significance was set at p < .05 for all statistical tests. Procedures are described in Kirk (1968).
74
WETZEL CUE:
0.0
AND
~cATEG~RY
24
SQUIRE 0 2 LETTERS
45
24
TOTAL
45
m RHYME
24
ITEMS
45
IN LIST
FIG. 1. Cued recall of patients receiving ECT and depressed control patients (DEP), both tested 1 min after learning. Right-hand panel shows cued recall for depressed controls after a retention interval of 1 day (DEP, 1 day). Corrected recall probabilities for the three retrieval cues are shown for learning lists of 24 and 45 words.
N.A.‘s performance was similar across the three cues, and for the category cue N.A. scored more poorly than did control subjects tested 1 min after learning (HSD = 0.23, & = 135). N.A.‘s performance did not differ significantly from that of I- or 7-day controls for any of the three cues. Thus, like ECT patients, N.A. performed similarly for the three cues, and this pattern of performance was mimicked in the weakened memory of controls tested 1 to 7 days after learning.
STUDY 2 The first study demonstrated that during the course of normal forgetting the performance of control subjects can mimic the pattern of recall exhibited by amnesic patients. In the second study, we asked whether the performance of amnesic patients could be improved by repeated presentations of the learning list prior to cuing. With increased memory strength, the pattern of cued recall might change to resemble that of normals. On the other hand, if the ability to use semantic information CUE:
ii
ICATEGORY
02
CONTROLS
0.6
3 0.2 ifi 0.0
LETTERS
IRHYME
CONTROLS I Day !I
24
45
24
TOTAL
45
ITEMS
24
45
24
45
IN LIST
FIG. 2. Cued recall for Case N.A. and matched controls tested 1 min after learning. The two right-hand panels show the cued recall of controls tested I or 7 days after learning.
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were in some way deficient in amnesia, then improvement might not be associated with any particular advantage of category cues over other kinds of cues. These possibilities were evaluated with additional patients receiving ECT, Case N.A., and a recently constituted population of alcoholic Korsakoff patients. Methods Patients ECT and depressed patients. Nine patients prescribed bilateral ECT (seven female, two male) were tested as described in the first study. Nine depressed patients not receiving ECT were tested as controls (eight female, one male). The patients receiving ECT averaged 45.5 years in age (46.0 for controls), and had an average of 13.4 years of education (12.3 for controls). One patient had received ECT 2 years previously, while none of the controls had ever received ECT. Three of the patients receiving ECT were tested on two different days and six were tested only once. Case N.A. and controls. Testing of N.A. began 1 year after the tests described in Study 1. Eight normal men served as controls (average age = 34.3, years of education = 15.6 years; WAIS information subtest score = 23.8; vocabulary = 62.3). Alcoholic Korsakoff and control putients. Nine alcoholic patients with Korsakoff syndrome participated in this study. This group of six men and three women averaged 51.8 years of age, and had 12.9 years of education. They had a mean full scale WAIS IQ of 102.4 and a mean Wechsler Memory Quotient of 76.4. None of the patients could recall any part of a short prose passage after 15 min. These patients were compared with a control group of nine male inpatients from the San Diego Veterans Hospital Alcoholic Treatment Program. The alcoholic patients were matched to the patients with Korsakoff syndrome with respect to age (49.1 years), years of education (12.9 years), and WAIS subtest scores.
Procedure The procedure was the same as in the first study, except that the list of words to be learned was repeated, up to 16 times, before the retention test. The order of the words in the list was randomly rearranged for each subject during an interval of 45-60 set between each list repetition. Patients receiving ECT were given either 4 x repetitions (n = 6) or 8 x repetitions (n = 6) of the 24-item learning list prior to the cuing test. Three patients were tested in both conditions. Nine depressed control subjects were given 4 x repetitions prior to cuing. For retention testing, three alternate forms were balanced across the subjects in each group so as to vary the order of the three cues. N.A. was given 4x and 8x repetitions of different 24-item learning lists. Eight different alternate forms of words and cues were given during a 6-month period. Korsakoff patients were tested after 1 x , 4 x , 8 x , or 16 x repetitions of the 24-item learning list. The patients were tested on four different occasions, and each patient received a different order of the four alternate test forms and a different order of the 1 x , 4 x , 8 x , and 16 x conditions. Nine alcoholic controls were given a single repetition of the learning list prior to retention testing.
Results ECT. Figure 3 shows the results of list repetition on cued recall. The results for a single presentation of the list, from Figs. 1 and 2, have been included here for comparison. Increasing memory strength by repetition raised the recall scores of ECT patients to the level and pattern of
WETZEL
76
‘.O
1
AND SQUIRE
ECT
DEP
0.6 z
0.4
iE
0.2
2 0.0 &
IX
4x
REPETITIONS
ax
IX
4x
PRIOR
TO RECALL
FIG. 3. Cued recall as a function of the number of pretest repetitions of a 24-word learning list. Patients receiving ECT (I x , 4 x , and 8 x repetitions) were compared to depressed controls (DEP, 1 x and 4 x ). The patient N.A. (1 x , 4 x , and 8 x ) was compared to his matched controls (1 x and 4 x ).
controls. A 3 x 3 ANOVA for the ECT patients showed a significant interaction of repetition trials x cue, F(4, 36) = 2.9. As repetitions of the learning list increased over the range 1 x , 4 x , and 8 x , ECT patients exhibited a different pattern of recall to the three cues. Simple main effect tests showed recall probability to increase significantly by .49 with category cuing (F = 20.9) and .34 with letter cuing (F = 9.8). An increase of .16 with rhyme cuing was not significant (F = 2.95).
