Neuropsychologia, 1978,Vol. 16,pp. 61 to 71. Pergamon Press.Printed in England.

RIGHT

TEMPORAL-LOBE MEDIATED

CONTRIBUTION VERBAL

MARILYN JONES-GOTMAN

TO IMAGE-

LEARNING

and BRENDA MILNER

Montreal Neurological Institute and Department of Neurology and Neurosurgery, McGill University, Montreal H3A 2B4, Canada (Received 2 August 1977) Abstract-The ability of patients with right temporal lobectomy to profit from visual imagery as a mediator in verbal paired-associate learning was investigated, using a 60-pair list of high-imagery words presented for one trial only. A group of 31 patients with right temporal lobectomy was impaired with respect to a matched normal control group in the recall of these image-linked pairs, whereas in a control experiment, in which pairs of abstract words had to be linked by sentences, the right temporal group showed normal recall. Further analysis revealed an inverse relationship between the extent of right hippocampal removal and the recall of the image-mediated, but not the sentence-mediated, pairs.

THERE is

by now abundant evidence for complementary specific memory defects after unilateral temporal lobectomy in human patients. Removals from the dominant hemisphere for speech impair the learning and recall of verbal material whether aurally [l-4] or visually [5, 61 presented, whereas right nondominant temporal-lobe excisions impair the recall [4, 7, 81 and recognition [8-121 of visual patterns that cannot be coded easily in words. One consequence of this material-specificity is that patients with unilateral lesions can, if time permits, have recourse to mnemonic strategies to minimize their memory defects. Thus BOLLER and DE RENZI [13, 141 found that patients with right posterior brain lesions were able to use verbal labels to mediate associative links between pairs of nonsense drawings, although such patients showed poor memory for this kind of material on a task where the inspection time was too short to allow for verbal coding. Similarly, patients with lefthemisphere lesions can learn to use visual images to aid verbal recall. This was first demonstrated by PATTEN [ 151 for aphasic subjects and more recently by JONES [16], who found that patients with left temporal-lobe lesions could use visual imagery to improve performance on a verbal paired-associates task, though not to reach a normal level. The differential vulnerability of verbal and pictorial memory to lesions of the left and right temporal lobes, respectively, accords well with experimental findings in normal subjects that point to the use, where possible, of a dual memory code, verbal and imaginal [17-221. On this view, the well-known fact that concrete words are easier to recall than abstract words of equal frequency in the language would be largely due to the greater image-evoking power of the concrete words [23]. When this is exploited by instructions to use images as mediators in a verbal-learning task, a considerably higher and more stable level of recall is achieved [17, 18, 22, 24, 251. If the right temporal lobe plays a major role in visual memory processes, then it should be possible to demonstrate an impairment after right temporal lobectomy on verbal recall tasks that foster the use of imagery in normal subjects. 61

62

MARILYNJONES-GOTMAN and BRENDAMILNER

This hypothesis could not be confirmed in JONES’S study [16], where no difference was found between the performance of patients with right temporal-lobe lesions and normal control subjects in learning (over 3 trials) a list of 10 paired associates with image-mediation. In this case, however, a ceiling effect for both groups obscured any differences that may have existed in the ability to profit from imagery. The present investigation explores the question further in two experiments, the second a control for the fist. Experiment 1 challenges the subject’s imagery capacities with a 60-pair list of concrete words to be learned with image-mediation in one trial. Presumably any inferiority of patients with right temporal lobe lesions in the ability to use imagery should emerge in this more demanding task. A left temporal-lobe group is included to give perspective to the results through the magnitude of their deficit on what remains primarily a test of verbal learning. Experiment 2 calls on a different associative-learning strategy, that of sentence-mediation [26, 271, and the word pairs to be learned are abstract. Whereas visual imagery is a more effective mnemonic than a sentence for learning concrete words [27], abstract words do not readily elicit images and hence sentence mediation becomes the more effective learning technique [28]. Patients with right temporal-lobe lesions are expected to perform normally on this strictly verbal task. EXPERIMENT

