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An analysis of Korsakoff patients' recall following varying types of distractor activity
Neuropsychologia,
1975,
Vol.
13, pp. 271 to 279.
Pergamon
Press.
Printed
in England
AN ANALYSIS OF KORSAKOFF PATIENTS’ RECALL FOLLOWING VARYING TYPES OF DISTRACTOR ACTIVITY DAVID
DE LUCA, LAIRD S. CERMAK*and NELSONBUTTERS
Psychology Service, Boston Veterans Administration Hospital and Aphasia Research Unit, Ncuro!ogy Department, Boston University School of Medicine, Boston, Mass 02118, U.S.A. (Received 31 August 1974) Abstract-Ten alcoholic Korsakoff patients and ten alcoholic control subjects were given several short-term memory, distractor type tasks in which consonant trigrams (verbal) and random shapes (nonverbal) were employed as the to-be-retained materials. The Korsakoff patients demonstrated a severe verbal memory deficit when the retention interval was filled with verbal distractor activity, but their retention of the same verbal material was intact when a nonverbal distractor task was used. In contrast, the Korsakoff patients’ retention of nonverbal material was impaired regardless of the nature of the distractor activity. In fact, their retention of nonverbal material was impaired even when an unfilled retention interval was used. INTRODUCTION RESEARCHdesigned to investigate the nature of the Korsakoff patients’ memory disorder has generally focused upon the difficulties experienced by these patients when attempting to retain verbal information [l]. These analyses have revealed that the major factor contributing to the Korsakoff patients’ verbal memory impairment is an inability to encode the semantic properties of verbal material [2]. The only analysis of these patients’ nonverbal memory abilities [3] indicated that Korsakoff patients have considerably less difficulty recognizing nonverbal than verbal material following verbal distractor activity [4]. However, the exclusive use of a verbal distractor task may have determined these results since recent studies [5, 61 using the short-term memory (STM) distractor technique with normal subjects have shown that the similarity between the to-be-retained material and the distractor activity is crucial in determining the amount of information loss. The Korsakoff patients’ retention of nonverbal materials may be intact only when the distractor activity differs from the to-be-remembered information (i.e. when nonverbal material is followed by a verbal distractor task), and, using the same reasoning, their verbal memory might improve when a nonverbal distractor is employed. In order to assess these possibilities, an analysis of the effect of different types of distractor activity upon the Korsakoff patients’ retention of verbal and nonverbal materials was performed.
EXPERIMENT
I
Method Subjects. Two groups of hospitalized patients were employed in the present study: ten patients diagnosed as alcoholic Korsakoffs by the Neurology Services of the Boston and Brockton VA Hospitals; and ten *Reprint requests should be sent to Laird S. Cermak, Psychology Service, Boston Veterans Administration Hospital, 150 South Huntington Avenue, Boston, Massachusetts 02130. 271
272
DAVID DELIJCA. LAIRD S. CERMAK
and NELSON BUTTERS
alcoholic control patienls who were involved in various treatment programs at the hospitals mentioned above. All of the Korsakoff patients had severe memory impairments as assessed by clinical methods. They had difficulty recalling day to day and current events (i.e., anterograde amnesia) and they had retrograde amnesias of varying severity for events which occurred prior to the onset of their illness. In contrast, the alcoholic control patients exhibited none of the clinical symptoms associated with Korsakoff’s syndrome. To insure that I.Q.‘s were all within normal range, the verbal section of the Wechsler Adult Intelligence Scale was administered to all patients participating in thisexperiment.The meanVerbal1.Q. for the Korsakoff patients was 105 (range 92-124). The mean Verbal I.Q. for the alcoholic controls was 105 (range 91-127). The Korsakoff patients had a mean age of 55 (range 45-61) as compared to a mean age of 51 (range 42-63) for the alcoholic group. Des&z. Each patient was given eight different tests, all of which were variations of the PETERSONand PETERSON[4] distractor technique. The to-be-remembered materials were visually presented consonant trigrams (verbal) and random shapes (nonverbal). Two auditory distractor tasks (one verbal and one nonverbal) and two visual distractor tasks (one verbal and one nonverbal) were paired with each of the two types of stimulus materials making a total of eight separate conditions. During test session I, retention of both verbal and nonverbal materials was tested following the two auditory distractor tasks. Patients saw the stimuli, then either counted backL3ards from 100 by two’s (verbal distractor) or tracked musical tones (nonverbal distractor) for a duration of 20 sec. During test session II verbal and nonverbal retention was tested again, but this time the distractor activity was presented in the visual modality. Patients saw the stimuli then either scanned a list for particular words (verbal distractor) or they scanned for particular “snowflake” figures (nonverbal distractor) for a period of 20 sec. The order of presentation of the verbal and nonverbal recognition tasks was randomly determined and an interval of at least three days occurred between sessions. Materials. The to-be-remembered verbal stimuli were consonant trigrams (CCC’s) with a 25% or less association value taken from Witmer’s norms [7]. The nonverbal stimuli were VANDER~LAS and GARVIN [8] computer-generated random shapes (see Fig. I). The trigrams and the random shapes were presented individually on 5 v 8 inch white cards.
