Neuropsychologia.
1976, Vol. 14, pp. 31 l-326. Pergamon Press. Printed in England.
THE ENCODING CAPACITY OF A PATIENT AMNESIA DUE TO ENCEPHALITIS
WITH
LAIRD S. CERMAK* Psychology Service, Boston Veterans Administration Hospital and Aphasia Research Unit, Neurology Department, Boston University School of Medicine, Boston, Mass. 02118, U.S.A. (Received 16Jwre 1975) Abstract-A patient with amnesia due to encephalitis was examined in an effort to identify the factors that might contribute to his memory disturbances. It was discovered that this patient had the ability to analyze incoming verbal information on a level comparable to that achieved by normals. Furthermore, this ability enabled him to retain a limited amount of information for a brief interval, but, as soon as further information was introduced, it appeared to displace completely the older information in his working memory. As a consequence, information never
seemed to be consolidated into permanent, long-term, memory. Several attempts to increase the amount of information that could be consolidated (e.g. through use of visual imagery, verbal mediation, etc.) were attempted with promising, yet limited, results. INTRODUCTION EXPERIMENTS designed to assess the short-term memory and encoding capabilities of amnesic patients have often produced quite disparate results. On the one hand, there are reports that demonstrate rather dramatic deficits in the ability of amnesic patients to remember verbal information for even very short periods of time [l, 21. These reports have generally concluded that this deficit can be attributed to the amnesic patients’ inability to encode spontaneously the semantic properties of information [3, 41. Meanwhile, reports that do not find these same short-term memory [5, 61 or encoding [7, 81 deficits in amnesic patients, have concluded that the amnesic syndrome represents an inability to “retrieve” information from long-term memory rather than an initial deficit in encoding or an inability to consolidate material into memory. One possible reason why these differential results have been obtained is that two different types of amnesics have been under investigation. Data favoring short-term retention and encoding deficits has come primarily from testing a population consisting solely of alcoholic Korsakoff patients, while the data favoring a retrieval deficit has been gathered from a “mixture” of amnesic patients including post-encephalitics, a case of CO2 poisoning and some Korsakoff cases. It has been suggested [9] that before any further generalizations about “amnesia” can be made, those tests which have demonstrated deficits in alcoholic Korsakoff patients must be given to other types of amnesics in the exact manner in which they were originally presented. In particular it would appear to be desirable to give these tests to post-encephalitic patients because, as previous reports have suggested [lo, 111, these patients are most likely to differ from the alcoholic KorsakofY patient. The present report provides such an analysis in the case of a post-encephalitic patient who is unique not only because of the extreme density of his
“Reprint requests may be sent to: Laird S. Cermak, Psychology Service, Boston VA Hospital, Huntington Ave., Boston, Mass., 02130. U.S.A. 311
150 So.
312
LAIRD S. CERMAK
amnesic syndrome but because he has remained an extremely intelligent, highly motivated individual despite his deficit. Also, since the clinical picture of this patient suggests bilateral hippocampal involvement, several parallels to results obtained with MILNER’S [12] patient, H.M., can be drawn wherever similar experiments have been performed. ln addition, a variety of therapeutic techniques were attempted with this patient and the results of these attempts have provided additional insight into the amnesic syndrome. CASE
HISTORY
S.S. is a 44 yr old male physicist who was in good health until August 17, 1971 when he developed specific malaise, fever and a headache. He was initially evaluated at the Waltham Hosoital and then transferred to the Peter Bent Brigham Hospital where a diagnosis of herpes simplex encephaliiis was made. Examination of CSF revealed increased pressure, 180 mg% protein with increased gamma globulin fraction (31 x) and 58 mononuclear cells. A left temporal biopsy was performed and the culture was positive for herpes simplex. In addition, a left frontal Ommaya shunt, which entered the left frontal horn, was inserted during the operation. The patient remained in a coma for approximately one month during which time he often ran a high fever (106-108”) with occasional seizures. Upon regaining consciousness the patient had a right hemiparesis, a language disturbance described as incoherent speech and amnesia. At discharge, six weeks later, his right hemiparesis and language disorder had cleared entirely, but the amnesic disturbance remained. Sometime during the 2 weeks between regaining consciousness and discharge the patient was given the Wechsler memory scale and it was discovered that his M.Q. was 50. On December 12, 1971, S.S. was readmitted to the Peter Bent Brigham Hospital for re-evaluation. A pneumoencephalogram performed at this time revealed dilation of the lateral ventricles and third ventricle. There was marked atrophy of the left temporal lobe, some atrophy of the right temporal lobe and possible atrophy of the thalamus. A brain scan showed uptake in the left temporal and left frontal regions with no change from 9/22/71. At this time his M.Q. had risen to 71 and his I.Q. was found to be 112. His wife reports that his I.Q. had been above 145 prior to the onset of his illness and this is consistent with his educational level (M.S. in physics) and occupational position (President of a small optical firm). At this time the patient denied having a memory problem, but showed anxiety in moments of failure. On October 11, 1973, the patient was referred to the Boston VA Psychology Service for evaluation and possible treatment of his memory disorder. He was subsequently admitted to the hospital October 17, 1973, for intensive observation and psychological testing. Hc remained at the hospital for two weeks and thercafter was seen 3 times a week by the Psychology Service as an outpatient for approximately 9 months. During his stay in the VA Hospital a neurologic examination was performed. Anosmia was demonstrated and there was evidence of a left ptosis and a pupil that was less reactive to light on the left side. There was decreased movement of the left eye to medial and superior directions, but the remainder of the examination was normal. A brain scan again showed uptake over the left periphery in the anterior view. An EEG revealed left mid-posterior abnormalities with lesser left anterior disturbance. I.Q. at this time was found to be 133 (Verbal I.Q. = 130; Performance I.Q. = 133), and his M.Q. was 83.5,both improvements from previous testing of 12171. The Boston Diagnostic aohasia battery was given and no imoairment was found. In addition. no impairment was found on aparietal iobe battery.Apparently the only residual behavioral deficit still remaining as a consequence of S.S.‘s herpes simplex encephalitis is a marked memory deficit. S.S. is still unable to remember day-to-day even&, he is disoriented in time and space, and has considerable retrograde amnesia (for instance he was unable to describe his honeymoon from the early forties or his college days) yet remembers many important national events that occurred prior to his illness. During testing S.S. demonstrated considerable insight into his memory disorder. and listed it as his sole difficulty. He was attentive and motivated, consistently seeking any cues to aid him during retrieval. He still evidenced some anxiety when unable to retrieve information but often covered hi, anxiety with flippant remarks which proved to be quite perseverative both within and between sessions. Testing was carried out over a period of 9 months and the results of this testing are reported here.
RESULTS The results of the Wechsler Adult Intelligence Scale (WAIS) examination and the Wcchslcr Memory Scale are reported in Table I. The rest of the tests that were given to S.S. have not been nearly as well documented as the WAIS; for that reason, the nature of these tests, and S.S’s performance on them relative to Korsakoff patients and normal controls, will be reported in greater detail.
THE ENCODtNG
CAPACITY
OF A PATIENT
WITH
AMNESIA
DUE TO ENCEPHALmS
313
Table 1. Wechsler adult intelligencescale and Wechsler memory scale subtest scores for S.S.
Scaled
Raw
UAIS test
Score
Informat ion Comprehension Arithmetic Similarities Digit Span Vocabulary
Score 14 14 14 19 13 17 -
25 22 16 25 13 76 Verbal Score
Digit Symbol Picture Completion ;jloc!c Design Picture Arrangement Object Assembly
=
130 I0
71
=
133 IQ
162
=
133 Ic,
16 12 18 14
73 16 48 30 33
II
Performance Full
91
Score
Scale Score
Rat, Score
1%!eci:sler I:emnry Information Orientation Hental Control Memory Passages Digits Total Visual Reproduction Associate Learning
3 3 6
a
14 7 5.5
Total Raw Score
46.5
Corrected Score
86.5
x.q.
53.5
Short-term memoty’ distractor tasks Recall of CCC’s, WWW’s ad sirzgle words. The distractor technique and its several variations have been described previously by several investigators [I, 5, 91. In the present instance, either a consonant trigram (CCC), a word triad (WWW), or a single word was presented visually to the patient for 2 sec. Immediately patient was required to count backward by threes from experimenter. This number differed from trial to trial and was paced at a rate of one number per second. After the
following this presentation the a number given to him by the the patient’s counting backward patient counted backward for an
LARD
314
S. CERMAK
interval varying from 3 to 18 set, he was asked to recall the material to be remembered. This procedure continued with the same type of material until the patient had received 5 trials at each retention interval (0, 3, 9 and 18 sec.). S.S. was tested 3 times on each type of material and the average of these 3 times is reported here. His performance on CCC’s, compared with the previously reported [I] performance for Korsakoff patients and for normal controls, is shown in Fig. I. The same comparisons for WWW’s are shown in Fig. -! and. for single words, in Fig. 3. As can be seen.
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FIG. 1. Percentage of CCC’s (consonant trigrams) recalled by S.S., Korsakoff and normal controls (N) following 0, 3, 9. or 18 sec.
patients (K),
FIG. 2. Percentage of word trigrams (WWW’s) recalled by S.S., Korsakoff patients (K), and normal controls (N) following 0, 3, 9 or 19 see of distraction.