ECT patients with 4 x repetitions did not significantly differ from depressed patients given a single list presentation for any of the three cues (F’s < 1). Both groups showed significant differences among cues (F’s = 5.2 and 6.4). After 8x repetitions, ECT patients recalled significantly less than the 4 x control group for letter cues (F = 8.1) and rhyme cues (F = 5.1), but not for category cues (F < 1). Both groups showed significant differences among cues (F’s = 26.3 and 30.5). Taken together, the results indicate that as recall scores improved through repetition, patients receiving ECT came to exhibit a normal pattern of performance. Case N.A. Figure 3 shows that Case N.A. improved his recall scores as a result of repetitions of the learning list, F(2, 9) = 14.7. Between 1 x and 8 x repetitions, N.A. showed increases of .71 with category cuing, . 45 with letters, and .36 with rhymes. In comparing N.A. to his controls, the HSD range statistic was based on the pooled MS error of
77
CUING IN AMNESIA CUE:
z i
1 CATEGORY
0.8
[7 2 LETTERS
KORSAKOFF
REPETITIONS
1 RHYME
A!-C.
PRIOR TO RECALL
FIG. 4. Cued recall of alcoholic Korsakoff patients tested after I x , 4 x , 8 x , or 16 x repetitions of a 24-word learning list. Alcoholic controls (ALC) were tested after a single (1 x ) repetition of the list.
1 x and 4x controls (HSD = .36, df = 42). After N.A. had received 4 x repetitions of the learning list, his recall to all three cues was similar to that of controls given a 1 x repetition. Likewise, after 8 x repetitions N.A. scored within the range of the 4x controls. Korsakoff syndrome. Figure 4 shows that after 16 x pretest repetitions the Korsakoff patients were able to achieve the pattern of recall achieved by alcoholic controls after a single acquisition trial. A 3 x 4 ANOVA showed a significant improvement in recall across the 1 x ,4 x , 8 x , and 16x repetitions, F(3, 24) = 8.5. The interaction of repetitions by the cue factor was not significant, F(6, 48) = 1.14. Over the 1 x to 16x range of repetitions, recall with the category cue increased .43, recall with the letters cue increased .26, and recall with the rhyme cue increased .24. Simple main effect tests indicated that this increase was significant only for the category cue (F = 8.2). These tests also showed that after 16x repetitions of the learning list there was a significant difference among the three cues (F = 4.7). An ANOVA for the alcoholic controls given a single 1 x repetition showed a significant difference among the recall cues, F(2, 16) = 3.9. Category-cue recall was significantly above the combined recall score associated with letter and rhyme cues, as determined by Scheffe’s method, F(2, 16) = 7.75. When 16x Korsakoff scores and the 1 x alcoholic scores were compared in a separate 2 x 3 ANOVA, there was a significant effect of cues F(2, 32) = 8.4, but no significant difference between the two groups, F(1, 16) = 2.07, and no interaction between groups in the pattern of cued recall (F < 1). DISCUSSION
As would have been expected from the literature on normal memory (Cermak & Craik, 1979), category cues were more effective than rhyme
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or letter cues in eliciting recall for the control groups. Patients receiving ECT, Case N.A., and patients with Korsakoff syndrome failed to demonstrate this normal advantage of category cues. Instead, the amnesic patients achieved about the same level of recall when given each of the three types of cues. Complementary methods were used to examine the efficacy of the different cues at different levels of overall performance by (a) lengthening the retention interval for control subjects so as to lower their performance level to that observed in amnesia; and (b) presenting the learning list repeatedly to amnesic patients so as to raise their performance level to that observed in control subjects. These two manipulations revealed a continuum of performance for both controls and amnesics, whereby at low levels of memory strength all cues benefited recall similarly and at higher levels of memory strength the category cue benefited recall more than the other cues. In the first study, the failure of N.A. and patients receiving ECT to be advantaged selectively by category cues was recapitulated in the performance of control subjects during forgetting. In the second study, which also involved patients with Korsakoff syndrome, category cues benefited performance of amnesic patients more and more as their overall level of performance improved, and in all cases a level of performance was eventually reached where the normal advantage of category cues over rhyme or letter cues could be demonstrated. Clearly a result that appears qualitatively distinct from the normal pattern of performance may sometimes be characterized more simply as a quantitative change along a normal continuum. This point has been made previously for other aspects of amnesia (Williams, 1953; Woods & Piercy, 1974; Squire et al., 1978; Wetzel & Squire, 1980; Squire, Nadel, & Slater, 1981; Mayes, Meudell, & Som, 1981; Meudell & Mayes, 1981). One might have expected the special effectiveness of category cues to have been maintained in normal subjects at all levels of memory strength. However, the selective advantage of category cues disappeared at long retention intervals. In order to obtain superior recall with the semantic cues there apparently must also be some minimal strength of the items in memory. By this view, recall reflects a multiplicative relationship between cue effectiveness, which is constant, and memory strength. Accordingly, differences in recall as a function of cue condition are best observed at short retention intervals when memory strength is maximal. When memory strength is weaker, absolute differences between the effects of category cues and other cues inevitably become smaller. Korsakoff patients have been considered to exhibit a greater difficulty in using semantic information than normal subjects (Butters & Cermak, 1980). In the present study this was reflected in the finding that for Korsakoff patients category cues were not more effective than the other cues, even after the learning list had been repeated four and eight times;
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IN AMNESIA
