Neuropsycholoym. Vol. 24, No. Printed m Great Bntain
5, pp.
659-670,
0028-3932/86 $3.00+0.00 Pergamon Journals Ltd.
1986.
RIGHT HIPPOCAMPAL EXCISION IMPAIRS LEARNING RECALL OF A LIST OF ABSTRACT DESIGNS MARILYN
AND
JONES-GOTMAN
Montreal Neurological Institute, McGill University, 3801 University Street, Montreal, Quebec, Canada
H3A 284
(Accepted 5 February 1986) Abstract-The role of the temporal lobes and the hippocampus in learning a list of abstract designs was investigated. Variables studied included trials to criterion, 24-hr delayed recall and serialposition effects. Normal control subjects and four groups of patients, classified according to side of temporal lobectomy and extent of excision from the hippocampal zone, were tested. Patients with a right temporal lobectomy that included a large hippocampal excision showed deficient learning and memory, and, on the serial-position analysis, they recalled essentially none of the first items of the list. The other patient groups were unimpaired, except in the number of trials required to reach criterion.
INTRODUCTION STUDIES of patients with focal brain lesions have established that the right nondominant temporal lobe is important in memory for material that is difficult to verbalize, such as unfamiliar faces [19, 351, unfamiliar tunes [ 17, 30, 401 and visually presented geometric or abstract patterns [12, 14, 333. It also plays a significant role in memory for visual patterns that can be verbalized, such as representational drawings [9, 201, and visual images that represent concrete nouns [ll, 131. In addition, the memory deficits that follow right temporal lobectomy are sometines contingent upon [S, 11, 18, 22, 321, or exacerbated by [6, 12, 131, inclusion of a significant portion of the mesial temporal-lobe structures (hippocampus, parahippocampal gyrus, uncus and amygdala) in the temporal-lobe removal. The dominant temporal lobe, in contrast, plays a crucial role in the memory for verbal material, but it does not seem to contribute significantly to memory for nonverbal materal [15, 161. Attempts to determine the source of the memory deficits associated with temporal-lobe lesions have revealed some minor impairments in the cognitive processing of materal that is to be remembered [lo, 13, 28, 381, but these non-mnemonic impairments are very mild. It seems clear, then, that the deficits arise from mechanisms within the memory process itself. They could result, for example, from an inefficient organization of memoranda into memory, from rapid trace decay, or from poor access to the memory trace. Some of these possibilities imply impairment during learning, whereas others imply that the deficit occurs at retrieval. The aim of the present experiment was to investigate the relative contributions of learning and memory to the impairments in visual pattern recall that occur after right temporal-lobe damage. A list-learning paradigm was chosen, where the material to be remembered was learned to a specific criterion and where recall was tested after a long delay. The task was designed to be analogous to verbal list-learning tasks that use unrelated words; therefore the list was relatively long, the designs to be learned were dissimilar, and memory was tested by 659
660
MARILYN JONES-GOTMAN
free recall. Because the delayed memory test was carried out after all subjects had reached a stable and equivalent level of acquisition, it was expected to yield a measure of memory that would not be confounded by varying levels of learning. Thus learning and memory performances could be assessed separately. The list-learning paradigm also allows the study of serial position effects 12, 2 1J, which are interesting for the light they may shed on hippocampal function. Verbal serial position studies have been carried out with patients who have undergone temporal lobectomy and with the patient H.M., in whom the uncus, the amygdala, and the anterior two-thirds of the hippocampus and parahippocampal gyrus have been excised bilaterally [29]. In those studies, H.M. was able to recall only the last few items from the word lists, and patients with a left temporal lobectomy that included a significant encroachment on the hippocampal structures showed, like H.M., a normal recency effect but no primacy effect [IO, 20, 281. This pattern of results was believed to reflect the intact short-term memory and faulty long-term storage of new material that is characteristic of patients with bilateral hippocampal damage. Those findings, however, were specific to verbal material. The present investigation will allow the assessment ofa possible right-hemisphere analogue when the material to be learned is a list of designs. The variables to be studied thus include acquisition to a specified criterion of learning, recall after 24 hr, and serial position effects. An impairment after right temporal lobectomy was expected on this task, but no predictions were made as to whether the deficit would appear in the learning phase, the recall phase, or both. A specific prediction was made that patients with extensive damage to the right hippocampal zone would fail to show a primacy effect on the serial position aspect of the study. Patients with a left temporal-lobe lesion were expected to perform normally.