THE
ENCODlNG
CAPACITY
OF A PATIENT
WITH
f+?temon
F’IG. 3. Percentage
AMNESIA
DUE
315
TO ENCEPHALITIS
interval, see
of single words recalled by S.S., Korsakoff patients controls (N) following 0, 3, 9 or 18 set of distraction.
(K), and normal
S.S. performed normally on all these tests despite having a more demanding activity than did the Korsakoff patients and the controls of the previous study, always permitted to start from 100 and to count backwards by twos.
distractor who were
Interference tasks. Previous research [2] has shown that alcoholic Korsakoff patients are more susceptible to the effects of proactive interference during their performance on the distractor task than are normal controls. Therefore, despite his normal performance on the task, it was decided to test the susceptibility of S.S. to the effects of increasing or decreasing interference within this task. This was accomplished in two ways: by massing the trials through the use of a short (6 set) intertrial interval and comparing this with distributed trials having a 1 min intertrial interval ; or by having every other trial preceded by material from either the same conceptual class (words or CCC’s) as the critical material or from the other class. In other words, when recall of CCC’s was investigated only recall from every other trial was counted, some of these trials being preceded by a trial also containing CCC’s, a high Proactive Interference (PI) condition, and some preceded by trials containing WWW’s (low PI condition). A more detailed description of both the massed vs distributed and high vs low interference tasks can be found elsewhere [2]. It suffices here to say that S.S. performed above even our normal controls on both these tasks. As Figs. 4 and 5 show, he was somewhat affected by increased interference, but the effects were no more than those found for the normal subjects. Release from PI. WICKENS [13] has shown that, for normal subjects, the proactive interference that is generated across successive trials by the distractor task can be eliminated, and recall can be increased, when material from a class differing from that of the preceding material is introduced (Fig. 6). CERMAK, BUTTERS and MOREINES [4] have shown that this “release from proactive interference” does not occur for Korsakoff patients (Fig. 7) when the critical material is drawn from different taxonomic categories (e.g. animals, vegetables,
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4. Percentage of CCC’S and WWW’S recalled by S.S., Korsakoff patients. and control\ as a function of the length of the intertrial interval.
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FIG. 5. Percentage of WWW’s recalled by S.S.. Korsakoff patients, and controls followmg high and low PI conditions and retention intervals of 3. 9 and 18 sec.
tools and articles of clothing). Since S.S. performed so well OII the distractor task it wnh decided to test whether or not he was encoding information semantically. This was tested by determining whether or not a change in taxonomic categories resulted in a release from proactive interference for S.S. in the way it does for normals.
THE
ENCODING
CAPACITY
IO0
OF A PATIENT
Taxonomic
WITH
categories
control
AMNESIA
DUE
317
TO ENCEPHALITIS
group
t
Trials FIG.
6. Probability
of recall for normal controls following a shift in taxonomic Taxonomic
100
categories
Korsakoff
categories.
group
t
Trials
FIG. 7. Probability of recall for Korsakoff patients following a shift in taxonomlc categories.
In the actual task, 3 words from one category (e.g. animals) were presented on each of the first 4 trials of a distractor task. Then on the Fifth Trial 3 words from another category (e.g. vegetables) were presented. S.S. was tested in this manner for three different taxonomic shifts; the results can be seen in Fig. 8. It can reasonably be inferred that S.S. does encode spontaneously by taxonomic category, and it may be this ability that accounts for his superior performance on the distractor task relative to the Korsakoff patients. Verbal recall vs non-verbal recall. Although S.S. had normal distractor task recall for verbal material, it did not necessarily follow that his non-verbal recall would also be normal. Therefore, S.S. was given a test of his non-verbal memory similar to the preceding tests except that it involved recognition rather than recall. This test, which has also been described elsewhere [14], involves showing the patient an irregular geometric form (Vanderplas
FIG. 8. Probatxllty
of recall for S.S. following
a shift in taXouomtc
categorle\
and Garvin randomly generated shapes) and then asking him to perform either a verbal distractor task (counting backward) or. in another condition, a non-verbal distractor task (tracking musical notes). At the end of a 20 see retention interval the patient is shown ;I second stimulus and asked whether it is the “same as” or “different from” the first. A verbal (WWW) recognition test is also given. using the same distractor conditions so that recognition scores for non-verbal materials can be compared to those for verbal material. Korsakoff patients arc impaired on the verbal task followed by verbal distraction and are normal on the verbal task followed by non-verbal distraction. On the other hand, the nonverbal recall of Korsakoff patients is impnircd regardless of the nature of the distractor task, though not quite to the same extent a> their verbal recall following verbal distraction. The same procedures wcrc used with S.S. in order to determine whether or not his nonverbal retention matched his verbal retention. As cm be seen in Fig. 9, S.S.‘s non-verbal recall was dramatically worse than his verbal recall and was far below the normal\. III
E&l 0 -
Korsakoff Control S.S.
l-l
v-v
FIG. 9. Percentage
ol’ CCC’S
non-verbal
NV-NV
NV-V
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-
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(V) and random forms (NV) recognized following verbal by S.S.. Korsakoff patients. and control\.
(NV) distraction
(V) 01
I HE ENCODING
CAPACITY
OF A PATIENT
WITH
AMNESlA
DUE
‘I’0 ENCEPHALITIS
319
fact it was on a par with that of the KorsakolI patients. Apparently, whatever form of encoding is available to normals for the retention of non-verbal information (possibly some form of imagery), it is not available to, or used by S.S. A comparable finding has also been reported for H.M. by SIDMAN, STODDARD and MOHR [15]. H.M. also had the ability to retain verbal material over an undisrupted retention interval of up to 40 set, but could not do the same for non-verbal material. It must be emphasized again, however, that such an undisrupted retention interval does not in any way prevent verbal rehearsal during the interval. Motor nremory. Interestingly enough what does seem to be available to S.S. is the ability to retain a motor movement, at least over a period of IO-20 sec. It has been discovered [ 161 that Korsakoff patients lose their recollection, more rapidly than normals, of how far to pull a bar. On this test the patient’s hand is placed on a sliding bar while he is blindfolded. The experimenter moves the bar a predetermined distance and returns it with the patients’ hand to the start position. Either 10 or 20 set later the patient is required to return the bar to the same position as that just shown him. S.S. performed this test as well as the best normal subject, which may mean that whatever cues normals use to enable them to perform this task may also be available to S.S.
Speed
of processit~g
One explanation for the impoverished encoding by Korsakoff patients has been advanced by OSCAR-BERMAN,GOODGLASSand CHERLOW [17] who found that the Korsakoff patients’ visual recognition thresholds for words and patterns was far higher than in normals, i.e. the duration of presentation had to be longer before the Korsakoff patients could identify either type of material than was the case for normals. These investigators also found that the interval between the presentation of a target stimulus and a second (masking) stimulus had to be longer in order for Korsakoff patients to identify the target stimulus than it had to be for normals. S.S.‘s threshold measure and critical inter-stimulus interval (ISI) fell within the normal range although in both cases he was on the low end (high threshold and long 1%) of this range. On a second speed of processing task recently developed by GLOSSER [18], Korsakoli’ patients were found to be normal in their ability to detect instances in which a particular number was presented to them through headphones, but deficient in their ability to detect instances in which a particular combination of numbers appeared dichotically (a 5 in one ear and a 9 in the other), at least when the interpair interval was brief (I.2 set). When this same interval was increased to 2 set, the performance of the Korsakoff patients approached normality. This seemed to indicate that Korsakoff patients need more processing time, perhaps to read out what is in their sensory register, than do normals. As might by now be expected, S.S.‘s performance on Glosser’s test was perfectly normal, in fact, superior to most normals. Evidently S.S. is capable of normal analysis at a normal speed. In light of this the results of the next set of encoding tasks were somewhat surprising.
False recogt~ith. UNDERWOOD 1193has developed a technique that can be used to measure the type of encoding subjects perform on particular words during the presentation of a list of words. The subjects’ task in this procedure is to detect repetitions within a list of 60 words. While 6 words are actually repeated within the list, there are also 6 homonyms, 6 associates, 6 synonyms and 6 randomly chosen neutral words. If a subject encodes
320
L.AIRD
s.