FIG. 1. Examples of the random shapes used on the nonverbal memory tasks. Both auditory distractor tasks were prerecorded on a two channel Sony tape recorder and were presented through Koss Pro/4AA headphones. The verbal tape consisted of 12 individual recordings of the words “count, 100, 98, (silence), stop”. The mnverbal tape consisted of 100 musical notes each presented for 4/5 set with an interstimulus interval of 1.5 sec. The notes (high D and low D) were produced by a two-octave electric organ and were recorded randomly on either the left or right channel. A 5 s 8 inch white card with four coordinates representing all possible responses (high, low, left ear, right car) was placed in front of the patient so that he could track 9 musical tones during each delay trial by indicating octave (high or low) and ear of presentation. The two visual distractor tasks were presented within 8 x 10 in. booklets. Each page of the verbal booklet contained 96 different nouns belonging to one of four tasonomic categories (animals, cars, cities, countries). Each noun appeared 4 times throughout a typed, triple spaced, 3 page list. The nonverbal booklet was 11 pages long, each page containing 25 “snowflake” figures (see Fig. 2). A different master figure appeared at
AN ANALYSIS
OF KORSAKOFF
PATIENTS’
RECALL
FOLLOWING
VARYING
TYPES
FIG. 2. Example of the Snowflake Figures employed on the nonverbal
OF DISTRACTOR
ACTIVITY
visual distractor
213
task.
the top of each page and 3 times among the other figures on one page. The position of these 3 target figures was randomly determined from page to page. Procedure All eight test conditions contained 6 non-delay (zero set) trials and 10 delay (20 set) trials. During each trial the to-be-retained material was presented for 2 set followed immediately (non-delay) or after 20 set (delay) by a second stimulus which the patient was asked to describe as being “identical to” or “different from” the first stimulus Patients were allowed 10 set to make this response Within each condition the second stimulus was identical to the first on half the non-delay and half the delay trials This same-different ordering was randomized for each individual condition. Following 6 non-delay trials, the nature of the distractor task was explained to the patient and he was allowed practice trials with each distractor task in order to familiarize himself with the correct technique. During the auditory distractor tasks, the patient was required either to count backwards from 100 by two’s (verbal) or to track the musical tones (nonverbal). The auditory distractor tape began immediately after the presentation of the to-be-remembered stimulus and terminated with the word “stop”, at which time the second stimulus was presented to the patient.
DAVID DELUCA, LAIRD S. CERMAKand NELSONBUTIERS
274
During the visual distractor conditions, the patient was required to scan either words (verbal) or “snowflake” figures (nonverbal). In the verbal condition, the patient was instructed to put a plus mark above every word which was a member of a pre-determined category, and a minus mark above every word which was not. Similarly, in the nonverbal task, the patient was required to put a plus mark above every “snowflake” figure that matched the master figure on top of the page, and a minus mark above every figure which did not. Scanning began immediately after the to-be-remembered stimulus had been presented and ended with the word “stop”. At this point the second stimulus was presented and the patient had to make a same-different response.
RESULTS Figure 3 shows the trials of each condition. group (P< 0.001) and were significant group No other interactions condition, or modality
percentage of correct responses each group achieved on the delay An analysis of variance performed on this data revealed significant condition (PC 0.001) effects but no significant modality effect. There x modality (PC 0.05) and group x condition (P< O*OOl)interactions. achieved significance. In addition, there were no significant group, effects for the non-delay trials. Recognition followlng vtsual dlstroctlon
Recognltlon following d!stractlon
audItory
100
a
Korsa koffs
sn
0
Alcoholics
t
‘g
: /
NV NV
I.: :
NV NV
VV
VNV
NVV
NVNV
FIG. 3. Percentage of correct responses by both groups on each of the 8 recognition conditions. Verbal stimuli: followed by verbal distractor activity=VV; Nonverbal stimuli: followed by nonverbal distractor activity=NVNV, etc.
Further analysis of the delay trials of each condition revealed that the Korsakoff patients recalled significantly less material than the alcoholic control patients under all conditions and modalities (P< 0.005) except for the condition where verbal material was followed by a nonverbal distractor (VNV). Here the Korsakoff patients performed as well as the control subjects with no difference at all when the distractor modality was auditory and some difference, though not a significant one, (P< 0.10) with the visual distractor. Overall, the alcoholic control subjects recalled less information following auditory distraction than they did following visual distraction (P< 0.01). However, such was not the case for Korsakoff patients, for whom the auditory distractor provided the most interference only in the instance where verbal material was followed by a verbal distractor (P< 0.05). Otherwise, the visual distractor produced the greater interference. Within group analyses revealed that the Korsakoff patients recalled more information in the verbal material, nonverbal distractor (VNV) condition than they did in any of the other conditions regardless of the modality of the distraction (P< 0.01). No other betweenconditions analyses were significant within this group following visual distraction but the
AN
ANALYSIS
OF KORSAKOFF
PATIENl-S’
RECALL
FOLLOWING
VARYING
TYPES
OF DISTRACTOR
ACTIVITY
275
nonverbal material, verbal distractor (NVV) performance was significantly above the remaining two conditions when the distraction was auditory (PC 0.05). The same comparisons for the alcoholic control subjects showed that they also recalled less information in the VV condition than in any other condition (P< 0.01) with the auditory distractor, and less in the W condition than in the VNV condition (PC O-05) when the distractor was visual. EXPERIMENT
II
Though it had been expected that the Korsakoff patients would improve, their remarkable performance in the retention of verbal material following a nonverbal distractor task was not anticipated. Since this effect had been obtained using a recognition test, it was decided to determine whether or not this performance would be preserved in a free recall paradigm. Method Subjects. The patients previously described in Experiment I also participated in the present investigation. Design. Each patient was given two different tests both of which were variations of the F’ETEWN and PETERSON distractor technique [4]. Only verbal to-be-remembered stimuli, presented visually, were used in this experiment. The two auditory distractor tasks (one verbal and one nonverbal) used in Experiment I were also employed in Experiment II. The patients saw the to-be-remembered materials, then they either counted backwards from 100 by two’s (verbal distractor) or tracked musical notes (nonverbal distractor) during the 20 set delay period. The order of presentation of the two recall conditions was randomly determined. Materials. The to-be-retained stimuli were two different sets of consonant trigrams (CCC’s) with a 25% or less association value taken from Witmer’s norms [I]. In addition, a question mark was presented at the end of each retention interval to signal recall. Each trigram and each question mark was presented on an individual 5 x 8 inch white card. Procedure. During each trial the to-be-remembered verbal stimulus was presented for two seconds followed immediately (non-delay) or after 20 set (delay) by the presentation of a question mark. Patients were allowed 10 seconds in which to recall the previously presented trigram. Jn all other respects, the procedure in this experiment was identical to that of Experiment 1.