1: LEARNING CONCRETE IMAGE-MEDIATION

WORD-PAIRS

WITH

Subjects

The experimental groups comprised 45 patients at the Montreal Neurological Hospital who had undergone a unilateral anterior temporal lobectomy for the relief of intractable epilepsy; 31 removals were from the right hemisphere, 14 from the left. In all cases the preoperative cerebral lesions had been well-lateralized, with no evidence of damage to the other side, and all lesions were static and atrophic. The right and the left temporal-lobe groups each included one case of arteriovenous malformation and one of pial angiomatosis forme fruste [29]. Although nine patients were left-handed or ambidextrous, all were left-hemisphere dominant for speech, four subjects having been excluded because preoperative intracarotid Amytal* tests [30,31] had disclosed an atypical pattern of speech representation. Thirteen patients in the right temporal-lobe group and three in the left were tested 2f weeks post-operatively; all other patients were seen in follow-up study one or more years after surgery. Right temporal-lobe group. For the 31 patients tested after a right temporal lobectomy, the mean extent of cortical excision measured along the right Sylvian fissure was 5.9 cm, ranging from 4.5 cm to 9.0 cm, and the mean extent along the base of the brain was 6.3 cm, ranging from 5.0 cm to 9.0 cm. The amygdala was reported to have been removed completely in 25 cases and partially in the remaining 6. In 5 cases the hippocampus was also radically excised and 19 of the others had varying degrees of hippocampal destruction. Leji temporal-lobe group. Because we realized that the verbal-learning task proposed would be too difficult for most patients with left temporal-lobe lesions, only 14 of 30 patients available were tested. Selection was based on their performance on the verbal memory tasks that all patients receive routinely [4]; only those scoring above the average of our larger left temporal-lobe group were included in the present study. In these 14 selected patients tested after a left temporal lobectomy, the mean extent of removal along the left Sylvian fissure was 4.6 cm, with a range from 3.0 cm to 6.0 cm, and the mean extent along the base of the brain was 5.3 cm, with a range from 4.5 cm to 6.5 cm. The amygdala was reported to have been removed completely in 13 cases and partially in one. The hippocampus was radically excised in four cases and partially in seven. Normal controlgroup. Because the most important comparison was to be that between the right temporallobe and the normal control groups, the control subjects were chosen to match the right temporal-lobe patients as closely as possible with respect to the distribution of age, sex, education and occupations. The sex distribution, mean age and mean full-scale Wechsler I.Q. ratings of the 45 temporal-lobe patients, grouped according to side of lesion, are shown in Table 1, as are the corresponding sex and age data for the 31 normal control subjects. No intelligence ratings were obtained for the latter group. *Sodium amobarbital-Sodium

Amytal, Eli Lilly and Company, Indianapolis,

Indiana, U.S.A.

RIGHT TEMPORAL-LOBE

CONTRIBUTION

Table 1. Concrete paired-associates

TOIMAGE-MEDIATF,D VERBALLEARNIKG

task: sex, age and intelligence data for the three subject groups

Sex Group Normal control Right temporal Left temporal

M 22 23 7

63

Age F 9 8 7

Mean 21.7 28.4 24.0

Range 18-47 18-46 16-31

Wechsler I.Q. Mean Range Not assessed 114.4 89-146 111.9 loo-129

Test materials

A list of 60 paired-associates was prepared, using 120 words rated high in imagery as determined from the norms of PAIVIO, YUILLE and MADIGAN [23]. All words were rated above 6.0 on a 7-point scale for imageevoking properties, with a mean of 6.48 and a range from 6.07 to 6.87. In order to avoid introducing words that some subjects might not know, only items with medium to high Thorndike-Lorge frequencies were chosen: 73 of the words had A or AA frequency ratings; the remaining 47 had a mean rating of 24.9, ranging from 10 to 49. The words were paired at random, except that no two words of a pair began with the same letter, nor did they have obvious semantic or acoustic similarities. The resulting pairs, although consisting of common words, were thus difficult to associate and to remember. Procedure