(‘I-RhiAK
primarily the acoustic features of the words, he is liable to make several false recognitions of homonyms as repetitions; if he encodes associatively, he may make associative errors, etc. The results for Korsakoff patients, for normal controls, and for S.S. [3] can be seen in Table 2. The test was given twice to S.S. on two separate occasions and the data represent the average of these two sessions which deviated only slightly (no more than one error in Table 2. Mean number of false recognitions as a function of the type of relationship previously presented word, with repeats representing correct responses
rclationsllip l’aticntr;
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either direction for any category) from one test to the next. As can be seen, S.S.‘s performance on this test parallels that of the Korsakoff patients, a result not expected on the basis of the distractor tasks. However. it must be emphasized that this test represents an overload of information, presented rapidly, under instructions to detect repetitions, not to try to rehearse and maintain information for later recall. Cueing tasks. A second way to measure the extent to which patients encode and retain supraspan amounts of verbal information involves determining whether cueing by semantic category will facilitate retrieval of lists of words. Instances in which such cueing aids retrieval represent evidence that the words in the list were linked by semantic categories during encoding and storage. CLRMAK et a/. [3] found that cueing KorsakoE patients fol 8 words in memory, by giving them the 4 categories to which the words belonged (both prior to presentation and immediately after), led to a “decrease” in recall, relative to a simple free recall task. However, when a 1 min delay was inserted between the end of list presentation and recall, free recall fell off to nearly nothing and the facilitating effect 01 cueing could then be seen (Fig. 10). The results for S.S. (shown also in Fig. 10) parallel those for the Korsakoff patients. This finding (which is the mean of two test sessions) again seems to indicate that although S.S. can spontaneously employ semantic encoding to aid his retention, utilization of such a strategy does not seem to extend the capacity of his short-term memory. DRACHMAN and ARBIT have reached much the same conclusion in their studies with bilateral hippocampal patients (20) including two post-encephalitics in addition to H.M. They too found that capacity of an otherwise useful “holding mechanism” in these patients could not be expanded through chunking procedures. Concept ,formatioti task S.S. was asked to perform a concept formation task previously described by OSCARBERMAN [21]. In this task the patient is asked to learn the concept behind a two-choice task in which the stimuli could vary in color, size, form and position. The patient is given
THE ENCODING
CAPACITY
TG
Ot
A PATIENT
WITH
AMNESIA
DUE TO ENCEPHALITIS
321
r
I
I
Delayed
lmmedla!e Recall
conditions
FIG. 10. Mean number of words recalled correctly for the Cued Recall (CR) and Free Recall (FR) conditions under Immediate and Delayed recall by S.S., Korsakoff patients, and controls. I6 trials to learn the task, but is only given feedback as to whether he is correct or incorrect on Trials 1, 6, 11 and 16. On this task the Korsakoff patients solved only 14% of the problems, alcoholic controls solved 36 “i, and normal controls solved 47 7;. S.S., on the other hand solved 69 % of the problems, better than 7 of 10 of the normals. When the patients were aided on the task by allowing them to refer back to previous outcomes (Trials I,6 or 11) as the task progressed (a so-called memory-aid condition), Korsakoff patients solved 51% of the problems, alcoholic controls 89 9:: and normals 97 ‘4. S.S. solved 100’~ of the problems under this condition. The reason why the Korsakofl’ patients performed so poorly on the standard condition of this experiment was that they perseverated on one strategy even after they had been shown that it was inappropriate. S.S., on the other hand, actively kept alive prior outcomes and was able to switch hypotheses effectively when learning that previous ones were inappropriate. When supported by memory aids the task became one of deduction and in this case S.S. was superb. It is interesting to note that MILNER [22] reports that H.M. also has little trouble with concept formation tasks. Maze leurttittg CERMAK, LEWIS, BUTTERS and GOODGLASS [23] reported that Korsakoff patients can learn and retain a finger maze, as has also been reported by MILNER, CORKIN and TEUBER for H.M. 1241, provided the maze is short. While learning takes far more trials for Korsakoff patients than it does for normals, once the maze is learned, savings from day to day are quite remarkable. It was discovered that S.S. needed as many trials to learn a 4 pt maze (12 trials) as did the Korsakoff patients and that he was unable to learn an 8 pt maze; after 25 trials he was still making as many errors as he had in the beginning of learning. However, it was also found that if the 8 pt maze were broken in half, it took S.S. 5 trials
322
LAIRD S. CFRMAK
to learn the first half, 9 trials to learn the second half, and then 10 additional trials to learn the entire maze when the two halves were rejoined. Half an hour later, S.S. took 4 trials to relearn this same 8 pt maze: 2 days later it took 5 trials to relearn; 4 days late1 it again took 5 trials; 8 days later it took 2 trials and I month later it again took 2 trials. So once S.S. learned the maze he appeared to retain it quite well although he denied, at each session, that he had ever experienced finger-maze learning before.
S.S.‘s ability to learn a 6 item paired-associate task wab quite poor when he was asked to learn it by rote. It took him 40 trials (more than many Korsakoff patients) to learn the list of stimuli and responses both of which were common words. However, S.S. profited, more than did the Korsakoff patients [25], when provided with a verbal mediating link between stimulus and response; and he was also helped by being instructed as to how to form a visual image [26] linking the two words together (Table 3). This result led directly to a series of therapeutic sessions in which attempts were made to teach S.S. meaningful information about current events and household happenings as reported by his wife
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The initial therapeutic program involved teaching S.S. 8 current events by the use of the paired-associates (P-A) technique providing him with as many verbal mediators or visual images as could be created by the staff. During each 1 hr session, held 3 times a week, S.S. was drilled on an 8 item P-A task consisting of current events such as “Who is the Vice President?“-Gerald Ford, “What problem does Nixon face?“--Watergate, “What place place, etc. (All facts that were true at the are the Bruins (local hockey team) in ?“-First time.) After 1 hr. S.S. usually was still making errors or stating that he didn’t know some answers. However, at the start of the next session using exactly the same list, S.S. always did better on the first trial than he had done on the final trials of the preceding session. This apparent consolidation always took place and became a factor upon which the therapists began to depend. Usually during the second session, S.S. mastered the list and the third session of the week was taken up with review of the current list as well as lists from the preceding week which S.S. retained at a near-100 “1 ,,,, level. Each week a new list was introduced, some including instructions his wife felt would be helpful for him to learn such as “What do you do when you enter your house?“--Put on my sweater, “What should you do first thing in the morning?“-Take a shower. interestingly enough, although S.S. could learn these instructions, as well as 50 or more current facts, he never carried them out.
I HE ENCODING
CAPACITY
OF A PATIENT
WITH
AMNESIA
DUE
TO ENCEPHALITIS
323
When he went home he never put on a sweater. If his wife said to him “What do you do when you enter the house?‘, he would reply “Put on my sweater” and then would stand there. If his wife said “Why don’t you ?” he was likely to reply “Do what?” In other words, his learning seemed to be on a sort of automatized level and what he learned was not assimilated into his previous cognitive framework. He was able to produce appropriate responses to questions, but seemed to have no cognitive awareness of what he was parrotting. Yet, 3 months after termination of this procedure the same responses were still remembered. Two other techniques of learning were attempted: First, S.S. would read a very short portion of a story and then would be quizzed about it. If the section was small enough, S.S. could answer all the queries. Then he was asked to go on to the next section and this was followed by questions as well. At this point, the same questions S.S. could answer about the first section were asked again. But, now he invariably failed to answer any of the questions correctly. The second procedure that was tried was to take him through a programmed textbook (part of an introductory psychology text). Here it was discovered that those steps which S.S. could deduce from his own prior knowledge were always answered correctly, but he could never learn to use what he had “learned” in one step to aid his analysis of subsequent steps. DISCUSSION Upon first interviewing S.S. it appeared that his memory deficit was essentially the same as that in Korsakoff patients. He was totally unable to remember current events or day-today happenings, he was disoriented in both time and space and he had retrograde amnesia which appeared even more dense than that seen in the Korsakoff syndrome. However, closer examination through the use of the tests described in this report revealed several marked differences in performance on memory and encoding tasks between S.S. and the Korsakoff patients. It was discovered that S.S. could perform normally on the Peterson distractor task, was normally influenced by the effects of interference on this task, displayed a release from proactive interference following taxonomic category-shifts during the course of the task (something Korsakoff patients do not do), and processed information rapidly. In addition, his ability to recall a motor movement after a short period of distraction was still intact. S.S. was also normal on the Oscar-Berman concept-formation task which demanded that patients be able to remember the outcomes of prior hypotheses in order to formulate new ones, again something Korsakoff patients do poorly. The only type of material for which S.S. showed a recall deficit following distraction were the non-verbalizable Vanderplas and Garvin random shapes. For this material S.S. showed a recall deficit similar to that found for Korsakoff patients. On all other tasks, S.S.‘s performance more nearly paralleled the Korsakoff patients than it did the normals. He made more false recognitions of homonyms and associates of correct responses than did the normals on the false recognition task and he was worse following cueing for a supraspan serial list than he was if allowed to recall the list freely. In both these instances his deficit in performance was precisely the same as had been the deficit for Korsakoff patients. In addition, S.S. was unable to learn simple mazes as rapidly as normals and was totally unable to learn a complex, 8 choice point maze unless it was
324
LAIRD S. CERMAK
learned in parts. However, once the combined parts were learned as a whole, S.S. retained solution of the maze over a 1 month period, while denying he had ever seen it. Finally. paired-associate learning was impaired unless mediating or visual imagery cues were provided in which case S.S. profited more than did the Korsakoff patient>. The common factor to all the tests on which S.S. succeeds is that they are verbal and hix short-term memory capacity is not overloaded. Under these conditions S.S. succeeded, where Korsakoff patients failed. The reason for this success could simply lie in the fact that S.S. is so intelligent, but that seems unlikely because two KorsakoL‘f patients tested by the Boston VA group have had I.Q.‘s greater than 120 yet performed no better than the other Korsakoffs. Furthermore, intelligence would not account for S.S.‘s normal “rate” of processing. A more plausible alternative lies in the fact that S.S. is keenly aware of his memory deficit and is highly motivated to seek ways during testing to overcome his deficit. Alcoholic Korsakoff patients, on the other hand, are usually less concerned about their deficit and are passive about trying to overcome it. It appears that S.S. is capable of performing enough semantic analysis to bridge a short distractor interval but, despite his desire, he is simply unable to consolidate any of this information into his permanent memory. Even after extensive rehearsal, as that performed in the therapy program, S.S. seemed not to have incorporated the new information into a logical, coherent, cognitive framework. This inability to incorporate new information into a permanent memory is, of course, the same problem as that suffered by Korsakoff patients. However, this report has shown that the strategy S.S. uses in trying to overcome this deficit is different from that used by Korsakoff patients in that it allows him to perform certain tasks normally despite his overall deficit. Since other reports of encephalitic patients by STARR and PHILLIPS [lo] and LHERMITTE and SIGNORET [II] have found similar performances on tasks identical, or similar, to the ones reported here it could be that these abilities are characteristic of some encephalitic patients. However, it would be incorrect to generalize from the case of S.S. to all other post-encephalitic amnesias for, while Korsakoff patients usually all sutfer from lesions in the same general arca of the brain (midline diencephalic), there are no guarantees that the encephalitic virus will attack one and the same specific area in all patients. The damage suffered by S.S. appears to be largely bilateral cortical damage with probable bilateral hippocampal involvement. It is most likely the case that the area of the brain affected by the virus is far niore important in determining the behavioral deficits exhibited by an encephalitic patient than is the nature of the patient’s disease. In fact, a second postencephalitic patient brought to the attention of the Boston V.A. Hospital research staff and diagnosed as having primarily subcortical damage, performed in precisely the same way as the Korsakoff patients on all tests of memory and encoding described in this paper. Still other post-encephalitic patients display absolutely no memory or encoding deficits whatsoever. Thus, although it would be impossible to generalize from S.S. to all other pustencephalitics, the existence of M.K. [lo] and other similar patients [1 l] suggests that at least some post-encephalitic amnesic patients display a type of amnesia different from that shown by alcoholic Korsakoff patients. Based on some of the similarities pointed out in this paper, it might be hypothesized that these patients display a pattern more nearly like that displayed by bilateral hippocampal patients than by Korsakoff patients precisely because these particular post-encephalitic patients suffer from bilateral hippocampal rather than deep-midline area, damage. Bilateral hippocampal damage may leave the patient more “aware” of his deficit than is the case for the patient with midline damage.