RESULTS Figure 4 shows the percentage of correct responses for each group on the delay trials of each condition. An analysis of variance showed significant group (PC 0.005) and condition (PC 0.001) effects as well as a significant group by condition interaction (P< 0*005). Again, no significant non-delay effects were observed. Further analysis revealed that the Korsakoff patients recalled significantly less verbal material than the alcoholic control patients when a verbal distractor task (VV) was used 100 90 80
m
Korsokoffs
0
Acohol,cs
-
t al 70 : 6
60 50
.
40 s
t
0
c
FIG. 4. Percentage of correct responses by both groups on each of the 2 recall conditions. V-V=verbal stimuli-verbal distractor; V-NV=verbal stimuli-nonverbal distractor.
276
DAWN DELUCA, LAIRD S.
CERMAK
and NELSONBU-ITERS
(P< 0401) but not when a nonverbal distractor task (VNV) was used. Within group analyses
revealed that the Korsakoff patients recalled more information in the VNV condition than they did in the W condition (P < 0401) as did the alcoholic control patients (PC 0401). EXPERIMENT
III
The normal performance exhibited by the Korsakoff patients on both recognition and recall of verbal material following a nonverbal distractor task suggested that under these conditions it was possible to rehearse the verbal information. However, the inability of the Korsakoff patients to retain nonverbal material following either verbal or nonverbal distractor activity implied that either both of these tasks prevented nonverbal rehearsal or Korsakoff patients do not normally rehearse this kind of material. In order to test these assumptions the effect of an unfilled delay interval on the retention of both verbal and nonverbal information was examined. If nonverbal retention was still impaired while verbal retention remained intact, then it would have to be concluded that the Korsakoff patients’ nonverbal encoding strategies do not provide a mechanism for the recirculation of the memory trace during the retention interval. Method Subjects. Ten alcoholic Korsakoff patients and ten alcoholic control patients participated in the present experiment. Eight of the Korsakoff patients and seven of the alcoholic control subjects took part in Experiments I and II. The five new patients who were employed in Experiment III were comparable to the original patients with regard to I.Q. and age. Design. Each patient was given two different test conditions, one containing consonant trigrams (verbal), the other involving random shapes (nonverbal) as the to-be-remembered materials. In both conditions, the experimental stimulus was presented to the patient for two seconds followed immediately by an unfilled (no distractor activity) delay interval of 20 sec. After this delay period the patient was presented with a second stimulus which he was asked to describe as being “identical to” or “different from” the lirst, experimental stimulus. This same-different ordering and the order in which the two conditions was presented were randomly determined. Materials. The to-be-retained stimuli were consonant trigrams and random shapes similar to those previously described in Experiment I. Procedure. The procedure employed in the present experiment was identical to the recognition procedure previously described in Experiment I, except that silence was maintained during the retention interval.
RESULTS Figure 5 shows the percentage of correct responses for each group on both delay conditions. Significant group (PC 0405) and condition (P< 0.025) effects as well as a significant group x condition interaction (PC 0.01) were revealed by analysis of variance.
Korsakoffs 0
Alcoholics
Random shapes
Fro. 5. Percentage
of correct responses by both groups for verbal and nonverbal following an unfilled retention interval.
material
AN
ANALYSIS
OF KORSAKOFF
PATIENTS’
RECALL
FOLLOWING
VARYING
TYPES
OF DISTRAITOR
ACTIVlTY
277
The Korsakoff patients retained significantly less nonverbal material than did the control patients (P< 0.01) but performed as well as the control subjects on the retention of verbal material. In addition, the Korsakoff patients’ retention of nonverbal materials was inferior to their retention of verbal materials (PC O-02). DISCUSSION The alcoholic Korsakoff patients exhibited a severe verbal memory deficit on both recognition (Experiment I) and recall (Experiment II) tests employing retention intervals filled with verbal distractor activity. In contrast, their retention of precisely the same type of material following a delay interval filled with nonverbal distractor activity, or no directed activity at all (Experiment III), was perfectly intact. While it had been expected that a reverse phenomenon would occur when retention of nonverbal information was tested, the Korsakoff patients’ retention of this material was as impaired following verbal distraction as it was following nonverbal distraction. In fact, their retention of nonverbal material was even impaired following an unfilled delay interval. Similar results have been reported by PRISKO[9] and by SIDMAN,STODDARDand MOHR [lo] for H.M., a bilateral hippocampal patient. Although severely impaired in his ability to retain nonverbal information, H.M. could retain verbal material during unfilled delay intervals as long as 40 sec. The Korsakoff patients’ proficiency in retaining verbal information following nonverbal distraction was surprising, though not entirely unpredictable. Recent studies [I] have shown that Korsakoff patients tend to rely on an acoustic code when attempting to maintain verbal information in memory. This acoustic code may be sufficient to maintain a trace in memory through a process of continual recirculation which may involve subvocal rehearsal. However, once this process is interrupted the memory trace fades rapidly. Apparently, Korsakoff patients’ acoustic recirculation of verbal materials can be disrupted by additional verbal analysis demands but not by nonverbal analysis requirements. In contrast, Korsakoff patients’ nonverbal memory was impaired regardless of the nature of the intervening distractor activity. Evidently, the mechanism normally used to maintain nonverbal information is not used appropriately by Korsakoff patients. It has been proposed that this mechanism involves the use of