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yet for N.A. and ECT patients four and eight repetitions did permit category cues to be more effective. Like ECT patients and N.A., Korsakoff patients were able to quantitatively improve their performance. However, 16 repetitions of the learning list were required to improve the performance of Korsakoff patients to the point where it exhibited the normal pattern. This finding, that patients with Korsakoff syndrome did not exhibit a superior response to category cues as readily as other patients, seemed to occur without any obvious difference in the severity of anterograde amnesia exhibited by these different patient groups (Cohen & Squire, 1981). Accordingly, this finding seems consistent with the notion that Korsakoff syndrome is different from other forms of amnesia in some respects (Zangwill, 1977; Squire & Cohen, 1982). For example, Korsakoff syndrome is characterized by cognitive deficits and widespread neuropathology not shared by other forms of amnesia (Butters & Cermak, 1980; Squire & Cohen, 1982; Moscovitch, 1981). Moreover, both patients receiving ECT and the patient N.A. exhibited the normal tendency to improve their memory test scores when induced to encode semantically, whereas Korsakoff patients do not always exhibit this tendency (Wetzel & Squire, 1980). Although in the circumstances of the present study, patients with Korsakoff syndrome did appear to differ from the other patients with respect to their ability to use semantic information, it is also clear that similar kinds of procedures may not always reveal such a deficit, especially when the task is simplified (Cermak & Reale, 1978; Mayes, Meudell, & Neary, 1978; Cermak, Uhly, & Reale, 1980). The results of the present study, as well as many aspects of anterograde amnesia, appear to be understandable as a deficit in initial learning and/ or in postlearning processes (Squire et al., 1981; Wetzel & Squire, 1980; Squire et al., 1978). By this view the memory traces available for cuing at the time of retention testing are weaker than normal. The results of cuing studies have sometimes been taken to support retrieval explanations of amnesia (Warrrington & Weiskrantz, 1970). Although storage and retrieval views of amnesia are difficult to unravel entirely (Squire, 1980; Squire, 1982), a retrieval interpretation of cuing studies seems unnecessary. First, cuing is at least as effective in normal subjects as in amnesics so that after cuing a difference in performance between groups is typically maintained. Second, apparent qualitative differences in the effects of cues on normal and amnesic groups can frequently be reduced to quantitative differences along a normal continuum. That is, the deficit in amnesia can be recapitulated in a variety of respects by testing normal subjects long after learning. These considerations suggest that the deficit underlying anterograde amnesia might be illuminated by additional knowledge about the process of normal forgetting. Finally, the present results are also consistent with a growing body of evidence that
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patients with Korsakoff syndrome are unique in certain respects (Squire & Cohen, 1982), in that they appear to have some deficits in cognitive function not exhibited in other forms of amnesia. REFERENCES Bahrick, H. P. 1970. Two-phase model for prompted recall. Psychological Review, 77, 215-222. Butters, N., & Cermak, L. S. 1980. Alcoholic Korsakoffs syndrome: An information processing approach to amnesia. New York: Academic Press. Cermak, L. S., & Craik, F. I. M. 1979. Levels of processing in human memory. New York: Erlbaum. Cermak, L. S., Butters, N., & Gerrein, .I. 1973. The extent of the verbal encoding ability of Korsakoff patients. Neuropsychologia, 11, 85-94. Cermak, L. S., & Reale, L. 1978. Depth of processing and retention of words by Alcoholic Korsakoff patients. Journal of Experimental Psychology: Human Learning and Memory,
4, 165-174.
Cermak, L. S., Uhly, B., & Reale, L. 1980. Encoding specificity in the alcoholic Korsakoff patient. Brain and Language, 11, II9-127. Cohen, N. J., & Squire, L. R. 1981. Retrograde amnesia and remote memory impairment. Neuropsychologia,
19, 337-356.
Green, D. M., & Swets, J. A. 1966. Signal detection theory and psychophysics. New York: Krieger. P. 129. Huppert, F. A., & Piercy, M. 1979. Normal and abnormal forgetting in organic amnesia: effect of locus of lesion. Cortex, 15, 385-390. Kirk, R. E. 1968. Experimental Design: Procedures for the behavioral sciences. Belmont, CA: Brooks-Cole. Mayes, A. R., Meudell, P. R., & Neary, D. 1978. Must amnesia be caused by either encoding or retrieval disorders? In M. M. Grunberg, P. E. Morris, & R. N. Sykes (Eds.), Practical aspects of memory. London: Academic Press. Pp. 712-719. Mayes, A. R., Meudell, P. R., & Som, S. 1981. Further similarities between amnesia and normal attenuated memory: effects with paired-associate learning and contextual shifts. Neuropsychologia, in press. Meudell, P. R., & Mayes, A. R. 1981. Normal and abnormal forgetting: some comments on the human amnesic syndrome. In A. Ellis (Ed.), Normality and pathology in cognitive function. Academic Press, New York, in press. Moscovitch, M. 1981. Multiple dissociation of function in the amnesic syndrome. In L. S. Cermak (Ed.), Memory and amnesia. Hillsdale, NJ: Erlbaum. Squire, L. R. 1980. Specifying the defect in human anterograde amnesia: Storage, retrieval and semantics. Neuropsychologia, 18, 369-372. Squire, L. R. 198Ia. Two forms of human amnesia: An analysis of forgetting. Submitted for publication. Squire, L. R. 1981b. The neuropsychology of ECT. In W. Essman & R. Abrams (Eds.), Electroconvulsive
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York: Spectrum Publications, in press. Squire, L. R., 1982. Ann. Rev. Neuroscience, in press. Squire, L. R., & Cohen, N. J. 1981. Remote memory, retrograde amnesia, and the neuropsychology of memory. In L. Cermak (Ed.), Memory and amnesia. Hillsdale, NJ: Erlbaum. Squire, L. R., & Cohen, N. J. 1982. Human amnesia. In R. Thompson & J. McGaugh (Eds.), Handbook of behavioral biology. New York: Plenum. Vol. IO, in press. Squire, L. R., & Moore, R. Y. 1979. Dorsal thalamic lesion in a noted case of human memory dysfunction. Annals of Neurology, 6, 503-506.