TuE ENCODINOCAPACITYOF A PATIENTWITH AMNESIADUE TO ENCEPHALITIS
325
This is certainly true of S.S., and has also been reported to be true of H.M. [22]. This very ‘Lawareness” might conceivably underlie the concentration shown by these patients in their attempts to retain material in short-term memory. Korsakoff patients, on the other hand, are often totally unaware of their deficit and, as a consequence, passive in their attempts to overcome it. This may account for their slower speed of processing and poorer analytic abilities. At any rate, the results of the present investigation into the memory deficit of a post-encephalitic patient certainly suggest that it is unwise to generalize from the findings obtained by testing one type of amnesic to all types of amnesia. Effort might better be concentrated upon delineating these different “types” more precisely than has been the case thus far. Acknowledgement-This research was supported in part by an NIH Grant AA-00187 to Boston University School of Medicine. I wish to thank the following people for their assistance in the preparation of this manuscript: Drs. NELSON BUTTERS, SUZANNE CORKIN, HAROLD GOODGLASS, FELIC~A HUPPERT, MARLENE OSCAR-BERMAN, MALCOLM PIERCY, H.-LUKAS TEUBER and EDGAR ZURIF. I also extend appreciation to DAVID DELUCA, LYNN REALE and SUSAN TARLOW for their help in collecting information on this patient.
REFERENCES 1. CERMAK, L. S., BUTTERS, N. and G~~DC+LASS,H. The extent of memory loss in Korsakoff patients. Neuropsychologia 9, 307-315, 1971. 2. CERMAK, L. S. and BUTTERS, N. The role of interference and encoding in the short-term memory deficits of Korsakoff patients. Neuropsychologia 10,89-96,1972. 3. CERMAK, L. S., BUTTERS, N. and GERREIN, J. The extent of the verbal encoding ability of Korsakoff patients. Neuropsychologia 11,85-94,1973. 4. CERMAK, L. S., BUTTERS, N. and MOREINES, J. Some analyses of the verbal encoding deficit of alcoholic Korsakdff patients. Brain Lang. 1,141-150, 1974. 5. BADDELEY. A. D. and WARRINGTON, E. K. Amnesia and the distinction between long and short-term memory. j. verb. Learn. verb. Behav: 9, 176189, 1970. 6. WARRINGTON, E. K. and WEISKRANTZ, L. An analysis of short-term and long-term memory defects in man. In The Physiological Basis of Memory, J. A. DEUTSCH (Editor). Academic Press, New York, 265-295, 1973. 7. WARRINGTON, E. K. and WEISKRANTZ, L. Organizational aspects of memory in amnesic patients. Neuropsychologia 9, 67-73, 1971. 11,159-165, 8. BADDELEY, A. D. and WARRINGTON, E. K. Memory coding and amnesia. Neuropsychologia 1973. 9. BUTTERS, N. and CERMAK, L. S. Some comments on Warrington and Baddeley’s reports of normal shortterm memory in amnesic patients. Neuropsychologia 12,283-285, 1974. 8, 10. STARR, A. and PHILLIPS, L. Verbal and motor memory in the amnestic syndrome. Neuropsychologia 75-88, 1970. et differentiation des syndromes 11. LHERMITTE, F. and SIONORET, J. C. Analyse neuropsychologique amnesiques. Rev. Neural. 126, 161-178, 1972. 12. MILNER, B. Amnesia following operation on the temporal lobes. In Amnesia, C. W. M. WHITT~ and 0. L. ZANCWILL (Editors.). Butterworths, London, 1966. 13. WICKENS, D. D. Encoding categories of words: An empirical approach to meaning. Psychol. Rev. 77, 1-15, 1970. 14. DELucA, D., CERMAK, L. S. and BUTTERS, N. An analysis of Korsakoff patients’ recall following varying types of distractor activity. Neuropsychologia 13, 271-279, 1975. 15. SIDMAN, M., STODDARD, L. T. and MOHR, J. P. Some additional quantitative observations of immediate memory in a patient with bilateral hippocampal lesions. Neuropsychologia 6,245-254,1968. 16. CERMAK, L. S. and UHLY, B. Short-term motor memory in Korsakoff patients. Percept. Mot. Skills 40, 275-281, 1975. 17. OSCAR-BERMAN, M., GOODGLASS, H. and CHERLOW, D. G. Perceptual laterality and iconic recognition of visual materials by Korsakoff patients and normal adults. J. camp. physiol. Psychol. 82, 316-321, 1973. 18. BUTTERS, N., CERMAK, L. S., JONES, B. and GLOSSER, G. Some analyses of the information processing and sensory capacities of alcoholic Korsakoff patients. In Experimental Studies of Alcohol Intoxication and Withdrawal, M. G. GROSS (Editor). Plenum Press, New York, 1975.
326
LAIKD
s.
CFKhlAK
B. J. False recognition by implicit verbal responses. J. exp. Psychol. 70, 122-12Y, 1965. 19. UNDERWOOD, complex. Arch. Neural. 15, 52-62, 1966. 20. DRACHMAN, D. A. and ARBIT, J. Memory and the hippocampal testing and focusing behavior during concept formation by amnestic 21. OSCAR-BERMAN, M. Hypothesis Korsakoff patients. Nertropsychologiu 11, 191-198, 1973. B. Disorders of memory after brain lesions in man. Preface: Material-specitic and generalized 22. MILNER, memory loss. Neuropsychologia 6, 175-179, 1968. in performance 23. CERMAK, L. S., LEWIS, R., BUYERS, N. and GOODGLASS, H. Role of verbal mediation of motor tasks by Korsakoff patients. Percept. Mot. Skills 37, 259-262, 1973. B., CORKIN, S. and TELJBER, H.-L. Further analysis of the hippocampal amnesic syndrome. 24. MILNER, Neuropsychologiu 6,267-282, 1968. Cortex 11, 163.-169, 1975. 25. CERMAK, L. S. Imagery as an aid to retrieval forKorsakoffpatients. as a mnemonic aid after left temporal lobectomy: Contrast between matella 26. JONES, M. K. Imagery specific and generalized memory disorders. Neuropsyrhologirr 12, 21-30, 1974.
Deutschsprachige
Zusammenfassunp;:
i:in Kraiiker. der a? ei?er Amqesie
infnlge Encepahlitis
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, die Faktnren herauszufi 7dl^i, ciir- EI~ der ~~763~~tnisstHrune beteiligt sind. 'Cp z*:irrte sic;:! , i!aP diesel, icranke fShi:: war, verbale
I tinr!natioEor!zu analvsieren,
verplei
chbar mit einem
CPs:.nd?n. ‘.'i?Pi:,r-!ii*: war ey imsta,?de, fiir eine kllrze Sit rine bcif're~~~zte iGenRe an Informationsmaterial zu be1ialter;.Dies i'elan&Taber r.ur so lange, bis eine weit:pre Infnrmati,), aufirer.,Tmmen wurde. verschwar?d
dir
vorherige
GedZchtnis
vollkommen.
nicilt konsolidiert nis zu eelaqpen. mationsmaterial
IF diesem kugenblick
Information
in seinem aktuellen
Demnach scheint die Information zu werden ll?d irl das l,a~~~i.jt~ed~cht-
Ernsthafte
A=strenellneen, dsr: Infor-
2~7 konslidiarcn (mit
;'i
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1976, Vol. 14, pp. 31 l-326. Pergamon Press. Printed in England.