METHODS Suhiecrs The experimental subjects were 67 patients at the Montreal Neurological Hospttal who had undergone a unilateral anterior temporal lobectomy for the relief of intractable epilepsy; 34 removals were from the right hemisphere and 33 were from the left. In all cases the preoperative cerebral lesion had been well-lateralized and. except for seven cases of cerebral tumor, all were static and atrophic. All patients were right-handed except for two who were left-handed or ambidextrous; those two patients had been shown by preoperative intracarotid sodium Amytal tests I-1. 341 to have speech represented in the left hemisphere. Patients with atypical speech representation, with known damage outside the temporal lobe, with a fast-growing tumor, or with a Full Scale IQ under X0 were excluded. Thirty-seven patients were tested 14 I8 days after surgery. and the others were seen in follow-up study one or more years after operation. The patients were grouped according to the side of temporal lobectomy and according to the extent of removal from the hippocampal region. Patients in whom the mesial excision did not exceed the pcs ofthe hippocampus wcrc placed in a small hippocampal-removal group (h). and those having a more radical excision of fhe hippocampus and.!or parahippocampal gyrus were assigned to a large hippocampal-removal group (H). Thus there were four patient groups, two in which the cerebral exctstons wcrc from the right temporal lobe but that differed in the extent of removal from the mesial temporal-lobe structures (groups RTh and RTH), and two corresponding left temporallobe groups (LTh and LTH). The mean cxtcnt of removal from the temporal neocortex, measured both along the Sylvian fissure and along the base of the brain, is detailed for each group in Table I. The table also provides group information regarding removal of the amygdala, and it shows the distribution of the seven cases ofcerebral tumor. Normal crntrrol yroup. Twenty-live normal control subjects were also tested. These were hospital support staff and relatives of patients, selected to match the patient groups as closely as possible with respect to the distribution of age. sex, education and occupation. The sex distribution, mean age and mean number of years of education for each subject group are shown in Table 2, together with the mean Full Scale Wechsler IQ ratings of the patient groups. No intelligence ratings were obtained for the normal control subjects. Putirnt H.M.:hila~rral mesial temporal-lobe remod One additional subject was tested; this was patient H.M.. who in 1953 underwent an g-cm resection along the mesial surface of both temporal lobes. The uncus, the amygdala and the anterior two-thirds of the hippocampus and parahippocampal gyrus were included in the removal. but the
RIGHT
HIPPOCAMPAL
EXCISION
661
Table 1. Extent of surgical excision from the temporal neocortex and amygdala, and distribution of cases of cerebral neoplasm, for each patient group (LT = left temporal, RT = right temporal, h = small hippocampal excision, H = large hippocampal excision)
Group
N
Extent of removal .along the base of the brain (cm) Range Mean
Extent of removal along the Sylvian fissure (cm) Mean Range
Extent of amygdala removal
Cases of cerebral neoplasm two cases of astrocytoma
LTh
20
4.75
4.c5.5
5.47
4.G6.5
partial in 5 cases and complete in all other
LTH
13
4.96
4.0-6.0
5.82
4.5-7.5
complete in one oligodenall cases droglioma; one astrocytoma
RTh
20
4.88
4.0-6.0
6.22
5.c7.5
partial in 3 cases and complete in all others
one astrocytoma; one low-grade glioma
RTH
14
5.31
5.0-6.5
6.49
5.5-8.0
complete in all cases
one astrocytoma
Table 2. Subjects
Sex
Age
Years of education Mean Range
Wechsler I.Q. Mean Range
Group
M
F
Mean
Range
control
10
15
21.2
1947
12.3
8-15
Left temporal small hippocampal excision (LTh)
8
12
26.1
1747
12.6
l&16
107.6
9&129
Left temporal large hippocampal excision (LTH)
8
5
28.7
1946
12.4
3-18
110.1
9&129
Right temporal small hippocampal excision (RTh)
11
9
27.8
17-49
12.2
8-17
1134
91-130
Right temporal large hippocampal excision (RTH)
11
3
30.4
1644
11.5
6-16
110.6
87-126
Normal
Not assessed
MARILYN JONES-GWMAN
662 lateral neocortex was spared Full Scale IQ of 104.