Subjects were told that a list of words would be read to them, two at a time, and that they were to listen carefully and to remember which words were said together. They were told that the list would be long, that it would be read to them only once, and that they must employ a special trick to help them remember how the words were paired. The way to use visual imagery as a mnemonic aid was then explained, and subjects were encouraged to make bizarre or funny images showing an interaction between the objects represented. At this point drawings representing the word pairs nail-salad and telephone-magazine were sketched as concrete examples of how interactive images might be formed in response to pairs of words. Subjects were told that they would be given 10 set for each word-pair, and that during that time they should conjure up an image and concentrate on it until they were given the next pair. Immediately after the list had been presented, the subjects were given a cued recall, in which the first word of each pair was read and they were required to respond with the second. A non-correction procedure was used throughout, and the order of presentation of the pairs for recall differed from that of the original presentation. A second cued recall (but with the order of items again changed) was obtained without warning 2 hr after the beginning of the test. The delay period was typically filled by unrelated nonverbal tasks, and there were no systematic group differences with respect to this interpolated activity.

RESULTS Figure 1 depicts the mean number of correct responses for the three groups in immediate and delayed recall, respectively. The figure shows the performance of the right temporallobe group to be consistently inferior to that of the normal control group, but still markedly superior to that of the left temporal-lobe group, who have a selective impairment of verbal memory. A two-way analysis of variance revealed significant differences for groups (F = 16.48, P < OXtOl)but not for recall conditions (P = 3*31,0*10 > P > O.OS), and there was no significant interaction (I? = 1.90). Subsequent 1 tests showed the difference between the right temporal-lobe and normal control groups to be significant both in immediate recall (t = 3.79, P < O-001) and at delay (t = 5-78, P < O+Ol). From Fig. 1 it might appear that the scores of the right temporal-lobe group dropped at delayed recall not only more than those of the control group, but also more than those of the left temporal-lobe group. The latter group, however, fell from a much lower original level of learning. For statistical treatment, the drop in score was expressed as the ratio of the amount of forgetting to the level of original learning, this ratio being calculated separately for the patients of each of the three groups and subsequently submitted to an analysis of variance. The group differences were significant (F = 18.26, P < 0~001). Individual

MARILYN JONES-GOTMANand BRENDA MILNCR

64

Narmol Control (N-31)

Righf Temporal (N=31)

Left Temporal (N=l4)

0

10

Mean FIG.

20

NO. Correct

30

Responses

40

50

(Max=60)

I. Concrete paired-associates

task. Mean number of correct responses for the three groups at immediate recall and after a 2-hr delay.

t tests revealed that this effect was attributable solely to differences between the normal control group and each temporal-lobe group (t = 5.16, P < 0.001, left temporal group; t = 5.77, P < OGOl, right temporal group); the difference between the two temporal-lobe groups was not significant (t = 1.18). Recall as related to extent of hippocumpal removal. To investigate the possible role of mesial temporal-lobe structures in immediate and in delayed recall, each of the two patient groups was then divided into two subgroups; in one the hippocampus was either spared or the removal did not exceed 1 cm of the body (subgrcup h); the other subgroup was composed of the remaining patients, all of whom had hippocampal removals that included at least 1 cm of the body (subgroup H). For the patients with right temporal-lobe lesions, 21 were in subgroup h and 10 in subgroup H. There were eight patients in the left temporallobe subgroup h and six in subgroup H. These subgroups, together with the normal control group, were compared in an analysis of variance on the two recall conditions. This analysis yielded a significant effect for groups (F = 9.03, P < 0.001) but not for recall conditions (F = 3.22), and no interaction (F = 0.97). There was no effect of extent of hippocampal removal for the left temporal-lobe patients (t = 0.56 immediate recall; t = 1.57 delayed recall). In contrast, for the right temporal-lobe subgroups, those patients with large hippocampal removals had significantly lower scores than those with small, in both immediate (t = 2.72, P c: 0.01) and delayed (t = 3.09, P < 0.01) recall. Nevertheless, both the right hippocampal subgroups (H and h) were impaired relative to the normal control group in both recall conditions. (For immediate recall, t = 4.59, P < 0.001 subgroup H; t = 2.21, P < 0.05 subgroup h. For delayed recall, t = 6.29, P < 0.001 subgroup H; t = 3.71, P < 0.001 subgroup h.) Relation to temporal neocortex. For each patient group the relationship between recall score and extent of neocortical excision (measured both along the Sylvian fissure and along the third temporal convolution) was assessed for both immediate and delayed recall. In no case was a significant correlation found. For the right temporal-lobe group in immediate recall the product-moment coefficients were -0.13 for the Sylvian fissure and -0.28 for the third temporal convolution. The corresponding figures in delayed recall were -0.12,