THE ENCODING CAPACITY OF A PATIENT AMNESIA DUE TO ENCEPHALITIS
WITH
LAIRD S. CERMAK* Psychology Service, Boston Veterans Administration Hospital and Aphasia Research Unit, Neurology Department, Boston University School of Medicine, Boston, Mass. 02118, U.S.A. (Received 16Jwre 1975) Abstract-A patient with amnesia due to encephalitis was examined in an effort to identify the factors that might contribute to his memory disturbances. It was discovered that this patient had the ability to analyze incoming verbal information on a level comparable to that achieved by normals. Furthermore, this ability enabled him to retain a limited amount of information for a brief interval, but, as soon as further information was introduced, it appeared to displace completely the older information in his working memory. As a consequence, information never
seemed to be consolidated into permanent, long-term, memory. Several attempts to increase the amount of information that could be consolidated (e.g. through use of visual imagery, verbal mediation, etc.) were attempted with promising, yet limited, results. INTRODUCTION EXPERIMENTS designed to assess the short-term memory and encoding capabilities of amnesic patients have often produced quite disparate results. On the one hand, there are reports that demonstrate rather dramatic deficits in the ability of amnesic patients to remember verbal information for even very short periods of time [l, 21. These reports have generally concluded that this deficit can be attributed to the amnesic patients’ inability to encode spontaneously the semantic properties of information [3, 41. Meanwhile, reports that do not find these same short-term memory [5, 61 or encoding [7, 81 deficits in amnesic patients, have concluded that the amnesic syndrome represents an inability to “retrieve” information from long-term memory rather than an initial deficit in encoding or an inability to consolidate material into memory. One possible reason why these differential results have been obtained is that two different types of amnesics have been under investigation. Data favoring short-term retention and encoding deficits has come primarily from testing a population consisting solely of alcoholic Korsakoff patients, while the data favoring a retrieval deficit has been gathered from a “mixture” of amnesic patients including post-encephalitics, a case of CO2 poisoning and some Korsakoff cases. It has been suggested [9] that before any further generalizations about “amnesia” can be made, those tests which have demonstrated deficits in alcoholic Korsakoff patients must be given to other types of amnesics in the exact manner in which they were originally presented. In particular it would appear to be desirable to give these tests to post-encephalitic patients because, as previous reports have suggested [lo, 111, these patients are most likely to differ from the alcoholic KorsakofY patient. The present report provides such an analysis in the case of a post-encephalitic patient who is unique not only because of the extreme density of his
“Reprint requests may be sent to: Laird S. Cermak, Psychology Service, Boston VA Hospital, Huntington Ave., Boston, Mass., 02130. U.S.A. 311
150 So.
312
LAIRD S. CERMAK
amnesic syndrome but because he has remained an extremely intelligent, highly motivated individual despite his deficit. Also, since the clinical picture of this patient suggests bilateral hippocampal involvement, several parallels to results obtained with MILNER’S [12] patient, H.M., can be drawn wherever similar experiments have been performed. ln addition, a variety of therapeutic techniques were attempted with this patient and the results of these attempts have provided additional insight into the amnesic syndrome. CASE
HISTORY
S.S. is a 44 yr old male physicist who was in good health until August 17, 1971 when he developed specific malaise, fever and a headache. He was initially evaluated at the Waltham Hosoital and then transferred to the Peter Bent Brigham Hospital where a diagnosis of herpes simplex encephaliiis was made. Examination of CSF revealed increased pressure, 180 mg% protein with increased gamma globulin fraction (31 x) and 58 mononuclear cells. A left temporal biopsy was performed and the culture was positive for herpes simplex. In addition, a left frontal Ommaya shunt, which entered the left frontal horn, was inserted during the operation. The patient remained in a coma for approximately one month during which time he often ran a high fever (106-108”) with occasional seizures. Upon regaining consciousness the patient had a right hemiparesis, a language disturbance described as incoherent speech and amnesia. At discharge, six weeks later, his right hemiparesis and language disorder had cleared entirely, but the amnesic disturbance remained. Sometime during the 2 weeks between regaining consciousness and discharge the patient was given the Wechsler memory scale and it was discovered that his M.Q. was 50. On December 12, 1971, S.S. was readmitted to the Peter Bent Brigham Hospital for re-evaluation. A pneumoencephalogram performed at this time revealed dilation of the lateral ventricles and third ventricle. There was marked atrophy of the left temporal lobe, some atrophy of the right temporal lobe and possible atrophy of the thalamus. A brain scan showed uptake in the left temporal and left frontal regions with no change from 9/22/71. At this time his M.Q. had risen to 71 and his I.Q. was found to be 112. His wife reports that his I.Q. had been above 145 prior to the onset of his illness and this is consistent with his educational level (M.S. in physics) and occupational position (President of a small optical firm). At this time the patient denied having a memory problem, but showed anxiety in moments of failure. On October 11, 1973, the patient was referred to the Boston VA Psychology Service for evaluation and possible treatment of his memory disorder. He was subsequently admitted to the hospital October 17, 1973, for intensive observation and psychological testing. Hc remained at the hospital for two weeks and thercafter was seen 3 times a week by the Psychology Service as an outpatient for approximately 9 months. During his stay in the VA Hospital a neurologic examination was performed. Anosmia was demonstrated and there was evidence of a left ptosis and a pupil that was less reactive to light on the left side. There was decreased movement of the left eye to medial and superior directions, but the remainder of the examination was normal. A brain scan again showed uptake over the left periphery in the anterior view. An EEG revealed left mid-posterior abnormalities with lesser left anterior disturbance. I.Q. at this time was found to be 133 (Verbal I.Q. = 130; Performance I.Q. = 133), and his M.Q. was 83.5,both improvements from previous testing of 12171. The Boston Diagnostic aohasia battery was given and no imoairment was found. In addition. no impairment was found on aparietal iobe battery.Apparently the only residual behavioral deficit still remaining as a consequence of S.S.‘s herpes simplex encephalitis is a marked memory deficit. S.S. is still unable to remember day-to-day even&, he is disoriented in time and space, and has considerable retrograde amnesia (for instance he was unable to describe his honeymoon from the early forties or his college days) yet remembers many important national events that occurred prior to his illness. During testing S.S. demonstrated considerable insight into his memory disorder. and listed it as his sole difficulty. He was attentive and motivated, consistently seeking any cues to aid him during retrieval. He still evidenced some anxiety when unable to retrieve information but often covered hi, anxiety with flippant remarks which proved to be quite perseverative both within and between sessions. Testing was carried out over a period of 9 months and the results of this testing are reported here.
RESULTS The results of the Wechsler Adult Intelligence Scale (WAIS) examination and the Wcchslcr Memory Scale are reported in Table I. The rest of the tests that were given to S.S. have not been nearly as well documented as the WAIS; for that reason, the nature of these tests, and S.S’s performance on them relative to Korsakoff patients and normal controls, will be reported in greater detail.
THE ENCODtNG
CAPACITY
OF A PATIENT
WITH
AMNESIA
DUE TO ENCEPHALmS
313
Table 1. Wechsler adult intelligencescale and Wechsler memory scale subtest scores for S.S.
Scaled
Raw
UAIS test
Score
Informat ion Comprehension Arithmetic Similarities Digit Span Vocabulary
Score 14 14 14 19 13 17 -
25 22 16 25 13 76 Verbal Score
Digit Symbol Picture Completion ;jloc!c Design Picture Arrangement Object Assembly
=
130 I0
71
=
133 IQ
162
=
133 Ic,
16 12 18 14
73 16 48 30 33
II
Performance Full
91
Score
Scale Score
Rat, Score
1%!eci:sler I:emnry Information Orientation Hental Control Memory Passages Digits Total Visual Reproduction Associate Learning
3 3 6
a
14 7 5.5
Total Raw Score
46.5
Corrected Score
86.5
x.q.
53.5
Short-term memoty’ distractor tasks Recall of CCC’s, WWW’s ad sirzgle words. The distractor technique and its several variations have been described previously by several investigators [I, 5, 91. In the present instance, either a consonant trigram (CCC), a word triad (WWW), or a single word was presented visually to the patient for 2 sec. Immediately patient was required to count backward by threes from experimenter. This number differed from trial to trial and was paced at a rate of one number per second. After the
following this presentation the a number given to him by the the patient’s counting backward patient counted backward for an
LARD
314
S. CERMAK
interval varying from 3 to 18 set, he was asked to recall the material to be remembered. This procedure continued with the same type of material until the patient had received 5 trials at each retention interval (0, 3, 9 and 18 sec.). S.S. was tested 3 times on each type of material and the average of these 3 times is reported here. His performance on CCC’s, compared with the previously reported [I] performance for Korsakoff patients and for normal controls, is shown in Fig. I. The same comparisons for WWW’s are shown in Fig. -! and. for single words, in Fig. 3. As can be seen.