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Squire, L. R., Nadel, L., & Slater, P. 1981. Anterograde amnesia and memory for temporal order. Neuropsychologia, 19, 141-145. Squire, L. R., & Slater, P. C. 1978. Anterograde and retrograde memory impairment in chronic amnesia. Neuropsychologia, 16, 313-322. Squire, L. R., Wetzel, C. D., & Slater, P. C. 1978. Anterograde amnesia following ECT: An analysis of the beneficial effects of partial information. Neuropsychologia, 16, 339-348. Teuber, H.-L., Mimer, B., & Vaughan, H. G. 1968. Persistent anterograde amnesia after stab wound of the basal brain. Neuropsychologia, 6, 267-282. Warrington, E. K., & Weiskrantz, L. 1970. Amnesic syndrome: Consolidation or retrieval? Nature
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Wetzel, C. D., & Squire, L. R. 1980. Encoding in anterograde amnesia. Neuropsychologia, 18, 177-184. Williams, M. 1953. Investigation of amnesic defects by progressive prompting. Journal of Neurology, Neurosurgety, and Psychiatry, 16, 14-18. Woods, R. T., & Piercy, M. 1974. A similarity between amnesic memory and normal forgetting. Neuropsychologia, 12, 437-445. Zangwill. 0. 1977. The amnesic syndrome. In 0. Zangwill & C. W. M. Witty (Eds.), Amnesia. London: Butterworths.
AND
LANGUAGE
15,
70-81 (1982)
Cued Recall in Anterograde Amnesia C. DOUGLASWETZEL AND LARRY R. SQUIRE Veterans
Administration
Medical
Center, San Diego, and of Medicine, La Jolla
University
of California
School
After a single presentation of a word list, normal subjects exhibited better retention when prompted with semantic cues than with rhyme or letter cues. Alcoholic Korsakoff patients, patients receiving electroconvulsive therapy (ECT), and the patient N.A. exhibited impaired retention and, unlike control subjects, did not exhibit an advantage of semantic cues over letter and rhyme cues. Two experimental manipulations designed to equate the level of performance of amnesics and controls indicated that these amnesias could be understood as a reflection of weak memory strength that results from deficiencies in initial learning and retention. In addition, alcoholic Korsakoff patients appeared to have greater difficulty utilizing semantic cues than patients receiving ECT or patient N.A.
Analysis of the amnesic syndrome has provided useful information about normal human memory and its neurological organization. The available evidence suggests that amnesia is not a unitary disorder, so that different amnesias might reflect disorders in different aspects of memory function (Huppert & Piercy, 1979; Squire, 1981a). In addition, the alcoholic Korsakoff syndrome seems to include certain features not exhibited by other forms of amnesia that have been studied (Zangwill, 1977; Squire & Cohen, 1981, 1982). One way that patients with Korsakoff syndrome might be distinct is in their apparently deficient use of deeper, more elaborative encoding strategies (Butters & Cermak, 1980). Although the use of meaningful semantic encoding strategies leads to superior recall in normal individuals, such strategies are employed less often than normal by Korsakoff patients. Moreover, procedures that induce normal This research was supported by the Medical Research Service of the Veterans Administration, by an NIMH Fellowship (USPHS 1 T32 NS-07086-01) and by NIMH Grant MH24600. We thank the staffs of Mesa Vista, San Luis Rey, Centre City, Mercy, and Vista Hill Hospials for their full cooperation, Joy Beck for assistance, and Drs. Neal Cohen and Lynn Nadel for helpful comments. Dr. Douglas Wetzel is now at Navy Personnel Research & Development Center, San Diego, CA 92152. Address reprint requests to Larry R. Squire, Ph.D., Veterans Administration Medical Center, 3350 La Jolla Village Drive, San Diego, CA 92161. 70 0093-934X/82/010070-12$02.00/0 Copyright All rights
0 1982 by Academic Press, Inc. of reproduction in any form reserved.
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IN AMNESIA
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subjects to encode semantically are not always effective with Korsakoff patients, though they can be with other forms of amnesia that have been evaluated (Wetzel & Squire, 1980). In the study of amnesia, the effectiveness of cues given at retention testing has been of interest because such cues can often have a marked facilitatory effect on performance (Warrington & Weiskrantz, 1970; Squire, Wetzel, & Slater, 1978). Prompting memory with meaningful semantic cues produces better recall in normal individuals than prompting with nonsemantic cues, e.g., rhymes. In the case of alcoholic Korsakoff patients, however, semantic cuing is sometimes no more beneficial than rhyme cuing (Cermak, Butters, & Gerrein, 1973). It is not yet clear if such a deficit is present in other forms of amnesia. STUDY
1
The first study asked whether patients receiving ECT and the patient N.A. might fail to benefit in the normal way from semantic cues given at retention testing, and whether any deficit exhibited by these patients could be mimicked in the performance of control subjects tested long after learning. When a long retention inverval is used to equate the performance of control subjects to that of amnesic patients, it is not necessary to suppose that this level of performance has been achieved in the same way by both groups. This method simply provides a way of examining a pattern of recall at different levels of performance. Thus, apparent deficits in the use of semantic cues might have more to do with the strength of memory than with the ability to process semantic information. The amnesia associated with ECT is a relatively circumscribed, transient deficit that recovers gradually after treatment (Squire, 198lb). By 90 min after treatment, patients can perform normally on conventional tests of intellectual ability. Yet at this time they are deficient at acquiring new information and at recalling information that was acquired during the few years prior to treatment. The patient N.A. has been described in detail previously (Teuber, Milner, & Vaughan, 1968; Squire & Slater, 1978). Since 1960, he has exhibited persistent and strikingly circumscribed anterograde amnesia for verbal material. Methods Subjects read aloud a list of words and later were tested of cues: the semantic category of the target word, the initial and a rhyme for the target word.