RIGHT TEMPORAL-LOBE

CONTRIBUTION

TO IMAGE-MEDIATED

VERBAL LEARNING

65

and - O-31. For the left temporal group, the coefficients for immediate recall were - 0.01 (Sylvian fissure) and - 0.20 (third temporal convolution); and for delayed recall the values were - 0.08 and -0.25, respectively. Thus for the left temporal-lobe group, there was no relationship between test performance and extent of removal, either mesial or lateral. No relationship existed for the right temporal-lobe group between performance on the test and the extent of lateral neocortical removal, but the efficiency of recall was inversely related to the amount of hippocampal tissue excised. The results of this experiment will be discussed together with those of the next one, as the two studies are complementary. EXPERIMENT

2 : LEARNING WITH SENTENCE

ABSTRACT WORD-PAIRS MEDIATION

In this experiment, subjects were required to learn two lists of abstract word pairs, the first without instructions as to how the words were to be associated, the second with instructions to invent sentences incorporating the words of each pair as a memorizing strategy. Ideally these lists of abstract words would have been as long as the concrete word list and would also have been presented for only one trial, but a pilot study showed that such lists would have been too difficult to yield meaningful data. Accordingly the lists were shortened to ten pairs each and three learning trials were given on each list, to ensure a reasonable level of acquisition. Even with this reduction in list-length, the task remained at least as difficult for normal subjects as the concrete paired-associates had been and thus was an adequate control for it. The abstract verbal-learning task was considered too stressful for even our selected group of patients with left temporal-lobe lesions; consequently, only the right temporal-lobe and normal control groups were tested. As in Experiment 1, these two groups were appropriately matched, although fewer subjects were tested on the abstract pairs because this task was added later. Subjects Table 2 gives the sex distribution and mean ages of the 20 normal control subjects and of the 17 patients tested after a right temporal lobectomy, as well as the mean Wechsler I.Q. rating of the latter group. All subjects had already completed Experiment 1. Table 2. Abstract paired-associates

task: Sex, age and intelligence data for the two subject groups

Sex Group Normal control Right temporal

M 13 9

Age F 7 8

Mean 26.1 261

Range 1847 18-46

Wechsler I.Q. Mean Range Not assessed 115.4 102-146

Test materials Two lists of 10 word pairs were constructed, all 40 words having low (below 4.0) imagery ratings [23]. List I had a mean rating of 3.31, ranging from 2.50 to 3.73 ; List II had a mean of 3.29, ranging from 2.20 to 3.83. An attempt was made to select words with the highest Thorndike-Lorge frequency ratings, but this was not altogether feasible. List I had 8 A or AA words: the ratings of the remaining 12 words ranged between 2 and 39 with a mean of 19.8. List II had 14 A or kA words; the ratings of the iemaining 6 words ranged between 1 and 23 with a mean of 17.2. In forming the word pairs, A and AA words were always used as the response members of the pairs. Care was taken that no two words should begin with the same letter, and semantic or acoustic similarities between words of a pair were avoided. Except for these precautions, the words were paired randomly.