a visualization technique referred to as “imagery” [ll, 121. Since it has already been shown that Korsakoff patients are impaired in their ability to “image” [13, 141, it follows that this deficit might account for their inability to maintain nonverbal memory traces. Thus, while Korsakoff patients can employ acoustic recirculation to successfully maintain verbal information, they have no comparable mechanism to maintain nonverbal material. BUTTERSet al. [3] reported that Korsakoff patients had less difficulty retaining nonverbal than verbal materials following verbal distraction. However, there was a nonverbal memory deficit at the retention interval comparable to the one used in the present investigation (18 set) when these materials were presented in the visual or the tactile modalities. It was only at the shorter retention interval (9 set) that the Korsakoff patients’ nonverbal memory was intact, suggesting that the decay rate for nonverbal material may be slower than for verbal information. Further evidence that Korsakoff patients’ nonverbal encoding mechanism (based on defective visualization) is impaired, was shown by the fact that their nonverbal retention was more easily disrupted by visual than by auditory distraction. Precisely the opposite effect was found for the control patients possibly because the auditory distractor tasks were always experimenter paced whereas the visual tasks were performed at a pace dictated by
DAVID DELUCA, LAIRD S. CERMAKand NELSONBUTTFRS
278
the patient. Since the time allotted during the retention interval must be divided between performance on the distractor task and the recirculation of the to-be-remembered material, the more time a distractor task demands, the more it takes away from the maintenance of the memory trace [6]. Nonetheless, even these time sharing demands were overshadowed for the Korsakoff patients when visual disruption of their already ill-defined trace occurred. In summary, it can be concluded that Korsakoff patients are impaired in their retention of both verbal and nonverbal materials because they tend to rely on inadequate encoding strategies. Their acoustic encoding of verbal information does allow recirculation of the trace providing no similar verbal analysis demands occur, but their nonverbal encoding strategies do not provide such a mechanism. Disruption of either trace by distractor material similar in nature and in modality of presentation to the stimulus material will produce the greatest levels of interference and will result in the Korsakoff patients being unable to retrieve the information. Acknowfedgement-This research was supported in part by NTH Grants AA-00187 and NB-06209 to Boston University School of Medicine.
REFERENCES 1. CERMAK,L. S. and BUTTERS,N. Information processing deficits of alcoholic Korsakoff patients. &a~/. J. Stud. Ale. 34, 1110-1132, 1973. 2 CERMAK,L S., BUTTERS,N. and GERREIN,J. The extent of the verbal encoding ability of Korsakoff patients. Neuropsychologia 11,85-94, 1973. H. Material-specificmemory deficits in alcoholic 3. BUTTERS,N., LEWIS,R., CERMAK,L. S. and GOODGLASS, Korsakoff patients. Neuropsychologia 11, 291-299, 1973. 4. PETERSON,L. R. and PETERSON,M. J. Short-term retention of individual verbal items. J. e.vp. Psycho/. S&193-198,1959. 5. REITMAN,J. S. Mechanisms of forgetting in short-term memory. Cog. Psycho/. 2, 185-195, 1971. 6. SHIFFRIN,R. M. Information persistence in short-term memory. J. exp. Psychol. 100,39-49, 1973. 7. WITMER,L. R. The association value of three-place consonant syllables. J. genet. Psychof. 47, 337-359, 1935. J. M. and GARVIN, E. A. Complexity, 8. VANDERPLAS, 9. 10. 11. 12. 13.
associative value and practice as factors in shape recognition following paired-associated training. J. exp. Psychol. 57, 155-163, 1959. PRISKO,L. Short-term memory in focal cerebral damage. Unpublished Ph.D. thesis, McGill University, 1963. SIDMAN,M., STORDARD,L. T. and MOHR, J. P. Some additional quantitative observations of immediate and memory in a patient with bilateral hippocampal lesions. Neuropsychologia 6, 245-254, 1968. BOWER,G. H. Mental imagery and associative learning. In L. GREGG (Editor), Cognition in Learn@ and Memory. Wiley, New York, 1974. PAIVIO,A. imagery and Verbal Processes. Holt, Rinehart and Winston, Inc. New York, 1971. BADDELEY,A. D. and WARRINGTON,E. K. Memory coding and amnesia. Newopsychologia 11,159-165,
1973. 14. CERMAK,L. S. Imagery as an aid to retrieval for Korsakoff
Rbumk-On
patients. Cortex (in press).
a soumis 10 malades atteints de Korsakoff d’origine alcoolique et 10 sujels de contrSle alcoolique B des Cpreuves de m&moire B court terme avec des activites de distraction surajoutCes; des trigrammes de consonnes (verbal) et de formes aleatoires (non verbal) ttaienl utilists comme materiel & retenir. Chez les sujets atteints de Korsakoff, il existait un grave dtficit de la mCmoire verbalc lorsque l’intervalle de detention Btait occupC par une activitC de distraction verbale, mais la rCtention du m&me materiel verbal Btait intacte lorsqu’une Cpreuve de distraction non verbale Ctait utilisee. A I’opposC, la retention du matCrie1 non verbal des sujets atteints de Korsakotf, Ctait deficitaire quelque soit la nature de l’activite de distraction. En fait, leur retention du materiel non verbal 6tait mCme troublCe lorsque I’intervalle de rttention ne comportait aucune activite de distraction.
AN
ANALYSIS
OF KORSAKOFF
PATIENTS’
RECALL
FOLLOWING
VARYING
TYPES
OF DISTRACTOR
ACTIVITY
Zusammenfassung-Zehn alkoholischen Korsakow-Patienten und zehn alkoholischen Kontrollpersonen wurden fiir das Kurzzeitgedachtnis bei Ablenkung verschiedene Aufgaben gestellt, bei denen als verbaler Test ‘consonants trigrams’ und als nonverbaler Test wahllose Figuren als zu behaltendes Material verwandt wurden. Die Korsakow-Patienten zeigten schwere verbale Merkschwgche, wenn die zeitliche Merkspanne mit verbaler Ablenkungsaktivitat ausgefiillt war, wehrend das Bchalten desselben verbalen Materials intakt war, wenn eine nichtverbale Ablenkung eingesetzt wurde. Im Gegensatz dazu war das Behalten nonverbalen Materials beintr%htigt unabhlngig von der Art der Ablcnkung. In der Tat war such dann das Behalten des nonverbalen Materials beeintrichtigt, wenn die Merkspanne frei von Ablenkung blieb.