[29]. This patient was 55 years old when tested. He had a high school education
and a
Test materials The material consisted of 13 abstract patterns that were simple enough to be copied rapidly but that were sufficiently complex to discourage direct descriptive naming. The stimuli are shown grouped together in Fig. 1: the subjects actually saw each design individually in the center of a 7.5 cm x 12.5 cm card. The order of presentation was determined for each subject from a table of random permutations of numbers. Although every subject received a different order of presentation, the order for each subject remained the same throughout the testing session.
The subjects
received
the following
instructions:
This is a design-learning test. To learn the designs you will copy each one on a small piece of paper, and after you have copied them all you will draw as many as you can remember on a regular sheet of paper. You will then copy the drawings again and recall them again, and you will keep doing this until you have learned them. Subjects were given pads of 7.5 cm x 12.5 cm paper for the copy task. They were allowed 10 set to copy each design, and the recall sheet was given to them immediately after the last drawing had been copied. The copy-then-recall procedure continued until at least 12 of the 13 designs had been recalled twice consecutively; if this criterion was not reached by the tenth trial, the learning session was terminated. A delayed recall was obtained 24 hr later without previous warning. Scoring. Each drawing could earn up to four points: zero was given to drawings that were umdentifiable; one was allotted to poor but recognizable drawings; two applied to drawings that were fair but contained additions. distortions, omissions or inversions; three was for those that were good but not perfect by size, shape or proportion; and four was reserved for near-exact reproductions of the model. The score per trial was the sum of the points for each recalled drawing. The measures to be analysed were the recall scores for each learning trial. the number of trials to criterion. a delayed-recall measure, and recall as a function of serial position on the first learning trial.
RESULTS On no measure were significant operative period vs follow-up) or to education correlated significantly measure. Those variables therefore
differences found related to time of testing (early postextent of removal along the temporal neocortex. Years of with IQ, but neither one correlated with any other will not be considered further.
Learning Recull scores. No subject reached criterion before trial 3, but 24% of the normal control subjects and two of the patients did reach criterion on the third trial, thus receiving no further learning trials. Therefore, from trial 4 onwards, the number of subjects still in training
FIG. I. The
13 stimuli
that
make
up the list of designs. Each 7.5 cm x 12.5 cm card.
design
wah shown
alone
on a
RIGHT HIPPOCAMPAL
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663
diminishes. In order to compare the groups on those later trials where the numbers were diminishing, scores were estimated after subjects reached criterion. An adjustment was made for this in statistical analysis by reducing the error degrees of freedom [39]. Figure 2 shows the mean recall scores for the five subject groups over the first eight learning trials. The ninth and tenth trials are not shown because only 20% (trial 9) and 9% (trial 10) of the patients were still being trained after trial 8. As can be seen from the graph, patients with a right temporal lobectomy that included a large removal from the hippocampal zone (group RTH) obtained lower scores than all the other groups on each of the first five trials. Furthermore, the scores of the control subjects remained consistently superior to those of the patients over the entire learning session. These data were submitted to a two-way analysis of variance, which yielded significant F ratios of 6.35 for groups (P
5
m-
II cs 2 2 z
o--D
Normal Control
N=
cz
l -e
Left Temporal h
N = 20
=% 8 @z
LeH Temporal H
N = 13
I---.-.