for retention with three types two letters of the target word,
Patients ECT und depressed patienrs. Eighteen patients scribed bilateral ECT for the relief of depressive units of five local hospitals. Eight of the patients
(10 female, 8 male) who had been preillness were tested on the psychiatric had received ECT previously, but none
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during the prior 2 years. ECT was given on Monday, Wednesday, and Friday with a Medcraft machine (140-160 V for 0.6-0.75 set) following medication with sodium methohexital, succinylcholine, and atropine. The electrodes were positioned bitemporally. The attending physician described each treatment as having produced a grand ma1 seizure, modified by the relaxant medication. Patients were tested on two different occasions, 90-120 min after the second, third, fourth, or fifth treatment in the series. For comparison to the ECT patients, 36 depressed psychiatric inpatients were also tested (13 males, 23 female). They were matched to the ECT patients with respect to age (40.5 vs. 42.7 for the ECT group) and years of education (13.6 vs. 12.5 for the ECT group). Three control subjects had received ECT more than 2 years previously. Case N.A. and controls. This individual became amnesic in 1960 at the age of 22 as the result of a penetrating brain injury with a miniature fencing foil (Teuber et al., 1968). In 1975 he scored well above average (124) on the Wechsler Adult Intelligence Scale (WARS). His Wechsler Memory Quotient is 27 points below his IQ. His verbal memory is considerably more impaired than his nonverbal memory, and he continues to exhibit a marked deficit in paired-associate learning and delayed recall (Squire & Slater, 1978). Computerized tomography has identified a lesion in the left thalamic region, in a position corresponding to the dorsomedial nucleus (Squire & Moore, 1979). In the present study, N.A.‘s performance was compared to that of 51 normal men, matched to him with respect to age (controls, 36.2; N.A., then 38). years of education (controls, 14.8; N.A., 13), WAIS subtest scores for information (controls, 22.3; N.A., 22), and for vocabulary (controls, 61.2; N.A., 66).
Materials A cued recall test was constructed using lists of 24 and 45 words. To allow repeated testing of subjects, several alternate forms were available for each list length. To select the words, a group of 62 hospital employees provided one-word answers to the cues used in the study (semantic category, initial two-letters, and rhyme; see Table 1). Frequently mentioned words were eliminated, and common nouns of four to seven letters were selected from the remainder. These data were also used to obtain a guessing correction for each cue used in the study. Recall probabilities were corrected with the formula (pU-pG)/(lpG), where pU is the observed (uncorrected) probability of correct recall and pG is the probability of obtaining a correct response by guessing (Green & Swets, 1966; Bahrick, 1970).
Procedure Prior to each word once for 4 10x 15-cm
presentation of a word list for learning, subjects were instructed to verbalize and to remember it in whatever manner they chose. Each word was presented set, with a 0.5~set interword interval. The words were printed individually on cards in 1.2~cm letters. The nature of the retention test was explained during
TABLE EXAMPLES
Information
type
Semantic (category) Graphic (2 letters) Phonemic (rhyme)
OF RETRIEVAL
1
CUES AND TARGET WORDS
Retrieval cue question
Target word
A type of BIRD ? Initial letters were DA ? Rhymes with MINE ?
CROW DANCE WINE
Note. All three cues were used once for each three words tested.
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a period of 45-60 set separating the end of the learning list from the presentation of the first retrieval cue. The learning word list was presented in a different random order for each subject. For retention testing, the experimenter asked for recall of each word from a fixed sequence of cues on a printed test. Each block of three words tested included a semantic-category, two-letter, and rhyme cue. In this way, successive blocks of cues in the test could equally sample the same average serial positions of the randomized learning list. Every cue was unique to only one word in the learning list. Subjects were asked to guess if they could not remember the target word. The 24-item list was given to a group of ECT patients (n = 9) and to a group of depressed control patients (n = 9). Similarly, the 4%item list was given to a different group of ECT patients (n = 9) and depressed control patients (n = 9). Each patient was tested twice on two nonconsecutive days with a different alternate form. The learning-retention interval was about 1 min. Two additional groups of depressed control patients (n = 9 each) were also given a 24-item or a 4%item learning list. Each of these patients was tested once after a retention interval of I day. The patient N.A. was given four alternate forms of the 24-item list and three alternate forms of the 4%item list. Retention was tested about 1 min after learning. His test sessions were spaced over a 4-month period. Twenty-four control subjects were tested once with the 24-item list, after retention intervals of 1 min, 1 day, and 7 days (n = 8 for each retention interval). Twenty-seven other control subjects were tested once with the 45item list, after retention intervals of 1 min. I day, and 7 days (n = 9 for each retention interval).
Results ECT. A 3 x 2 x 3 analysis of variance (ANOVA) was performed for the factors of patient group (ECT, I min; depressed, I min; depressed, I day), list length (24 vs. 45 items), and retrieval cue (category, letters, and rhyme). Overall, significantly’ greater recall was demonstrated with the short 24-item list than with the longer 45item list, F(1, 48) = 8.58 (Fig. 1). List length did not interact with any other factor (p’s > .3). Significant overall main effects were also obtained among the three patient groups, F(2, 48) = 18.19, and among the three retrieval cues, F(2, 96) = 19.36. The single significant interaction showed the ECT and depressed groups to differ in their responses to the three cues, F(4, 96) = 4.91. Tukey HSD studentized comparisons were performed on the nine means of the Groups x Cue interaction, collapsing list length (critical mean difference HSD = 0.136, df = 144). The depressed controls tested 1 min after learning recalled significantly better with the category cue than with either letter or rhyme cues. By contrast, ECT patients and controls tested 1 day after learning recalled about the same number of words in response to each cue. Thus the pattern of amnesic performance observed in patients receiving ECT was recapitulated in the performance of control subjects tested I day after learning. Case N.A. A 3 ~2x3 ANOVA was performed for the 51 control subjects. Significant main effects were obtained for the effect of retention interval, F(2, 45) = 49.3; list length, F( 1, 45) = 5.23, and for the effect of the three cues, F(2, 90) = 11.14. Recall of the 24and 45item lists was similar, and list length did not interact with other factors (p’s > .3). The only significant interaction indicated that differences among the three retrieval cues declined over the three retention intervals; Groups x Cue F(4, 90) = 4.24 (Fig. 2). That is, when tested 1 min after learning, category-cue recall was significantly greater than recall with letter or rhyme cues, but recall did not differ significantly among the three cues at 1 or 7 days after learning (HSD = 0.16, df = 135).