66

MARILYNJONES-GOTMAN and BRENDAMILNER

The first list was meant to provide a baseline of the subject’s ability to learn abstract paired-associates. The second list tested the efficacy of sentences as a verbal mnemonic, and to this end subjects were instructed to invent and use meaningful sentences incorporating the two words of each pair. Procedure List I: Rote learning. List I was introduced

simply as pairs of words that must be remembered, with no mention as to how this should be achieved. Examples of advantage-occasion and excuse-rhoughf were given to acquaint subjects with the nature of the material and to illustrate the procedure to be followed. There were three learning trials. On the first presentation, the list was read at the rate of one pair every 10 set and, on subsequent trials, at the rate of one every 5 sec. Each list-presentation was followed by a cued recall, and, throughout the test, if a subject answered incorrectly or failed to respond within 15 set, he was told the correct word (correction procedure). A different order of presentation was used on each learning trial and on each recall. List II: Sefzfence mediation. List II was described as being similar to List I, except that a special method was to be used to learn the pairs. At this point the idea of using a meaningful sentence as a mnemonic was first introduced, and the two previous examples, this time linked in sentences, were used as illustrations. Completely abstract sentences were offered as examples (e.g. “the e.ycuse for his thought was made public”) in order to discourage subjects from incorporating into their own sentences ideas that could be easily pictured. The same procedure was followed for List II as for List I, except that before each presentation of the list, subjects were reminded to make (presentation 1) or to rehearse (presentations 2 and 3) sentences embodying each word pair. Two hours after the beginning of the experiment the subjects were tested again, without warning, on both lists. The treatment of the groups during the delay interval was the same as for the concrete paired-associates task. Recall was cued at delay, as it had been in the immediate-recall tests, but this time no correction procedure was used. RESULTS

Figure 2 compares the learning curves and the mean delayed-recall scores of the right temporal-lobe and normal control groups under the two test conditions. For List I, the learning curves of the two groups are almost superimposed; on the second list it appears as though the right temporal-lobe patients performed at a slightly higher level than the control subjects on each of the three learning trials and at delayed recall. The consistent separation of the two groups in the sentence-mediation condition is, however, deceptive, because there are large standard deviations at all points of the curves for this difficult task. Analysis of variance comparing the performance of the two groups on the three learning trials of

I”, ..L.. i ;‘.>I ia‘

;

_/ _ ’ _“..L.._1. L‘dlO , : I’ i

&_A_!

L._J_.__.L-Lr, * 3 IL

FIG. 2. Abstract paired-associates task. Learning curves and delayed-recall scores for Lists I and II, showing the mean number of correct responses per trial for the two groups.