279
1975,
Vol.
13, pp. 271 to 279.
Pergamon
Press.
Printed
in England
AN ANALYSIS OF KORSAKOFF PATIENTS’ RECALL FOLLOWING VARYING TYPES OF DISTRACTOR ACTIVITY DAVID
DE LUCA, LAIRD S. CERMAK*and NELSONBUTTERS
Psychology Service, Boston Veterans Administration Hospital and Aphasia Research Unit, Ncuro!ogy Department, Boston University School of Medicine, Boston, Mass 02118, U.S.A. (Received 31 August 1974) Abstract-Ten alcoholic Korsakoff patients and ten alcoholic control subjects were given several short-term memory, distractor type tasks in which consonant trigrams (verbal) and random shapes (nonverbal) were employed as the to-be-retained materials. The Korsakoff patients demonstrated a severe verbal memory deficit when the retention interval was filled with verbal distractor activity, but their retention of the same verbal material was intact when a nonverbal distractor task was used. In contrast, the Korsakoff patients’ retention of nonverbal material was impaired regardless of the nature of the distractor activity. In fact, their retention of nonverbal material was impaired even when an unfilled retention interval was used. INTRODUCTION RESEARCHdesigned to investigate the nature of the Korsakoff patients’ memory disorder has generally focused upon the difficulties experienced by these patients when attempting to retain verbal information [l]. These analyses have revealed that the major factor contributing to the Korsakoff patients’ verbal memory impairment is an inability to encode the semantic properties of verbal material [2]. The only analysis of these patients’ nonverbal memory abilities [3] indicated that Korsakoff patients have considerably less difficulty recognizing nonverbal than verbal material following verbal distractor activity [4]. However, the exclusive use of a verbal distractor task may have determined these results since recent studies [5, 61 using the short-term memory (STM) distractor technique with normal subjects have shown that the similarity between the to-be-retained material and the distractor activity is crucial in determining the amount of information loss. The Korsakoff patients’ retention of nonverbal materials may be intact only when the distractor activity differs from the to-be-remembered information (i.e. when nonverbal material is followed by a verbal distractor task), and, using the same reasoning, their verbal memory might improve when a nonverbal distractor is employed. In order to assess these possibilities, an analysis of the effect of different types of distractor activity upon the Korsakoff patients’ retention of verbal and nonverbal materials was performed.
EXPERIMENT
I
Method Subjects. Two groups of hospitalized patients were employed in the present study: ten patients diagnosed as alcoholic Korsakoffs by the Neurology Services of the Boston and Brockton VA Hospitals; and ten *Reprint requests should be sent to Laird S. Cermak, Psychology Service, Boston Veterans Administration Hospital, 150 South Huntington Avenue, Boston, Massachusetts 02130. 271
272
DAVID DELIJCA. LAIRD S. CERMAK
and NELSON BUTTERS
alcoholic control patienls who were involved in various treatment programs at the hospitals mentioned above. All of the Korsakoff patients had severe memory impairments as assessed by clinical methods. They had difficulty recalling day to day and current events (i.e., anterograde amnesia) and they had retrograde amnesias of varying severity for events which occurred prior to the onset of their illness. In contrast, the alcoholic control patients exhibited none of the clinical symptoms associated with Korsakoff’s syndrome. To insure that I.Q.‘s were all within normal range, the verbal section of the Wechsler Adult Intelligence Scale was administered to all patients participating in thisexperiment.The meanVerbal1.Q. for the Korsakoff patients was 105 (range 92-124). The mean Verbal I.Q. for the alcoholic controls was 105 (range 91-127). The Korsakoff patients had a mean age of 55 (range 45-61) as compared to a mean age of 51 (range 42-63) for the alcoholic group. Des&z. Each patient was given eight different tests, all of which were variations of the PETERSONand PETERSON[4] distractor technique. The to-be-remembered materials were visually presented consonant trigrams (verbal) and random shapes (nonverbal). Two auditory distractor tasks (one verbal and one nonverbal) and two visual distractor tasks (one verbal and one nonverbal) were paired with each of the two types of stimulus materials making a total of eight separate conditions. During test session I, retention of both verbal and nonverbal materials was tested following the two auditory distractor tasks. Patients saw the stimuli, then either counted backL3ards from 100 by two’s (verbal distractor) or tracked musical tones (nonverbal distractor) for a duration of 20 sec. During test session II verbal and nonverbal retention was tested again, but this time the distractor activity was presented in the visual modality. Patients saw the stimuli then either scanned a list for particular words (verbal distractor) or they scanned for particular “snowflake” figures (nonverbal distractor) for a period of 20 sec. The order of presentation of the verbal and nonverbal recognition tasks was randomly determined and an interval of at least three days occurred between sessions. Materials. The to-be-remembered verbal stimuli were consonant trigrams (CCC’s) with a 25% or less association value taken from Witmer’s norms [7]. The nonverbal stimuli were VANDER~LAS and GARVIN [8] computer-generated random shapes (see Fig. I). The trigrams and the random shapes were presented individually on 5 v 8 inch white cards.