’ The level for significance was set at p < .05 for all statistical tests. Procedures are described in Kirk (1968).
74
WETZEL CUE:
0.0
AND
~cATEG~RY
24
SQUIRE 0 2 LETTERS
45
24
TOTAL
45
m RHYME
24
ITEMS
45
IN LIST
FIG. 1. Cued recall of patients receiving ECT and depressed control patients (DEP), both tested 1 min after learning. Right-hand panel shows cued recall for depressed controls after a retention interval of 1 day (DEP, 1 day). Corrected recall probabilities for the three retrieval cues are shown for learning lists of 24 and 45 words.
N.A.‘s performance was similar across the three cues, and for the category cue N.A. scored more poorly than did control subjects tested 1 min after learning (HSD = 0.23, & = 135). N.A.‘s performance did not differ significantly from that of I- or 7-day controls for any of the three cues. Thus, like ECT patients, N.A. performed similarly for the three cues, and this pattern of performance was mimicked in the weakened memory of controls tested 1 to 7 days after learning.
STUDY 2 The first study demonstrated that during the course of normal forgetting the performance of control subjects can mimic the pattern of recall exhibited by amnesic patients. In the second study, we asked whether the performance of amnesic patients could be improved by repeated presentations of the learning list prior to cuing. With increased memory strength, the pattern of cued recall might change to resemble that of normals. On the other hand, if the ability to use semantic information CUE:
ii
ICATEGORY
02
CONTROLS
0.6
3 0.2 ifi 0.0
LETTERS
IRHYME
CONTROLS I Day !I
24
45
24
TOTAL
45
ITEMS
24
45
24
45
IN LIST
FIG. 2. Cued recall for Case N.A. and matched controls tested 1 min after learning. The two right-hand panels show the cued recall of controls tested I or 7 days after learning.
CUING IN AMNESIA
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were in some way deficient in amnesia, then improvement might not be associated with any particular advantage of category cues over other kinds of cues. These possibilities were evaluated with additional patients receiving ECT, Case N.A., and a recently constituted population of alcoholic Korsakoff patients. Methods Patients ECT and depressed patients. Nine patients prescribed bilateral ECT (seven female, two male) were tested as described in the first study. Nine depressed patients not receiving ECT were tested as controls (eight female, one male). The patients receiving ECT averaged 45.5 years in age (46.0 for controls), and had an average of 13.4 years of education (12.3 for controls). One patient had received ECT 2 years previously, while none of the controls had ever received ECT. Three of the patients receiving ECT were tested on two different days and six were tested only once. Case N.A. and controls. Testing of N.A. began 1 year after the tests described in Study 1. Eight normal men served as controls (average age = 34.3, years of education = 15.6 years; WAIS information subtest score = 23.8; vocabulary = 62.3). Alcoholic Korsakoff and control putients. Nine alcoholic patients with Korsakoff syndrome participated in this study. This group of six men and three women averaged 51.8 years of age, and had 12.9 years of education. They had a mean full scale WAIS IQ of 102.4 and a mean Wechsler Memory Quotient of 76.4. None of the patients could recall any part of a short prose passage after 15 min. These patients were compared with a control group of nine male inpatients from the San Diego Veterans Hospital Alcoholic Treatment Program. The alcoholic patients were matched to the patients with Korsakoff syndrome with respect to age (49.1 years), years of education (12.9 years), and WAIS subtest scores.
Procedure The procedure was the same as in the first study, except that the list of words to be learned was repeated, up to 16 times, before the retention test. The order of the words in the list was randomly rearranged for each subject during an interval of 45-60 set between each list repetition. Patients receiving ECT were given either 4 x repetitions (n = 6) or 8 x repetitions (n = 6) of the 24-item learning list prior to the cuing test. Three patients were tested in both conditions. Nine depressed control subjects were given 4 x repetitions prior to cuing. For retention testing, three alternate forms were balanced across the subjects in each group so as to vary the order of the three cues. N.A. was given 4x and 8x repetitions of different 24-item learning lists. Eight different alternate forms of words and cues were given during a 6-month period. Korsakoff patients were tested after 1 x , 4 x , 8 x , or 16 x repetitions of the 24-item learning list. The patients were tested on four different occasions, and each patient received a different order of the four alternate test forms and a different order of the 1 x , 4 x , 8 x , and 16 x conditions. Nine alcoholic controls were given a single repetition of the learning list prior to retention testing.
Results ECT. Figure 3 shows the results of list repetition on cued recall. The results for a single presentation of the list, from Figs. 1 and 2, have been included here for comparison. Increasing memory strength by repetition raised the recall scores of ECT patients to the level and pattern of
WETZEL
76
‘.O
1
AND SQUIRE
ECT
DEP
0.6 z
0.4
iE
0.2
2 0.0 &
IX
4x
REPETITIONS
ax
IX
4x
PRIOR
TO RECALL
FIG. 3. Cued recall as a function of the number of pretest repetitions of a 24-word learning list. Patients receiving ECT (I x , 4 x , and 8 x repetitions) were compared to depressed controls (DEP, 1 x and 4 x ). The patient N.A. (1 x , 4 x , and 8 x ) was compared to his matched controls (1 x and 4 x ).
controls. A 3 x 3 ANOVA for the ECT patients showed a significant interaction of repetition trials x cue, F(4, 36) = 2.9. As repetitions of the learning list increased over the range 1 x , 4 x , and 8 x , ECT patients exhibited a different pattern of recall to the three cues. Simple main effect tests showed recall probability to increase significantly by .49 with category cuing (F = 20.9) and .34 with letter cuing (F = 9.8). An increase of .16 with rhyme cuing was not significant (F = 2.95).