20
;o 0
L_-_-+ -
?
____l_i_l
Retentionintend,
i:
cot
FIG. 1. Percentage of CCC’s (consonant trigrams) recalled by S.S., Korsakoff and normal controls (N) following 0, 3, 9. or 18 sec.
patients (K),
FIG. 2. Percentage of word trigrams (WWW’s) recalled by S.S., Korsakoff patients (K), and normal controls (N) following 0, 3, 9 or 19 see of distraction.
THE
ENCODlNG
CAPACITY
OF A PATIENT
WITH
f+?temon
F’IG. 3. Percentage
AMNESIA
DUE
315
TO ENCEPHALITIS
interval, see
of single words recalled by S.S., Korsakoff patients controls (N) following 0, 3, 9 or 18 set of distraction.
(K), and normal
S.S. performed normally on all these tests despite having a more demanding activity than did the Korsakoff patients and the controls of the previous study, always permitted to start from 100 and to count backwards by twos.
distractor who were
Interference tasks. Previous research [2] has shown that alcoholic Korsakoff patients are more susceptible to the effects of proactive interference during their performance on the distractor task than are normal controls. Therefore, despite his normal performance on the task, it was decided to test the susceptibility of S.S. to the effects of increasing or decreasing interference within this task. This was accomplished in two ways: by massing the trials through the use of a short (6 set) intertrial interval and comparing this with distributed trials having a 1 min intertrial interval ; or by having every other trial preceded by material from either the same conceptual class (words or CCC’s) as the critical material or from the other class. In other words, when recall of CCC’s was investigated only recall from every other trial was counted, some of these trials being preceded by a trial also containing CCC’s, a high Proactive Interference (PI) condition, and some preceded by trials containing WWW’s (low PI condition). A more detailed description of both the massed vs distributed and high vs low interference tasks can be found elsewhere [2]. It suffices here to say that S.S. performed above even our normal controls on both these tasks. As Figs. 4 and 5 show, he was somewhat affected by increased interference, but the effects were no more than those found for the normal subjects. Release from PI. WICKENS [13] has shown that, for normal subjects, the proactive interference that is generated across successive trials by the distractor task can be eliminated, and recall can be increased, when material from a class differing from that of the preceding material is introduced (Fig. 6). CERMAK, BUTTERS and MOREINES [4] have shown that this “release from proactive interference” does not occur for Korsakoff patients (Fig. 7) when the critical material is drawn from different taxonomic categories (e.g. animals, vegetables,
31h
LAIRD
tT3
100
s.
CERhfAK
tiorsakoff
/
6”
6’1
6”
Retention FIG.
interval
4. Percentage of CCC’S and WWW’S recalled by S.S., Korsakoff patients. and control\ as a function of the length of the intertrial interval.
.-.
.
.--__
-0.
\
\
z
& a
50
.
‘1 ‘Y \
.\ \
‘\
\
\
‘-3
\
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E
‘L.,
\ \ .-.
CCC
‘\
.
‘\ l\.
After
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\ \
AfterCCC After
WWW
After
WWW
After
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-\
\
‘0 \ \ \
40
\ \ \ \
30
\ \
.---------.
AfterwW’&
20
j,, _. -’
1
0 5
9 Relention
----
Control
----SS
Korsakoff
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ial,
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FIG. 5. Percentage of WWW’s recalled by S.S.. Korsakoff patients, and controls followmg high and low PI conditions and retention intervals of 3. 9 and 18 sec.
tools and articles of clothing). Since S.S. performed so well OII the distractor task it wnh decided to test whether or not he was encoding information semantically. This was tested by determining whether or not a change in taxonomic categories resulted in a release from proactive interference for S.S. in the way it does for normals.
THE
ENCODING
CAPACITY
IO0
OF A PATIENT
Taxonomic
WITH
categories
control
AMNESIA
DUE
317
TO ENCEPHALITIS
group
t
Trials FIG.
6. Probability
of recall for normal controls following a shift in taxonomic Taxonomic
100
categories
Korsakoff
categories.
group
t
Trials
FIG. 7. Probability of recall for Korsakoff patients following a shift in taxonomlc categories.
In the actual task, 3 words from one category (e.g. animals) were presented on each of the first 4 trials of a distractor task. Then on the Fifth Trial 3 words from another category (e.g. vegetables) were presented. S.S. was tested in this manner for three different taxonomic shifts; the results can be seen in Fig. 8. It can reasonably be inferred that S.S. does encode spontaneously by taxonomic category, and it may be this ability that accounts for his superior performance on the distractor task relative to the Korsakoff patients. Verbal recall vs non-verbal recall. Although S.S. had normal distractor task recall for verbal material, it did not necessarily follow that his non-verbal recall would also be normal. Therefore, S.S. was given a test of his non-verbal memory similar to the preceding tests except that it involved recognition rather than recall. This test, which has also been described elsewhere [14], involves showing the patient an irregular geometric form (Vanderplas
FIG. 8. Probatxllty
of recall for S.S. following
a shift in taXouomtc
categorle\
and Garvin randomly generated shapes) and then asking him to perform either a verbal distractor task (counting backward) or. in another condition, a non-verbal distractor task (tracking musical notes). At the end of a 20 see retention interval the patient is shown ;I second stimulus and asked whether it is the “same as” or “different from” the first. A verbal (WWW) recognition test is also given. using the same distractor conditions so that recognition scores for non-verbal materials can be compared to those for verbal material. Korsakoff patients arc impaired on the verbal task followed by verbal distraction and are normal on the verbal task followed by non-verbal distraction. On the other hand, the nonverbal recall of Korsakoff patients is impnircd regardless of the nature of the distractor task, though not quite to the same extent a> their verbal recall following verbal distraction. The same procedures wcrc used with S.S. in order to determine whether or not his nonverbal retention matched his verbal retention. As cm be seen in Fig. 9, S.S.‘s non-verbal recall was dramatically worse than his verbal recall and was far below the normal\. III
E&l 0 -
Korsakoff Control S.S.
l-l
v-v
FIG. 9. Percentage
ol’ CCC’S
non-verbal
NV-NV
NV-V
“_-NV
StltTIUlUS ~Otsrial
-
distroctw
task
(V) and random forms (NV) recognized following verbal by S.S.. Korsakoff patients. and control\.
(NV) distraction
(V) 01
I HE ENCODING
CAPACITY
OF A PATIENT
WITH
AMNESlA
DUE
‘I’0 ENCEPHALITIS
319
fact it was on a par with that of the KorsakolI patients. Apparently, whatever form of encoding is available to normals for the retention of non-verbal information (possibly some form of imagery), it is not available to, or used by S.S. A comparable finding has also been reported for H.M. by SIDMAN, STODDARD and MOHR [15]. H.M. also had the ability to retain verbal material over an undisrupted retention interval of up to 40 set, but could not do the same for non-verbal material. It must be emphasized again, however, that such an undisrupted retention interval does not in any way prevent verbal rehearsal during the interval. Motor nremory. Interestingly enough what does seem to be available to S.S. is the ability to retain a motor movement, at least over a period of IO-20 sec. It has been discovered [ 161 that Korsakoff patients lose their recollection, more rapidly than normals, of how far to pull a bar. On this test the patient’s hand is placed on a sliding bar while he is blindfolded. The experimenter moves the bar a predetermined distance and returns it with the patients’ hand to the start position. Either 10 or 20 set later the patient is required to return the bar to the same position as that just shown him. S.S. performed this test as well as the best normal subject, which may mean that whatever cues normals use to enable them to perform this task may also be available to S.S.
Speed
of processit~g
One explanation for the impoverished encoding by Korsakoff patients has been advanced by OSCAR-BERMAN,GOODGLASSand CHERLOW [17] who found that the Korsakoff patients’ visual recognition thresholds for words and patterns was far higher than in normals, i.e. the duration of presentation had to be longer before the Korsakoff patients could identify either type of material than was the case for normals. These investigators also found that the interval between the presentation of a target stimulus and a second (masking) stimulus had to be longer in order for Korsakoff patients to identify the target stimulus than it had to be for normals. S.S.‘s threshold measure and critical inter-stimulus interval (ISI) fell within the normal range although in both cases he was on the low end (high threshold and long 1%) of this range. On a second speed of processing task recently developed by GLOSSER [18], Korsakoli’ patients were found to be normal in their ability to detect instances in which a particular number was presented to them through headphones, but deficient in their ability to detect instances in which a particular combination of numbers appeared dichotically (a 5 in one ear and a 9 in the other), at least when the interpair interval was brief (I.2 set). When this same interval was increased to 2 set, the performance of the Korsakoff patients approached normality. This seemed to indicate that Korsakoff patients need more processing time, perhaps to read out what is in their sensory register, than do normals. As might by now be expected, S.S.‘s performance on Glosser’s test was perfectly normal, in fact, superior to most normals. Evidently S.S. is capable of normal analysis at a normal speed. In light of this the results of the next set of encoding tasks were somewhat surprising.