FIG. 1. Examples of the random shapes used on the nonverbal memory tasks. Both auditory distractor tasks were prerecorded on a two channel Sony tape recorder and were presented through Koss Pro/4AA headphones. The verbal tape consisted of 12 individual recordings of the words “count, 100, 98, (silence), stop”. The mnverbal tape consisted of 100 musical notes each presented for 4/5 set with an interstimulus interval of 1.5 sec. The notes (high D and low D) were produced by a two-octave electric organ and were recorded randomly on either the left or right channel. A 5 s 8 inch white card with four coordinates representing all possible responses (high, low, left ear, right car) was placed in front of the patient so that he could track 9 musical tones during each delay trial by indicating octave (high or low) and ear of presentation. The two visual distractor tasks were presented within 8 x 10 in. booklets. Each page of the verbal booklet contained 96 different nouns belonging to one of four tasonomic categories (animals, cars, cities, countries). Each noun appeared 4 times throughout a typed, triple spaced, 3 page list. The nonverbal booklet was 11 pages long, each page containing 25 “snowflake” figures (see Fig. 2). A different master figure appeared at
AN ANALYSIS
OF KORSAKOFF
PATIENTS’
RECALL
FOLLOWING
VARYING
TYPES
FIG. 2. Example of the Snowflake Figures employed on the nonverbal
OF DISTRACTOR
ACTIVITY
visual distractor
213
task.
the top of each page and 3 times among the other figures on one page. The position of these 3 target figures was randomly determined from page to page. Procedure All eight test conditions contained 6 non-delay (zero set) trials and 10 delay (20 set) trials. During each trial the to-be-retained material was presented for 2 set followed immediately (non-delay) or after 20 set (delay) by a second stimulus which the patient was asked to describe as being “identical to” or “different from” the first stimulus Patients were allowed 10 set to make this response Within each condition the second stimulus was identical to the first on half the non-delay and half the delay trials This same-different ordering was randomized for each individual condition. Following 6 non-delay trials, the nature of the distractor task was explained to the patient and he was allowed practice trials with each distractor task in order to familiarize himself with the correct technique. During the auditory distractor tasks, the patient was required either to count backwards from 100 by two’s (verbal) or to track the musical tones (nonverbal). The auditory distractor tape began immediately after the presentation of the to-be-remembered stimulus and terminated with the word “stop”, at which time the second stimulus was presented to the patient.
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During the visual distractor conditions, the patient was required to scan either words (verbal) or “snowflake” figures (nonverbal). In the verbal condition, the patient was instructed to put a plus mark above every word which was a member of a pre-determined category, and a minus mark above every word which was not. Similarly, in the nonverbal task, the patient was required to put a plus mark above every “snowflake” figure that matched the master figure on top of the page, and a minus mark above every figure which did not. Scanning began immediately after the to-be-remembered stimulus had been presented and ended with the word “stop”. At this point the second stimulus was presented and the patient had to make a same-different response.
RESULTS Figure 3 shows the trials of each condition. group (P< 0.001) and were significant group No other interactions condition, or modality
percentage of correct responses each group achieved on the delay An analysis of variance performed on this data revealed significant condition (PC 0.001) effects but no significant modality effect. There x modality (PC 0.05) and group x condition (P< O*OOl)interactions. achieved significance. In addition, there were no significant group, effects for the non-delay trials. Recognition followlng vtsual dlstroctlon
Recognltlon following d!stractlon
audItory
100
a
Korsa koffs
sn
0
Alcoholics
t
‘g
: /
NV NV
I.: :
NV NV
VV
VNV
NVV
NVNV
FIG. 3. Percentage of correct responses by both groups on each of the 8 recognition conditions. Verbal stimuli: followed by verbal distractor activity=VV; Nonverbal stimuli: followed by nonverbal distractor activity=NVNV, etc.
Further analysis of the delay trials of each condition revealed that the Korsakoff patients recalled significantly less material than the alcoholic control patients under all conditions and modalities (P< 0.005) except for the condition where verbal material was followed by a nonverbal distractor (VNV). Here the Korsakoff patients performed as well as the control subjects with no difference at all when the distractor modality was auditory and some difference, though not a significant one, (P< 0.10) with the visual distractor. Overall, the alcoholic control subjects recalled less information following auditory distraction than they did following visual distraction (P< 0.01). However, such was not the case for Korsakoff patients, for whom the auditory distractor provided the most interference only in the instance where verbal material was followed by a verbal distractor (P< 0.05). Otherwise, the visual distractor produced the greater interference. Within group analyses revealed that the Korsakoff patients recalled more information in the verbal material, nonverbal distractor (VNV) condition than they did in any of the other conditions regardless of the modality of the distraction (P< 0.01). No other betweenconditions analyses were significant within this group following visual distraction but the
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nonverbal material, verbal distractor (NVV) performance was significantly above the remaining two conditions when the distraction was auditory (PC 0.05). The same comparisons for the alcoholic control subjects showed that they also recalled less information in the VV condition than in any other condition (P< 0.01) with the auditory distractor, and less in the W condition than in the VNV condition (PC O-05) when the distractor was visual. EXPERIMENT
II
Though it had been expected that the Korsakoff patients would improve, their remarkable performance in the retention of verbal material following a nonverbal distractor task was not anticipated. Since this effect had been obtained using a recognition test, it was decided to determine whether or not this performance would be preserved in a free recall paradigm. Method Subjects. The patients previously described in Experiment I also participated in the present investigation. Design. Each patient was given two different tests both of which were variations of the F’ETEWN and PETERSON distractor technique [4]. Only verbal to-be-remembered stimuli, presented visually, were used in this experiment. The two auditory distractor tasks (one verbal and one nonverbal) used in Experiment I were also employed in Experiment II. The patients saw the to-be-remembered materials, then they either counted backwards from 100 by two’s (verbal distractor) or tracked musical notes (nonverbal distractor) during the 20 set delay period. The order of presentation of the two recall conditions was randomly determined. Materials. The to-be-retained stimuli were two different sets of consonant trigrams (CCC’s) with a 25% or less association value taken from Witmer’s norms [I]. In addition, a question mark was presented at the end of each retention interval to signal recall. Each trigram and each question mark was presented on an individual 5 x 8 inch white card. Procedure. During each trial the to-be-remembered verbal stimulus was presented for two seconds followed immediately (non-delay) or after 20 set (delay) by the presentation of a question mark. Patients were allowed 10 seconds in which to recall the previously presented trigram. Jn all other respects, the procedure in this experiment was identical to that of Experiment 1.