ECT patients with 4 x repetitions did not significantly differ from depressed patients given a single list presentation for any of the three cues (F’s < 1). Both groups showed significant differences among cues (F’s = 5.2 and 6.4). After 8x repetitions, ECT patients recalled significantly less than the 4 x control group for letter cues (F = 8.1) and rhyme cues (F = 5.1), but not for category cues (F < 1). Both groups showed significant differences among cues (F’s = 26.3 and 30.5). Taken together, the results indicate that as recall scores improved through repetition, patients receiving ECT came to exhibit a normal pattern of performance. Case N.A. Figure 3 shows that Case N.A. improved his recall scores as a result of repetitions of the learning list, F(2, 9) = 14.7. Between 1 x and 8 x repetitions, N.A. showed increases of .71 with category cuing, . 45 with letters, and .36 with rhymes. In comparing N.A. to his controls, the HSD range statistic was based on the pooled MS error of
77
CUING IN AMNESIA CUE:
z i
1 CATEGORY
0.8
[7 2 LETTERS
KORSAKOFF
REPETITIONS
1 RHYME
A!-C.
PRIOR TO RECALL
FIG. 4. Cued recall of alcoholic Korsakoff patients tested after I x , 4 x , 8 x , or 16 x repetitions of a 24-word learning list. Alcoholic controls (ALC) were tested after a single (1 x ) repetition of the list.
1 x and 4x controls (HSD = .36, df = 42). After N.A. had received 4 x repetitions of the learning list, his recall to all three cues was similar to that of controls given a 1 x repetition. Likewise, after 8 x repetitions N.A. scored within the range of the 4x controls. Korsakoff syndrome. Figure 4 shows that after 16 x pretest repetitions the Korsakoff patients were able to achieve the pattern of recall achieved by alcoholic controls after a single acquisition trial. A 3 x 4 ANOVA showed a significant improvement in recall across the 1 x ,4 x , 8 x , and 16x repetitions, F(3, 24) = 8.5. The interaction of repetitions by the cue factor was not significant, F(6, 48) = 1.14. Over the 1 x to 16x range of repetitions, recall with the category cue increased .43, recall with the letters cue increased .26, and recall with the rhyme cue increased .24. Simple main effect tests indicated that this increase was significant only for the category cue (F = 8.2). These tests also showed that after 16x repetitions of the learning list there was a significant difference among the three cues (F = 4.7). An ANOVA for the alcoholic controls given a single 1 x repetition showed a significant difference among the recall cues, F(2, 16) = 3.9. Category-cue recall was significantly above the combined recall score associated with letter and rhyme cues, as determined by Scheffe’s method, F(2, 16) = 7.75. When 16x Korsakoff scores and the 1 x alcoholic scores were compared in a separate 2 x 3 ANOVA, there was a significant effect of cues F(2, 32) = 8.4, but no significant difference between the two groups, F(1, 16) = 2.07, and no interaction between groups in the pattern of cued recall (F < 1). DISCUSSION
As would have been expected from the literature on normal memory (Cermak & Craik, 1979), category cues were more effective than rhyme
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or letter cues in eliciting recall for the control groups. Patients receiving ECT, Case N.A., and patients with Korsakoff syndrome failed to demonstrate this normal advantage of category cues. Instead, the amnesic patients achieved about the same level of recall when given each of the three types of cues. Complementary methods were used to examine the efficacy of the different cues at different levels of overall performance by (a) lengthening the retention interval for control subjects so as to lower their performance level to that observed in amnesia; and (b) presenting the learning list repeatedly to amnesic patients so as to raise their performance level to that observed in control subjects. These two manipulations revealed a continuum of performance for both controls and amnesics, whereby at low levels of memory strength all cues benefited recall similarly and at higher levels of memory strength the category cue benefited recall more than the other cues. In the first study, the failure of N.A. and patients receiving ECT to be advantaged selectively by category cues was recapitulated in the performance of control subjects during forgetting. In the second study, which also involved patients with Korsakoff syndrome, category cues benefited performance of amnesic patients more and more as their overall level of performance improved, and in all cases a level of performance was eventually reached where the normal advantage of category cues over rhyme or letter cues could be demonstrated. Clearly a result that appears qualitatively distinct from the normal pattern of performance may sometimes be characterized more simply as a quantitative change along a normal continuum. This point has been made previously for other aspects of amnesia (Williams, 1953; Woods & Piercy, 1974; Squire et al., 1978; Wetzel & Squire, 1980; Squire, Nadel, & Slater, 1981; Mayes, Meudell, & Som, 1981; Meudell & Mayes, 1981). One might have expected the special effectiveness of category cues to have been maintained in normal subjects at all levels of memory strength. However, the selective advantage of category cues disappeared at long retention intervals. In order to obtain superior recall with the semantic cues there apparently must also be some minimal strength of the items in memory. By this view, recall reflects a multiplicative relationship between cue effectiveness, which is constant, and memory strength. Accordingly, differences in recall as a function of cue condition are best observed at short retention intervals when memory strength is maximal. When memory strength is weaker, absolute differences between the effects of category cues and other cues inevitably become smaller. Korsakoff patients have been considered to exhibit a greater difficulty in using semantic information than normal subjects (Butters & Cermak, 1980). In the present study this was reflected in the finding that for Korsakoff patients category cues were not more effective than the other cues, even after the learning list had been repeated four and eight times;
CUING