False recogt~ith. UNDERWOOD 1193has developed a technique that can be used to measure the type of encoding subjects perform on particular words during the presentation of a list of words. The subjects’ task in this procedure is to detect repetitions within a list of 60 words. While 6 words are actually repeated within the list, there are also 6 homonyms, 6 associates, 6 synonyms and 6 randomly chosen neutral words. If a subject encodes
320
L.AIRD
s.
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primarily the acoustic features of the words, he is liable to make several false recognitions of homonyms as repetitions; if he encodes associatively, he may make associative errors, etc. The results for Korsakoff patients, for normal controls, and for S.S. [3] can be seen in Table 2. The test was given twice to S.S. on two separate occasions and the data represent the average of these two sessions which deviated only slightly (no more than one error in Table 2. Mean number of false recognitions as a function of the type of relationship previously presented word, with repeats representing correct responses
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either direction for any category) from one test to the next. As can be seen, S.S.‘s performance on this test parallels that of the Korsakoff patients, a result not expected on the basis of the distractor tasks. However. it must be emphasized that this test represents an overload of information, presented rapidly, under instructions to detect repetitions, not to try to rehearse and maintain information for later recall. Cueing tasks. A second way to measure the extent to which patients encode and retain supraspan amounts of verbal information involves determining whether cueing by semantic category will facilitate retrieval of lists of words. Instances in which such cueing aids retrieval represent evidence that the words in the list were linked by semantic categories during encoding and storage. CLRMAK et a/. [3] found that cueing KorsakoE patients fol 8 words in memory, by giving them the 4 categories to which the words belonged (both prior to presentation and immediately after), led to a “decrease” in recall, relative to a simple free recall task. However, when a 1 min delay was inserted between the end of list presentation and recall, free recall fell off to nearly nothing and the facilitating effect 01 cueing could then be seen (Fig. 10). The results for S.S. (shown also in Fig. 10) parallel those for the Korsakoff patients. This finding (which is the mean of two test sessions) again seems to indicate that although S.S. can spontaneously employ semantic encoding to aid his retention, utilization of such a strategy does not seem to extend the capacity of his short-term memory. DRACHMAN and ARBIT have reached much the same conclusion in their studies with bilateral hippocampal patients (20) including two post-encephalitics in addition to H.M. They too found that capacity of an otherwise useful “holding mechanism” in these patients could not be expanded through chunking procedures. Concept ,formatioti task S.S. was asked to perform a concept formation task previously described by OSCARBERMAN [21]. In this task the patient is asked to learn the concept behind a two-choice task in which the stimuli could vary in color, size, form and position. The patient is given
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FIG. 10. Mean number of words recalled correctly for the Cued Recall (CR) and Free Recall (FR) conditions under Immediate and Delayed recall by S.S., Korsakoff patients, and controls. I6 trials to learn the task, but is only given feedback as to whether he is correct or incorrect on Trials 1, 6, 11 and 16. On this task the Korsakoff patients solved only 14% of the problems, alcoholic controls solved 36 “i, and normal controls solved 47 7;. S.S., on the other hand solved 69 % of the problems, better than 7 of 10 of the normals. When the patients were aided on the task by allowing them to refer back to previous outcomes (Trials I,6 or 11) as the task progressed (a so-called memory-aid condition), Korsakoff patients solved 51% of the problems, alcoholic controls 89 9:: and normals 97 ‘4. S.S. solved 100’~ of the problems under this condition. The reason why the Korsakofl’ patients performed so poorly on the standard condition of this experiment was that they perseverated on one strategy even after they had been shown that it was inappropriate. S.S., on the other hand, actively kept alive prior outcomes and was able to switch hypotheses effectively when learning that previous ones were inappropriate. When supported by memory aids the task became one of deduction and in this case S.S. was superb. It is interesting to note that MILNER [22] reports that H.M. also has little trouble with concept formation tasks. Maze leurttittg CERMAK, LEWIS, BUTTERS and GOODGLASS [23] reported that Korsakoff patients can learn and retain a finger maze, as has also been reported by MILNER, CORKIN and TEUBER for H.M. 1241, provided the maze is short. While learning takes far more trials for Korsakoff patients than it does for normals, once the maze is learned, savings from day to day are quite remarkable. It was discovered that S.S. needed as many trials to learn a 4 pt maze (12 trials) as did the Korsakoff patients and that he was unable to learn an 8 pt maze; after 25 trials he was still making as many errors as he had in the beginning of learning. However, it was also found that if the 8 pt maze were broken in half, it took S.S. 5 trials
322
LAIRD S. CFRMAK
to learn the first half, 9 trials to learn the second half, and then 10 additional trials to learn the entire maze when the two halves were rejoined. Half an hour later, S.S. took 4 trials to relearn this same 8 pt maze: 2 days later it took 5 trials to relearn; 4 days late1 it again took 5 trials; 8 days later it took 2 trials and I month later it again took 2 trials. So once S.S. learned the maze he appeared to retain it quite well although he denied, at each session, that he had ever experienced finger-maze learning before.
S.S.‘s ability to learn a 6 item paired-associate task wab quite poor when he was asked to learn it by rote. It took him 40 trials (more than many Korsakoff patients) to learn the list of stimuli and responses both of which were common words. However, S.S. profited, more than did the Korsakoff patients [25], when provided with a verbal mediating link between stimulus and response; and he was also helped by being instructed as to how to form a visual image [26] linking the two words together (Table 3). This result led directly to a series of therapeutic sessions in which attempts were made to teach S.S. meaningful information about current events and household happenings as reported by his wife
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The initial therapeutic program involved teaching S.S. 8 current events by the use of the paired-associates (P-A) technique providing him with as many verbal mediators or visual images as could be created by the staff. During each 1 hr session, held 3 times a week, S.S. was drilled on an 8 item P-A task consisting of current events such as “Who is the Vice President?“-Gerald Ford, “What problem does Nixon face?“--Watergate, “What place place, etc. (All facts that were true at the are the Bruins (local hockey team) in ?“-First time.) After 1 hr. S.S. usually was still making errors or stating that he didn’t know some answers. However, at the start of the next session using exactly the same list, S.S. always did better on the first trial than he had done on the final trials of the preceding session. This apparent consolidation always took place and became a factor upon which the therapists began to depend. Usually during the second session, S.S. mastered the list and the third session of the week was taken up with review of the current list as well as lists from the preceding week which S.S. retained at a near-100 “1 ,,,, level. Each week a new list was introduced, some including instructions his wife felt would be helpful for him to learn such as “What do you do when you enter your house?“--Put on my sweater, “What should you do first thing in the morning?“-Take a shower. interestingly enough, although S.S. could learn these instructions, as well as 50 or more current facts, he never carried them out.