RESULTS Figure 4 shows the percentage of correct responses for each group on the delay trials of each condition. An analysis of variance showed significant group (PC 0.005) and condition (PC 0.001) effects as well as a significant group by condition interaction (P< 0*005). Again, no significant non-delay effects were observed. Further analysis revealed that the Korsakoff patients recalled significantly less verbal material than the alcoholic control patients when a verbal distractor task (VV) was used 100 90 80
m
Korsokoffs
0
Acohol,cs
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t al 70 : 6
60 50
.
40 s
t
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c
FIG. 4. Percentage of correct responses by both groups on each of the 2 recall conditions. V-V=verbal stimuli-verbal distractor; V-NV=verbal stimuli-nonverbal distractor.
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(P< 0401) but not when a nonverbal distractor task (VNV) was used. Within group analyses
revealed that the Korsakoff patients recalled more information in the VNV condition than they did in the W condition (P < 0401) as did the alcoholic control patients (PC 0401). EXPERIMENT
III
The normal performance exhibited by the Korsakoff patients on both recognition and recall of verbal material following a nonverbal distractor task suggested that under these conditions it was possible to rehearse the verbal information. However, the inability of the Korsakoff patients to retain nonverbal material following either verbal or nonverbal distractor activity implied that either both of these tasks prevented nonverbal rehearsal or Korsakoff patients do not normally rehearse this kind of material. In order to test these assumptions the effect of an unfilled delay interval on the retention of both verbal and nonverbal information was examined. If nonverbal retention was still impaired while verbal retention remained intact, then it would have to be concluded that the Korsakoff patients’ nonverbal encoding strategies do not provide a mechanism for the recirculation of the memory trace during the retention interval. Method Subjects. Ten alcoholic Korsakoff patients and ten alcoholic control patients participated in the present experiment. Eight of the Korsakoff patients and seven of the alcoholic control subjects took part in Experiments I and II. The five new patients who were employed in Experiment III were comparable to the original patients with regard to I.Q. and age. Design. Each patient was given two different test conditions, one containing consonant trigrams (verbal), the other involving random shapes (nonverbal) as the to-be-remembered materials. In both conditions, the experimental stimulus was presented to the patient for two seconds followed immediately by an unfilled (no distractor activity) delay interval of 20 sec. After this delay period the patient was presented with a second stimulus which he was asked to describe as being “identical to” or “different from” the lirst, experimental stimulus. This same-different ordering and the order in which the two conditions was presented were randomly determined. Materials. The to-be-retained stimuli were consonant trigrams and random shapes similar to those previously described in Experiment I. Procedure. The procedure employed in the present experiment was identical to the recognition procedure previously described in Experiment I, except that silence was maintained during the retention interval.
RESULTS Figure 5 shows the percentage of correct responses for each group on both delay conditions. Significant group (PC 0405) and condition (P< 0.025) effects as well as a significant group x condition interaction (PC 0.01) were revealed by analysis of variance.
Korsakoffs 0
Alcoholics
Random shapes
Fro. 5. Percentage
of correct responses by both groups for verbal and nonverbal following an unfilled retention interval.
material
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The Korsakoff patients retained significantly less nonverbal material than did the control patients (P< 0.01) but performed as well as the control subjects on the retention of verbal material. In addition, the Korsakoff patients’ retention of nonverbal materials was inferior to their retention of verbal materials (PC O-02). DISCUSSION The alcoholic Korsakoff patients exhibited a severe verbal memory deficit on both recognition (Experiment I) and recall (Experiment II) tests employing retention intervals filled with verbal distractor activity. In contrast, their retention of precisely the same type of material following a delay interval filled with nonverbal distractor activity, or no directed activity at all (Experiment III), was perfectly intact. While it had been expected that a reverse phenomenon would occur when retention of nonverbal information was tested, the Korsakoff patients’ retention of this material was as impaired following verbal distraction as it was following nonverbal distraction. In fact, their retention of nonverbal material was even impaired following an unfilled delay interval. Similar results have been reported by PRISKO[9] and by SIDMAN,STODDARDand MOHR [lo] for H.M., a bilateral hippocampal patient. Although severely impaired in his ability to retain nonverbal information, H.M. could retain verbal material during unfilled delay intervals as long as 40 sec. The Korsakoff patients’ proficiency in retaining verbal information following nonverbal distraction was surprising, though not entirely unpredictable. Recent studies [I] have shown that Korsakoff patients tend to rely on an acoustic code when attempting to maintain verbal information in memory. This acoustic code may be sufficient to maintain a trace in memory through a process of continual recirculation which may involve subvocal rehearsal. However, once this process is interrupted the memory trace fades rapidly. Apparently, Korsakoff patients’ acoustic recirculation of verbal materials can be disrupted by additional verbal analysis demands but not by nonverbal analysis requirements. In contrast, Korsakoff patients’ nonverbal memory was impaired regardless of the nature of the intervening distractor activity. Evidently, the mechanism normally used to maintain nonverbal information is not used appropriately by Korsakoff patients. It has been proposed that this mechanism involves the use of a visualization technique referred to as “imagery” [ll, 121. Since it has already been shown that Korsakoff patients are impaired in their ability to “image” [13, 141, it follows that this deficit might account for their inability to maintain nonverbal memory traces. Thus, while Korsakoff patients can employ acoustic recirculation to successfully maintain verbal information, they have no comparable mechanism to maintain nonverbal material. BUTTERSet al. [3] reported that Korsakoff patients had less difficulty retaining nonverbal than verbal materials following verbal distraction. However, there was a nonverbal memory deficit at the retention interval comparable to the one used in the present investigation (18 set) when these materials were presented in the visual or the tactile modalities. It was only at the shorter retention interval (9 set) that the Korsakoff patients’ nonverbal memory was intact, suggesting that the decay rate for nonverbal material may be slower than for verbal information. Further evidence that Korsakoff patients’ nonverbal encoding mechanism (based on defective visualization) is impaired, was shown by the fact that their nonverbal retention was more easily disrupted by visual than by auditory distraction. Precisely the opposite effect was found for the control patients possibly because the auditory distractor tasks were always experimenter paced whereas the visual tasks were performed at a pace dictated by
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the patient. Since the time allotted during the retention interval must be divided between performance on the distractor task and the recirculation of the to-be-remembered material, the more time a distractor task demands, the more it takes away from the maintenance of the memory trace [6]. Nonetheless, even these time sharing demands were overshadowed for the Korsakoff patients when visual disruption of their already ill-defined trace occurred. In summary, it can be concluded that Korsakoff patients are impaired in their retention of both verbal and nonverbal materials because they tend to rely on inadequate encoding strategies. Their acoustic encoding of verbal information does allow recirculation of the trace providing no similar verbal analysis demands occur, but their nonverbal encoding strategies do not provide such a mechanism. Disruption of either trace by distractor material similar in nature and in modality of presentation to the stimulus material will produce the greatest levels of interference and will result in the Korsakoff patients being unable to retrieve the information. Acknowfedgement-This research was supported in part by NTH Grants AA-00187 and NB-06209 to Boston University School of Medicine.