Rlght Tempera, h N = 20
k---d
Rlght Temporal H N = 14
zo-
o--
5 iz
lo-
O-
I
I
I
I
I
I
I
I
1
2
3
4
5
6
7
8
Learnmg FIG.
---0
25
2. Learning
Trial
performance: mean recall scores obtained by each subject group, as a function trials. (h =small hippocampal excisions; H =large hippocampal excisions.)
of
MARILYN JONES-GOTMAN
664
Group N FIG. 3. Mean
number
of trials
Normal CNltKlI
n
H
?5
20
13
to reach criterion. (h=small hippocampal excisions.)
RlqhrTemporal n I,
20
14
hippocampal
excisions:
H =large
(F=6.92, PO.O5). Accuracy. The slowness of the patients in the left temporal-lobe groups to reach criterion was especially surprising given that their performances appeared normal throughout most of the test. To verify a clinical impression that those patients produced ‘good’ drawings, accuracy scores were calculated for each subject. This was done by dividing the score earned on each trial by the number of drawings produced, which yielded a mean score for the drawings of that trial. These data were submitted to a two-way analysis of variance, which yielded significant main effects for groups (F=6.50, P
real1
The delayed recall measure was computed as a percent forgetting score: each delayed recall score (D) was subtracted from the score obtained on the last learning and the difference was divided by the score on the last learning trial ({[L - D]/L} x gives a relative score that takes into account each subject’s peak performance.
subject’s trial (L), 100). This The four
RIGHT
HIPPOCAMPAL
665
EXCISION
subjects who failed to reach criterion were not included in the delayed recall analysis, and group RTh was also diminished by one subject who was not present for the delayed recall test. Because of the initial stable acquisition, the performance drop after 24 hr was very small, and for some subjects the delayed recall was actually slightly better than that on the last learning trial. The mean forgetting scores for the five groups are depicted in Fig. 4. A one-way analysis of variance performed on these data revealed a significant difference between the groups (F= 2.65, P-c 0.039), and subsequent Neuman-Keuls comparisons showed that this was due entirely to the deficient performance of group RTH. That group was impaired with respect to all the others except RTh (RTH vs NC, q=3.51, PcO.05; RTH vs LTh, q=3.70, PO.O5). Serial position For the serial position analysis, performance on the first learning trial was analysed. The input positions were grouped together by threes, and the drawing occupying the seventh (middle) position was excluded. This resulted in four input position groups of three drawings each (l-3,46, 8-10 and ll-13), determined according to the order in which they had been presented within the list. A simple count of recognizable drawings was used for this measure. Figure 5 shows the mean number of recognizable drawings recalled by each subject group from each of the four grouped input positions. The analysis of variance yielded a significant result for groups (F= 5.07, P-c 0.001) and for input position (P’= 26.28, P < O.OOOl), but no interaction (F= 0.79, P > 0.05). Neuman-Keuls comparisons showed that recall was
r Group N
Normal
LeftTemporal
25
RightTemporal
h
H
h
H
20
10
19
13
ClllltrOl
FIG. 4. Mean forgetting scores, showing memory the last learning trial. (h = small hippocampal
loss after 24 hr as a percentage of performance excisions; H = large hippocampal excisions.)
on
MARILYN JONES-GOTMAN
666
0-n
Normal Control
.-.
Lelt lemporal
0
--0
I.
-
-.
h----h
N-
75
h
N=
20
Let! Temporal H
N=
13
Right Temporal h
N = 20
Rlght Temporal H
N =
14
?/.I .‘.\
. .., ..,,,.,
/ -. ;i;-....~.-z.G”
\/
/’ ,’
,’
”
>
.
,’
,.....”
‘...’
,,
,’
:
..d’ ,,.... .’