KIGHT

TEMPORAL-LOBE

CONTRIBUTION

TO IMAGE-MEDIATED

VERBAL

LEARNING

67

each list revealed no significant differences for groups (F = 0.67), or for lists (F = l-77) and no groups x lists interaction (F = 2.23). It is clear from Fig. 2 that the performance of the two groups was also similar in delayed recall of the lists. Analysis of variance on the delayed-recall scores for the two lists revealed no difference between the groups (F = 0.29) but a significant difference between lists (F = 9.41, P < O.Ol), and no interaction (F = 0.20). Thus the advantage of the sentence mnemonic is only apparent on delayed recall. The amount of forgetting from immediate to delayed recall was explored by an analysis of variance comparing the two groups in their drop from the third learning trial of each list to its corresponding delayed-recall score. There was no difference between groups (F = 0.05) or lists (F = 3.95), although the interaction was significant (F = 4.69, P < 0.051, reflecting a slightly greater retention by the normal control group of List II, compared to List I. Thus, no difference has been found between the right temporal-lobe and normal control groups in learning abstract paired-associates either with or without the verbal mnemonic, whereas there were significant differences between these groups for concrete paired-associate learning. To make sure that these differing results in the two experiments were not merely an artefact of sampling, an additional analysis of concrete paired-associates was made, including only those subjects who had been tested on the abstract pairs. The significant group differences seen in the analysis of variance on the larger sample remained true for the subset of that sample: the right temporal-lobe group was impaired in immediate (t = 3.50, P < 0.01) and in delayed recall (t = 7.79, P < 0.001). Recall as dated to extent of hippocampal removal. As in the previous experiment, the effect of hippocampal removal was investigated by subdividing the patient group into those patients with large (H, N = 6) and those with small (h, N = 11) hippocampal excisions. The scores of these two subgroups and of the normal control group on the summed learning trials of List I and of List II were then submitted to analysis of variance. There was no difference between groups (F = 0.43) or between lists (F = I*%), and no interaction (F = 1.70). The corresponding analysis for their delayed-recall scores also showed no difference between the groups (F = 0.23), but the list effect was significant (F = 9.60, P < O.Ol), reflecting again the higher delayed recall of the word-pairs learned with the sentence mediator. There was no interaction (F = 0.95). Relation to temporal neocortex. To determine whether recall was related to the extent of neocortical excision, correlational analyses were made for the right temporal group between recall scores and extent of removal along the Sylvian fissure and along the third temporal convolution. For the Sylvian fissure there were no significant correlations with the summed learning trials of List I (r = 0.34, t = 1.40, 0.50 > P > 0.20), nor of List II (r = O.OO), nor with the delayed recall of List I (r = 0.29), nor that of List II (r = - 0.13). Likewise, there was no significant correlation with the extent of removal along the third temporal convolution for the summed learning trials of List I (r = 0.44, t = l-89,0.20 > p > O.lO), nor for those of List II (r = 0*05), nor for the delayed recall of List I (r = 0.32), nor that of List IT (r = -0.02).

DISCUSSION The findings of these two experiments are clear; whereas the patients with right temporallobe lesions performed normally in both immediate and delayed recall of the abstract

68

MARILYN JONES-GOTMAN

and

BRENDA

MILNER

paired-associates, they were impaired in both recalls of the concrete. The difference is not due to the fact that the abstract-words task extended over three trials, as there were no group differences on the first learning trial, when the conditions were more directly comparable to those for the concrete pairs. The lack of any impairment after right temporal lobectomy on either version of the more difficult abstract-learning task shows that the right temporal and normal control groups were indeed suitably matched and that therefore the deficit found for the concrete pairs must be attributed to its visual component, the imagery mnemonic. The results for concrete paired-associates point to the importance of the right hippocampal region for image-mediated verbal learning. Although both right temporal-lobe subgroups were impaired in immediate and in delayed recall of the concrete words, the deficits were significantly greater for the subgroup with large hippocampal lesions than for that with small. In this experiment, as in those cited below, it is not clear whether the hippocampus itself or the parahippocampal gyrus is the critical structure, nor do we know whether the same impairment would be found with a removal that spared the temporal pole and amygdala. The right hippocampal effect observed in the present study was not specific to pairedassociate learning, for a similar result was obtained on an incidental verbal-learning task embodying image-mediated free recall [32]. These findings add to the number of investigations showing specific memory defects after unilateral temporal lobectomy that are either contingent upon [33, 341 or accentuated by [3, 11, 35, 361 removal of the hippocampus and neighboring tissue. They are also consistent with the observation [16] that images are forgotten as quickly as words in the amnesic syndrome resulting from bilateral medial temporal-lobe lesions (as is also the case for some [37], but apparently not all [38], amnesias of different etiology). Nevertheless, this result had not been predicted, because until now those visual memory tasks on which the severity of deficit after right temporal lobectomy had been most clearly linked to the amount of hippocampus excised had involved either sequentially organized material [3, 33, 34, 391 or such perceptually simple memoranda as the position of a spot on a line [3, 351, although a similar effect had been found on one test of face recognition [I I]. In contrast, the right temporal deficit in memory for abstract visual patterns has always appeared to be unrelated to the extent of hippocampal removal. This is true for the ability to recognize recurring nonsense figures [9] and for the free recall of the Rey-Osterrieth figure [40, 411, an elaborate geometric design that is copied and then reproduced from memory 40 min later without forewarning [7, 81. The Rey-Osterrieth task is given to all our patients [4] and thus we could ascertain whether the right hippocampal effect demonstrated above for image-mediated verbal recall reflects a difference in task-demands or merely one in patient sampling. The former appears to be the case. When the data for the present right temporal-lobe group on the Rey figure were analyzed with respect to the role of the hippocampus, we found no difference in delayed-recall scores between the subgroup with large and that with small hippocampal removals. Both were impaired, the mean recall score of subgroup H being 52% and that of subgroup h 49x, contrasting with the normal score of 76% achieved by the left temporallobe group. These results replicate TAYLOR’S [7] earlier findings and raise the question of how these two recall tasks differ. One possible divergence is in the accuracy of visual detail required for success on the task, MILNER [42] has suggested that recall or recognition tests that demand careful per-