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yet for N.A. and ECT patients four and eight repetitions did permit category cues to be more effective. Like ECT patients and N.A., Korsakoff patients were able to quantitatively improve their performance. However, 16 repetitions of the learning list were required to improve the performance of Korsakoff patients to the point where it exhibited the normal pattern. This finding, that patients with Korsakoff syndrome did not exhibit a superior response to category cues as readily as other patients, seemed to occur without any obvious difference in the severity of anterograde amnesia exhibited by these different patient groups (Cohen & Squire, 1981). Accordingly, this finding seems consistent with the notion that Korsakoff syndrome is different from other forms of amnesia in some respects (Zangwill, 1977; Squire & Cohen, 1982). For example, Korsakoff syndrome is characterized by cognitive deficits and widespread neuropathology not shared by other forms of amnesia (Butters & Cermak, 1980; Squire & Cohen, 1982; Moscovitch, 1981). Moreover, both patients receiving ECT and the patient N.A. exhibited the normal tendency to improve their memory test scores when induced to encode semantically, whereas Korsakoff patients do not always exhibit this tendency (Wetzel & Squire, 1980). Although in the circumstances of the present study, patients with Korsakoff syndrome did appear to differ from the other patients with respect to their ability to use semantic information, it is also clear that similar kinds of procedures may not always reveal such a deficit, especially when the task is simplified (Cermak & Reale, 1978; Mayes, Meudell, & Neary, 1978; Cermak, Uhly, & Reale, 1980). The results of the present study, as well as many aspects of anterograde amnesia, appear to be understandable as a deficit in initial learning and/ or in postlearning processes (Squire et al., 1981; Wetzel & Squire, 1980; Squire et al., 1978). By this view the memory traces available for cuing at the time of retention testing are weaker than normal. The results of cuing studies have sometimes been taken to support retrieval explanations of amnesia (Warrrington & Weiskrantz, 1970). Although storage and retrieval views of amnesia are difficult to unravel entirely (Squire, 1980; Squire, 1982), a retrieval interpretation of cuing studies seems unnecessary. First, cuing is at least as effective in normal subjects as in amnesics so that after cuing a difference in performance between groups is typically maintained. Second, apparent qualitative differences in the effects of cues on normal and amnesic groups can frequently be reduced to quantitative differences along a normal continuum. That is, the deficit in amnesia can be recapitulated in a variety of respects by testing normal subjects long after learning. These considerations suggest that the deficit underlying anterograde amnesia might be illuminated by additional knowledge about the process of normal forgetting. Finally, the present results are also consistent with a growing body of evidence that
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patients with Korsakoff syndrome are unique in certain respects (Squire & Cohen, 1982), in that they appear to have some deficits in cognitive function not exhibited in other forms of amnesia. REFERENCES Bahrick, H. P. 1970. Two-phase model for prompted recall. Psychological Review, 77, 215-222. Butters, N., & Cermak, L. S. 1980. Alcoholic Korsakoffs syndrome: An information processing approach to amnesia. New York: Academic Press. Cermak, L. S., & Craik, F. I. M. 1979. Levels of processing in human memory. New York: Erlbaum. Cermak, L. S., Butters, N., & Gerrein, .I. 1973. The extent of the verbal encoding ability of Korsakoff patients. Neuropsychologia, 11, 85-94. Cermak, L. S., & Reale, L. 1978. Depth of processing and retention of words by Alcoholic Korsakoff patients. Journal of Experimental Psychology: Human Learning and Memory,
4, 165-174.
Cermak, L. S., Uhly, B., & Reale, L. 1980. Encoding specificity in the alcoholic Korsakoff patient. Brain and Language, 11, II9-127. Cohen, N. J., & Squire, L. R. 1981. Retrograde amnesia and remote memory impairment. Neuropsychologia,
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Green, D. M., & Swets, J. A. 1966. Signal detection theory and psychophysics. New York: Krieger. P. 129. Huppert, F. A., & Piercy, M. 1979. Normal and abnormal forgetting in organic amnesia: effect of locus of lesion. Cortex, 15, 385-390. Kirk, R. E. 1968. Experimental Design: Procedures for the behavioral sciences. Belmont, CA: Brooks-Cole. Mayes, A. R., Meudell, P. R., & Neary, D. 1978. Must amnesia be caused by either encoding or retrieval disorders? In M. M. Grunberg, P. E. Morris, & R. N. Sykes (Eds.), Practical aspects of memory. London: Academic Press. Pp. 712-719. Mayes, A. R., Meudell, P. R., & Som, S. 1981. Further similarities between amnesia and normal attenuated memory: effects with paired-associate learning and contextual shifts. Neuropsychologia, in press. Meudell, P. R., & Mayes, A. R. 1981. Normal and abnormal forgetting: some comments on the human amnesic syndrome. In A. Ellis (Ed.), Normality and pathology in cognitive function. Academic Press, New York, in press. Moscovitch, M. 1981. Multiple dissociation of function in the amnesic syndrome. In L. S. Cermak (Ed.), Memory and amnesia. Hillsdale, NJ: Erlbaum. Squire, L. R. 1980. Specifying the defect in human anterograde amnesia: Storage, retrieval and semantics. Neuropsychologia, 18, 369-372. Squire, L. R. 198Ia. Two forms of human amnesia: An analysis of forgetting. Submitted for publication. Squire, L. R. 1981b. The neuropsychology of ECT. In W. Essman & R. Abrams (Eds.), Electroconvulsive
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Wetzel, C. D., & Squire, L. R. 1980. Encoding in anterograde amnesia. Neuropsychologia, 18, 177-184. Williams, M. 1953. Investigation of amnesic defects by progressive prompting. Journal of Neurology, Neurosurgety, and Psychiatry, 16, 14-18. Woods, R. T., & Piercy, M. 1974. A similarity between amnesic memory and normal forgetting. Neuropsychologia, 12, 437-445. Zangwill. 0. 1977. The amnesic syndrome. In 0. Zangwill & C. W. M. Witty (Eds.), Amnesia. London: Butterworths.