,I’
,
. .._ o\
.//p’ ,,,,f’ .‘;
,,q
,’
I’
a”
,’
,’
Input
FIG.
5. Serial
function
PosItIon
position curve for the first learning trial: mean of input position in the series. (h = small hippocdmpal excisions.)
number of drawings recalled. as a excisions; H = large hippocampal
significantly higher from the last input positions (11-l 3) compared to all others (positions 1 l-1 3 vs positions 8-10, q= 6.89, PcO.01; positions 1 l-13 vs positions 4-6, q = 1 I. 15, P 0.05). Analysing performance by group, only the RTH group was impaired, and it differed significantly from each of the others (RTH vs NC, q = 6.24, P ~0.01; RTH vs LTh, q = 3.60, P-cO.05; RTH vs LTH, q=3.89, P-cO.05; RTH vs RTh, q=3.81, P-cO.05). As the input positions were collapsed for the group comparison, this finding parallels the one reported for trial 1 in the learning analysis; the difference is that the measure in this analysis was a simple count of recognizable drawings whereas in the other the quality of the drawings was taken into consideration. It had been predicted that the patients with a large right hippocampal-zone excision would be inferior to all other groups specifically on the initial items of the list: therefore, planned nonorthogonal comparisons were carried out to compare the performance of the RTH group to that of the four other groups (combined mean) for each input position. The results showed a highly significant impairment in the RTH group for the initial items of the list (RTH vs all other groups combined for positions 1 3, F= 12.59, P < 0.00 I). The difference between group RTH and the others on the two middle input positions just reached significance (positions 4 6, F=4.09, PcO.05; positions 8-10, F=4.3_5, PcO.O.5) while the difference on the final position was negligible (F= 1.36, P> 0.05).
RIGHT
Mnemonic
HIPPOCAMPAL
EXCISION
667
strategies
In order to estimate to what extent verbalization or other mnemonic aids were used in the learning task, each subject was asked after the delayed recall test what he or she had done to learn the designs. Seventy-four percent of normal control subjects reported using verbal strategies, compared with 50% in each of the right temporal-lobe groups, 55% of the LTH group and only 25% of the LTh group. A chi-square test performed on these data confirmed that a greater proportion of control subjects than patients attempted naming (x2 = 10.58, P
DISCUSSION As predicted, patients with a right temporal lobectomy were impaired on the design learning task: the patients with a large hippocampal removal obtained low recall scores during learning, they required more trials than did control subjects to reach criterion, and their recall after 24 hr was impaired. In contrast, patients whose right temporal-lobe excision encroached very little on hippocampal structures did not differ significantly from normal on any measure. These findings differ from those of a previous study in which subjects also had to copy and recall simple patterns, but in which recall was tested only once, unexpectedly, 45 min after the copy task [12]. In that experiment the RTh and RTH groups did not differ, and both were impaired. Considering only the first recall trial of the present study, there are two differences between the two experiments. The first is that learning was incidental in the previous study, whereas in the present one it was intentional; knowing that memory will be tested could prompt subjects to attempt a learning strategy, which could differentially help some subjects and exaggerate the differences between groups. The other difference between the studies is the time interval between copying the designs and recalling them. Perhaps a subtle memory deficit attributable to the temporal neocortex is brought out only by longer delay intervals, whereas hippocampal damage interferes significantly with memory even when the interval is short. An unexpected finding in this study was the impairment in the left temporal-lobe groups on the trials to criterion measure. Those groups showed the predicted normal performance on all other measures, but they tended to ‘hover’ near criterion, recalling only 10 or 11 drawings trial after trial. Furthermore, they recalled different drawings from one trial to the next, and all were recalled with normal accuracy. Thus their difficulty seemed to be an inability to access well-formed images that were in memory. One means of accessing images could be by a verbal label. Since a verbalizing strategy was used by most control subjects, it may be that dual encoding is necessary for normal performance on this task. If it is, then the slow mastery of the material might be attributed to inefficient verbal coding in the left temporal-lobe groups and to inefficient visual coding in the RTH group. This interpretation is consistent with a finding by JACCARINO that both a verbal and a visual code are necessary for normal recall of pictured objects [9, 201. A principal aim of this experiment was to determine the relative contributions of slow learning and rapid forgetting to the right temporal-lobe deficit in visual-pattern memory. The impairments in both learning and retention that were clearly demonstrated for group RTH, while group RTh was unimpaired, point up the importance of the hippocampal structures in this kind of task. One function that has been postulated for the hippocampus is