RIGHT TEMPORAL-LOBECONTRIBUTIONTO IMAGE-MEDIATED VERBALLEARNING

69

ceptual analysis of new visual patterns depend at least as much for their performance upon the integrity of the right temporal neocortex as upon that of the right hippocampus. The Rey-Osterrieth test (like Kimura’s recurring nonsense figures) falls into this category, whereas the re-evocation of a self-generated visual image probably does not, even though such images may be regarded as complex. A second major difference between the two recall tasks may lie in the amount of proactive and retroactive interference generated by each. The Rey figure is a cohesive unit in which recall of one part is likely to aid rather than interfere with recall of another. In contrast, interference must play a large part in the imagery task, where 60 unrelated word pairs are presented in rapid succession and recall of the associations is tested in a random order imposed by the experimenter. The fact that in this case the magnitude of the performance deficit after right temporal lobectomy does depend on the extent of hippocampal removal suggests that the hippocampal region may indeed be involved in the inhibition of potentially disrupting influences on the newly formed trace [3, 431 or, possibly in the suppression of competing responses at the time of recall [44, 451. Finally, although no quantitative relationship was found between extent of neocortical removal and performance on the imagery task, evidence for a temporal neocortical contribution is strong, since patients were impaired after right temporal lobectomy even with the hippocampus intact. Acknan,ledgements-This work is based upon a thesis submitted by MARILYN JONES-GOTMANin May, 1975 to McGill University in partial fulfillment of the requirements of the Ph.D. degree. The research was supported by operating grant MT2624 from the Medical Research Council of Canada to BRENDA MILNER. We wish to thank Dr. THEODORE RASMUSSEN, Dr. WILLIAM FEINDEL, Dr. CARL DILA and Dr. ANDRE OLIVIER for inviting us to study their patients, and JEAN GOTMANfor analyzing the data by computer.

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9. 10. II. 12. 13. 14. 15.