REFERENCES 1. CERMAK,L. S. and BUTTERS,N. Information processing deficits of alcoholic Korsakoff patients. &a~/. J. Stud. Ale. 34, 1110-1132, 1973. 2 CERMAK,L S., BUTTERS,N. and GERREIN,J. The extent of the verbal encoding ability of Korsakoff patients. Neuropsychologia 11,85-94, 1973. H. Material-specificmemory deficits in alcoholic 3. BUTTERS,N., LEWIS,R., CERMAK,L. S. and GOODGLASS, Korsakoff patients. Neuropsychologia 11, 291-299, 1973. 4. PETERSON,L. R. and PETERSON,M. J. Short-term retention of individual verbal items. J. e.vp. Psycho/. S&193-198,1959. 5. REITMAN,J. S. Mechanisms of forgetting in short-term memory. Cog. Psycho/. 2, 185-195, 1971. 6. SHIFFRIN,R. M. Information persistence in short-term memory. J. exp. Psychol. 100,39-49, 1973. 7. WITMER,L. R. The association value of three-place consonant syllables. J. genet. Psychof. 47, 337-359, 1935. J. M. and GARVIN, E. A. Complexity, 8. VANDERPLAS, 9. 10. 11. 12. 13.
associative value and practice as factors in shape recognition following paired-associated training. J. exp. Psychol. 57, 155-163, 1959. PRISKO,L. Short-term memory in focal cerebral damage. Unpublished Ph.D. thesis, McGill University, 1963. SIDMAN,M., STORDARD,L. T. and MOHR, J. P. Some additional quantitative observations of immediate and memory in a patient with bilateral hippocampal lesions. Neuropsychologia 6, 245-254, 1968. BOWER,G. H. Mental imagery and associative learning. In L. GREGG (Editor), Cognition in Learn@ and Memory. Wiley, New York, 1974. PAIVIO,A. imagery and Verbal Processes. Holt, Rinehart and Winston, Inc. New York, 1971. BADDELEY,A. D. and WARRINGTON,E. K. Memory coding and amnesia. Newopsychologia 11,159-165,
1973. 14. CERMAK,L. S. Imagery as an aid to retrieval for Korsakoff
Rbumk-On
patients. Cortex (in press).
a soumis 10 malades atteints de Korsakoff d’origine alcoolique et 10 sujels de contrSle alcoolique B des Cpreuves de m&moire B court terme avec des activites de distraction surajoutCes; des trigrammes de consonnes (verbal) et de formes aleatoires (non verbal) ttaienl utilists comme materiel & retenir. Chez les sujets atteints de Korsakoff, il existait un grave dtficit de la mCmoire verbalc lorsque l’intervalle de detention Btait occupC par une activitC de distraction verbale, mais la rCtention du m&me materiel verbal Btait intacte lorsqu’une Cpreuve de distraction non verbale Ctait utilisee. A I’opposC, la retention du matCrie1 non verbal des sujets atteints de Korsakotf, Ctait deficitaire quelque soit la nature de l’activite de distraction. En fait, leur retention du materiel non verbal 6tait mCme troublCe lorsque I’intervalle de rttention ne comportait aucune activite de distraction.
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Zusammenfassung-Zehn alkoholischen Korsakow-Patienten und zehn alkoholischen Kontrollpersonen wurden fiir das Kurzzeitgedachtnis bei Ablenkung verschiedene Aufgaben gestellt, bei denen als verbaler Test ‘consonants trigrams’ und als nonverbaler Test wahllose Figuren als zu behaltendes Material verwandt wurden. Die Korsakow-Patienten zeigten schwere verbale Merkschwgche, wenn die zeitliche Merkspanne mit verbaler Ablenkungsaktivitat ausgefiillt war, wehrend das Bchalten desselben verbalen Materials intakt war, wenn eine nichtverbale Ablenkung eingesetzt wurde. Im Gegensatz dazu war das Behalten nonverbalen Materials beintr%htigt unabhlngig von der Art der Ablcnkung. In der Tat war such dann das Behalten des nonverbalen Materials beeintrichtigt, wenn die Merkspanne frei von Ablenkung blieb.
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