66X
MARILYN JONES-GOTMAN
that of organizing unstructured material in memory [I, 11,12, 36; but see 371. That hypothesis seems applicable to the design learning task. If one accepts an organization hypothesis, then the fact that the RTH group ultimately succeeded in learning the designs suggests that the memorandum eventually did become organized, mediated perhaps by hippocampal tissue remaining posterior to the excision, perhaps by the intact left hippocampus, perhaps by the frontal lobes [8, 221. Furthermore, the RTH group’s additional impairment in delayed recall suggests that that organization was probably atypical in some way; it is also possible that decay proceeds more rapidly when structural links are deficient. The serial position aspect of this experiment was exploratory. Other visual pattern serial position studies have differed from this one in several ways. They have used short lists 171, they usually used similar designs within a list [4, 241 and they never used free recall to test memory [4]; the serial position curves obtained were typically flat except for better recall of the final items [23, 311. Thus the present study was the first to require free recall of a long list of dissimilar designs. A recency effect was clearly demonstrated for all subjects with this paradigm, and there was also a tendency for patients with a small hippocampal excision to recall more designs from the first input position groups (items l-3) than from the second. This tendency was not seen in the normal control group, perhaps reflecting different strategies. POWELL et al. have shown in a verbal task that patients with a temporal-lobe lesion, often aware of their memory impairments, attempted to ensure some recall of a series by rehearsing the early items [25]. In contrast, the strategy typically used by the control subjects of the present study was naming, which would not systematically favor items from any particular position of the list. Unlike the subject in all the other groups, the patients of group RTH recalled essentially nothing from the beginning of the list. This result provides a right-hemisphere parallei to the depressed primacy effect on word lists reported by JAC‘CARINO-HIATT [IO] and READ [28] for patients with a left temporal-lobe lesion that included a large excision from the hippocampal zone. Furthermore, their findings that the amnesic patient, H.M., recalled only the last two or three items of a word list [lo, 281 was also replicated with the designs of the present experiment. H.M. was given a reduced set of six designs, and he recalled only the last one on every recall trial except the second. The failure of patients with hippocampal damage to recall early items is consistent with RAWLINS’ [26, 271 view of the hippocampus as a high-capacity intermediate-term memory buffer that holds memoranda for a relatively long time until associations can be formed between temporally discontiguous stimuli. Rawlins suggests that the capacity is greatly reduced after hippocampal damage, and that new information crowds out earlier items from the buffer. This view is consistent with the notion that the hippocampus performs an organizational function, and one can speculate further that when memoranda are ‘crowded out of the buffer’ they may not be lost altogether, but instead they may become stored in an unorganized or poorly organized form. This explanation could account for both the slow learning and the impaired recall of group RTH in the present experiment.
A~~now/edgem~nr.\~~This research was supported in part by operating grant MT 3624 awarded by the Medical Research Council of Canada to Brenda Milner. I am grateful to Dr. Theodore Rasmussen. Dr. William Feindel, Dr Andr& Olivier and Dr J.-G. Villemure for the opportunity to study their patients and for providing detailed descriptions of the surgical removals. 1 also thank Bessie Alivisatos, Jean Gotman and Brenda Milner for their valuable comments, and Rhonda Amsel for statistical advice.
RIGHT HIPPOCAMPALEXCISION
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