MEYER, V. and YATES, H. J. Intellectual changes following temporal lobectomy for psychomotor seizures. J. Neurol. Neuromrg. Psychiat. 18, 44-52, 1955. MILNER, B. Psycholonical defects vroduced bv_ temvoral-lobe excision. Res. Publ. Ass. Res. new. ment. . Dis. 36;244-257, 195% CORSI, P. Human memory and the medial temporal region of the brain. Unpublished Doctoral Thesis, McGill University, 1972. MILNER, B. Psychological aspects of focal epilepsy and its neurosurgical management. In Advances in Neurology, D. P. PURPURA, J. K. PENRY and R. D. WALTER (Editors), Vol. 8, pp. 299-321. Raven Press, New York, 1975. MILNER, B. Brain mechanisms suggested by study of the temporal lobes. In Bruin Mechanisms Underlyirzg Speech andLanguage, F. L. DARLEY (Editor), pp. 123-145. Grune & Stratton, New York, 1967. BLAKEMoRE, C. B. and FALCONER, M. A. Long-term effects of anterior temporal lobectomy on certain cognitive functions. J. Neural. Neurosurg. Psychiut. 30, 364-367, 1967. TAYLOR, L. Localisation of cerebral lesions by psychological testing. C&z. Neurosurg. 16,269-287, 1969. MILNER, B. and TEUBER, H.-L. Alterations of perception and memory in man : reflections on methods. In Analysis of Behavioral Change, L. WEISKRANTZ (Editor), pp. 268-375. Harper & Row, New York, 1968. KIMURA, D. Right temporal-lobe damage. Archs Neural. 8,264-271, 1963. PRISKO, L. Short-term memory in focal cerebral damage. Unpublished Doctoral Thesis, McGill University, 1963. MILNER, B. Visual recognition and recall after right temporal-lobe excision in man, Neuropsychologiu 6, 191-209, 1968. WARRINGTON, E. and JAMES, M. An experimental investigation of facial recognition in patients with unilateral cerebral lesions. Cortex 3, 317-326, 1967. BOLLER, F. and DE RENZI, E. Relationship between visual memory defects and hemispheric locus of lesion. Neurology 17, 1052-1058, 1967. DE RENZI, E. Nonverbal memory and hemispheric side of lesion. Neuropsychologiu 6, 181-189, 1968. PATTEN, B. M. The ancient art of memory. Archs Neural. 26,25-3 I, 1972.

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in retention by rats with hippocampal

lesions. J. camp. physiol.

RIGHT

RBsume -__

TEMPORAL-LOBE

CONTRIBUTION

TO IMAGE-MEDIATED

WRBAL

LEARNING

71

:

On a 6tudi6 imagerie, subi une

au moyfn

lobectomie

temporal@

en tant que mediateur verbales. etait

Un groupe

d&fici:aire

liste

rience

de contrdle

normal. inverse

et le rappel n'existait

dans

avec

d'association

droite

pour

ic

l'imagcrie

tandis

laquellf

les pairfs

de riots abstraits

religes

les paires

13 grcupc

ulterieurc

ei:tr@ l'itendue

Deutschsprachige

de paires

tfnporalf

de contr5les

montrlit

de l'ahlation par

l'imogerie

rcli.&s

par

ayant

visuelle

par

Une anslyse

pas pour

?i haute

des malades

l'imagerie

lohectomie

par des phrases,

des paires

q~e dens une exp&-

temporal qu'il

existait

hippocampique mais

devaient

droit

avait une

droite

que cette

relation

les p:l;-ases.

Zusammenfassunc

I3ei rechts-temporal

lobektomierten

keit, die optische Vorstellung assoziativen

2 utiliser

l'apprentissage

reli&zs

en relation

un rappel

droite

de mats

la capacite

par rapport_ 2 un groupf

de ces paires

etre mises

dans

de 60 paires

reprise,

de 31 maladcs

rappel

relation

d'une

priSsent6es .S uric seule

Patienten

als Vermittler

Lernen zu nutzen, untersucht,

nit 60 Wortpaaren

hut-de die Fahigbairn verbal-

indem eine Liste

mit hohem optischen Vorstellungsgehalt

verwandt wurde. Die Liste wurde nur einmnl pr~~sentiert. Eine Gruppe von 31 rechts-tempcrai

lobektomierten

sich gegentiber einer cntsprechenden beim Evozieren

dieser vorstellungsgebundenen

gemindert, wghrend

Patienten

Kontrollgruppe

dieselbe rechts-temporale

Paare

leistungs-

Gruppe in einem

Kontrollexperimen-t, in welchem Pnare a‘cstrakter Ydrter Satze zu verbinden waren, normale Leisturgen weitere

Analyse deckte ein umgekehrtes

dem AusmaR rechts-hippocampaler Abrufleistungen mittelten

Leistungen

durch

aufwies. Die

Verhsltnis

Substanzminderung

zwischen und den

auf, die durch die optische Vorstellung

mittelt waren, w5hrend

zeigte

Gesunder

ver-

dies nicht bei den durch Satze ver-

der Fall war.