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When he went home he never put on a sweater. If his wife said to him “What do you do when you enter the house?‘, he would reply “Put on my sweater” and then would stand there. If his wife said “Why don’t you ?” he was likely to reply “Do what?” In other words, his learning seemed to be on a sort of automatized level and what he learned was not assimilated into his previous cognitive framework. He was able to produce appropriate responses to questions, but seemed to have no cognitive awareness of what he was parrotting. Yet, 3 months after termination of this procedure the same responses were still remembered. Two other techniques of learning were attempted: First, S.S. would read a very short portion of a story and then would be quizzed about it. If the section was small enough, S.S. could answer all the queries. Then he was asked to go on to the next section and this was followed by questions as well. At this point, the same questions S.S. could answer about the first section were asked again. But, now he invariably failed to answer any of the questions correctly. The second procedure that was tried was to take him through a programmed textbook (part of an introductory psychology text). Here it was discovered that those steps which S.S. could deduce from his own prior knowledge were always answered correctly, but he could never learn to use what he had “learned” in one step to aid his analysis of subsequent steps. DISCUSSION Upon first interviewing S.S. it appeared that his memory deficit was essentially the same as that in Korsakoff patients. He was totally unable to remember current events or day-today happenings, he was disoriented in both time and space and he had retrograde amnesia which appeared even more dense than that seen in the Korsakoff syndrome. However, closer examination through the use of the tests described in this report revealed several marked differences in performance on memory and encoding tasks between S.S. and the Korsakoff patients. It was discovered that S.S. could perform normally on the Peterson distractor task, was normally influenced by the effects of interference on this task, displayed a release from proactive interference following taxonomic category-shifts during the course of the task (something Korsakoff patients do not do), and processed information rapidly. In addition, his ability to recall a motor movement after a short period of distraction was still intact. S.S. was also normal on the Oscar-Berman concept-formation task which demanded that patients be able to remember the outcomes of prior hypotheses in order to formulate new ones, again something Korsakoff patients do poorly. The only type of material for which S.S. showed a recall deficit following distraction were the non-verbalizable Vanderplas and Garvin random shapes. For this material S.S. showed a recall deficit similar to that found for Korsakoff patients. On all other tasks, S.S.‘s performance more nearly paralleled the Korsakoff patients than it did the normals. He made more false recognitions of homonyms and associates of correct responses than did the normals on the false recognition task and he was worse following cueing for a supraspan serial list than he was if allowed to recall the list freely. In both these instances his deficit in performance was precisely the same as had been the deficit for Korsakoff patients. In addition, S.S. was unable to learn simple mazes as rapidly as normals and was totally unable to learn a complex, 8 choice point maze unless it was
324
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learned in parts. However, once the combined parts were learned as a whole, S.S. retained solution of the maze over a 1 month period, while denying he had ever seen it. Finally. paired-associate learning was impaired unless mediating or visual imagery cues were provided in which case S.S. profited more than did the Korsakoff patient>. The common factor to all the tests on which S.S. succeeds is that they are verbal and hix short-term memory capacity is not overloaded. Under these conditions S.S. succeeded, where Korsakoff patients failed. The reason for this success could simply lie in the fact that S.S. is so intelligent, but that seems unlikely because two KorsakoL‘f patients tested by the Boston VA group have had I.Q.‘s greater than 120 yet performed no better than the other Korsakoffs. Furthermore, intelligence would not account for S.S.‘s normal “rate” of processing. A more plausible alternative lies in the fact that S.S. is keenly aware of his memory deficit and is highly motivated to seek ways during testing to overcome his deficit. Alcoholic Korsakoff patients, on the other hand, are usually less concerned about their deficit and are passive about trying to overcome it. It appears that S.S. is capable of performing enough semantic analysis to bridge a short distractor interval but, despite his desire, he is simply unable to consolidate any of this information into his permanent memory. Even after extensive rehearsal, as that performed in the therapy program, S.S. seemed not to have incorporated the new information into a logical, coherent, cognitive framework. This inability to incorporate new information into a permanent memory is, of course, the same problem as that suffered by Korsakoff patients. However, this report has shown that the strategy S.S. uses in trying to overcome this deficit is different from that used by Korsakoff patients in that it allows him to perform certain tasks normally despite his overall deficit. Since other reports of encephalitic patients by STARR and PHILLIPS [lo] and LHERMITTE and SIGNORET [II] have found similar performances on tasks identical, or similar, to the ones reported here it could be that these abilities are characteristic of some encephalitic patients. However, it would be incorrect to generalize from the case of S.S. to all other post-encephalitic amnesias for, while Korsakoff patients usually all sutfer from lesions in the same general arca of the brain (midline diencephalic), there are no guarantees that the encephalitic virus will attack one and the same specific area in all patients. The damage suffered by S.S. appears to be largely bilateral cortical damage with probable bilateral hippocampal involvement. It is most likely the case that the area of the brain affected by the virus is far niore important in determining the behavioral deficits exhibited by an encephalitic patient than is the nature of the patient’s disease. In fact, a second postencephalitic patient brought to the attention of the Boston V.A. Hospital research staff and diagnosed as having primarily subcortical damage, performed in precisely the same way as the Korsakoff patients on all tests of memory and encoding described in this paper. Still other post-encephalitic patients display absolutely no memory or encoding deficits whatsoever. Thus, although it would be impossible to generalize from S.S. to all other pustencephalitics, the existence of M.K. [lo] and other similar patients [1 l] suggests that at least some post-encephalitic amnesic patients display a type of amnesia different from that shown by alcoholic Korsakoff patients. Based on some of the similarities pointed out in this paper, it might be hypothesized that these patients display a pattern more nearly like that displayed by bilateral hippocampal patients than by Korsakoff patients precisely because these particular post-encephalitic patients suffer from bilateral hippocampal rather than deep-midline area, damage. Bilateral hippocampal damage may leave the patient more “aware” of his deficit than is the case for the patient with midline damage.
TuE ENCODINOCAPACITYOF A PATIENTWITH AMNESIADUE TO ENCEPHALITIS
325
This is certainly true of S.S., and has also been reported to be true of H.M. [22]. This very ‘Lawareness” might conceivably underlie the concentration shown by these patients in their attempts to retain material in short-term memory. Korsakoff patients, on the other hand, are often totally unaware of their deficit and, as a consequence, passive in their attempts to overcome it. This may account for their slower speed of processing and poorer analytic abilities. At any rate, the results of the present investigation into the memory deficit of a post-encephalitic patient certainly suggest that it is unwise to generalize from the findings obtained by testing one type of amnesic to all types of amnesia. Effort might better be concentrated upon delineating these different “types” more precisely than has been the case thus far. Acknowledgement-This research was supported in part by an NIH Grant AA-00187 to Boston University School of Medicine. I wish to thank the following people for their assistance in the preparation of this manuscript: Drs. NELSON BUTTERS, SUZANNE CORKIN, HAROLD GOODGLASS, FELIC~A HUPPERT, MARLENE OSCAR-BERMAN, MALCOLM PIERCY, H.-LUKAS TEUBER and EDGAR ZURIF. I also extend appreciation to DAVID DELUCA, LYNN REALE and SUSAN TARLOW for their help in collecting information on this patient.
REFERENCES 1. CERMAK, L. S., BUTTERS, N. and G~~DC+LASS,H. The extent of memory loss in Korsakoff patients. Neuropsychologia 9, 307-315, 1971. 2. CERMAK, L. S. and BUTTERS, N. The role of interference and encoding in the short-term memory deficits of Korsakoff patients. Neuropsychologia 10,89-96,1972. 3. CERMAK, L. S., BUTTERS, N. and GERREIN, J. The extent of the verbal encoding ability of Korsakoff patients. Neuropsychologia 11,85-94,1973. 4. CERMAK, L. S., BUTTERS, N. and MOREINES, J. Some analyses of the verbal encoding deficit of alcoholic Korsakdff patients. Brain Lang. 1,141-150, 1974. 5. BADDELEY. A. D. and WARRINGTON, E. K. Amnesia and the distinction between long and short-term memory. j. verb. Learn. verb. Behav: 9, 176189, 1970. 6. WARRINGTON, E. K. and WEISKRANTZ, L. An analysis of short-term and long-term memory defects in man. In The Physiological Basis of Memory, J. A. DEUTSCH (Editor). Academic Press, New York, 265-295, 1973. 7. WARRINGTON, E. K. and WEISKRANTZ, L. Organizational aspects of memory in amnesic patients. Neuropsychologia 9, 67-73, 1971. 11,159-165, 8. BADDELEY, A. D. and WARRINGTON, E. K. Memory coding and amnesia. Neuropsychologia 1973. 9. BUTTERS, N. and CERMAK, L. S. Some comments on Warrington and Baddeley’s reports of normal shortterm memory in amnesic patients. Neuropsychologia 12,283-285, 1974. 8, 10. STARR, A. and PHILLIPS, L. Verbal and motor memory in the amnestic syndrome. Neuropsychologia 75-88, 1970. et differentiation des syndromes 11. LHERMITTE, F. and SIONORET, J. C. Analyse neuropsychologique amnesiques. Rev. Neural. 126, 161-178, 1972. 12. MILNER, B. Amnesia following operation on the temporal lobes. In Amnesia, C. W. M. WHITT~ and 0. L. ZANCWILL (Editors.). Butterworths, London, 1966. 13. WICKENS, D. D. Encoding categories of words: An empirical approach to meaning. Psychol. Rev. 77, 1-15, 1970. 14. DELucA, D., CERMAK, L. S. and BUTTERS, N. An analysis of Korsakoff patients’ recall following varying types of distractor activity. Neuropsychologia 13, 271-279, 1975. 15. SIDMAN, M., STODDARD, L. T. and MOHR, J. P. Some additional quantitative observations of immediate memory in a patient with bilateral hippocampal lesions. Neuropsychologia 6,245-254,1968. 16. CERMAK, L. S. and UHLY, B. Short-term motor memory in Korsakoff patients. Percept. Mot. Skills 40, 275-281, 1975. 17. OSCAR-BERMAN, M., GOODGLASS, H. and CHERLOW, D. G. Perceptual laterality and iconic recognition of visual materials by Korsakoff patients and normal adults. J. camp. physiol. Psychol. 82, 316-321, 1973. 18. BUTTERS, N., CERMAK, L. S., JONES, B. and GLOSSER, G. Some analyses of the information processing and sensory capacities of alcoholic Korsakoff patients. In Experimental Studies of Alcohol Intoxication and Withdrawal, M. G. GROSS (Editor). Plenum Press, New York, 1975.
326
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s.
CFKhlAK
B. J. False recognition by implicit verbal responses. J. exp. Psychol. 70, 122-12Y, 1965. 19. UNDERWOOD, complex. Arch. Neural. 15, 52-62, 1966. 20. DRACHMAN, D. A. and ARBIT, J. Memory and the hippocampal testing and focusing behavior during concept formation by amnestic 21. OSCAR-BERMAN, M. Hypothesis Korsakoff patients. Nertropsychologiu 11, 191-198, 1973. B. Disorders of memory after brain lesions in man. Preface: Material-specitic and generalized 22. MILNER, memory loss. Neuropsychologia 6, 175-179, 1968. in performance 23. CERMAK, L. S., LEWIS, R., BUYERS, N. and GOODGLASS, H. Role of verbal mediation of motor tasks by Korsakoff patients. Percept. Mot. Skills 37, 259-262, 1973. B., CORKIN, S. and TELJBER, H.-L. Further analysis of the hippocampal amnesic syndrome. 24. MILNER, Neuropsychologiu 6,267-282, 1968. Cortex 11, 163.-169, 1975. 25. CERMAK, L. S. Imagery as an aid to retrieval forKorsakoffpatients. as a mnemonic aid after left temporal lobectomy: Contrast between matella 26. JONES, M. K. Imagery specific and generalized memory disorders. Neuropsyrhologirr 12, 21-30, 1974.
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