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The effect of inferotemporal lesions on memory for visual stimuli in rhesus monkeys
Brain Research, 77 (1974) 4 5 1 4 6 9
451
© Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands
THE EFFECT OF I N F E R O T E M P O R A L LESIONS ON MEMORY VISUAL STIMULI IN RHESUS MONKEYS
FOR
P. D E A N
Department of Experimental Psychology, Oxford OX1 3PS (Great Britain) (Accepted April 24th, 1974)
SUMMARY
To test the hypothesis that inferotemporal ablations impair memory for visual stimuli, rhesus monkeys were trained to a criterion of stable performance on delayed matching from sample. Four colours were used as samples, and either 2 or 4 as retrieval cues. Inferotemporal removal initially affected matching performance at all delays, including zero, and for both retrieval conditions. However, when animals had been retrained to criterion on zero delay 4-alternative matching, they very rapidly achieved preoperative levels of performance at all delays. It is concluded that the deficit obtained by Bufferya on 4-alternative delayed matching reflected the inferotemporals' inadequate learning of the basic zero delay 4-alternative task; and that inferotemporal removal probably has no effect on the ability to remember visual stimuli.
INTRODUCTION
Why do inferotemporal lesions in monkeys impair visual discrimination learning? Present evidence indicates that they do not cause sensory or perceptual disturbances 8,14. Perhaps, therefore, the defect is in remembering visual stimuli, as has frequently been suggestedS,20, z4. Tests of this idea have typically measured the retention of previously learnt object discriminations3,15-17, with results that are not easy to interpret. However, such tests require the animal to remember at least two different kinds of information: purely visual information about the appearance of the objects (which object is which), and information about object-reward associations (which object is the positive one). Memory for the first may be called visual stimulus memory, for the second, visual association memory. A task that would seem to test visual stimulus memory but not visual association memory is delayed matching from sample, since in this paradigm no one sample is more associated with reward than any other. The animal cannot, therefore, use stimulus-reward information to bridge the delay
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between sample presentation and the appearance of the matching cues, but must relay on visual stimulus memory alone. Delayed matching from sample may thus be a suitable paradigm for testing the hypothesis that inferotemporal ablations impair memory for visual stimuli. A series of experiments using this idea was carried out by Buffery1,2 (described in ref. 25). His most interesting finding was obtained with 4-alternative delayed matching from sample, in which the sample could be any one of 4 colours, all of which appeared at the end of the delay. Length o f delay was titrated, i.e., it was increased when an animal got two consecutive matching responses correct, and decreased when it made an error. This had the effect of stabilizing the animals at those delays after which they could score about 70 ~ correct. Buffery found that baboons with inferotemporal lesions could not tolerate such long delays as normal animals. This was only true for 4 alternatives; with 2 or 3 alternatives the animals with irlferotemporal lesions were not significantly worse than the controls. This suggested that inferotemporal ablation did indeed cause a defect in visual memory which became apparent when the amount of information to be remembered increased. However, another interpretation of these results is possible. Four-alternative delayed matching from sample is more difficult to learn than 2- or 3-alternative matching. It has been clearly established that the learning impairment produced by inferotemporal ablation is more pronounced the more difficult the task. It is therefore possible that the operated animals in Buffery's experiment were worse than normal animals because they had not learnt the basic 4-alternative task so well, an effect obscured by the use of the titration schedule. If this were true, no conclusion about the effect of inferotemporal lesions on visual memory could be drawn from Buffery's results. The present experiment was designed to allow for the effects of slow learning by the operated animals. Firstly, they were required to meet a very stringent criterion at zero delay with 4-alternative matching, to ensure that they had learnt the basic task. Secondly, a constant delay paradigm was used, so that performance could be measured at several values of delay. If, despite the stringent criterion, the animals with inferotemporal lesions were nonetheless insufficiently familiar with the basic task, they would be impaired at all values of delay, not just at long ones. Thirdly, an attempt was made to measure asymptotic delay performance, i.e. delay performance that was no longer improving, by having the animals meet a criterion of stable performance on the constant delay paradigm. One other change was made from Buffery's experiment. Delay performance was measured in the same animals before and after inferotemporal removal. Effects of the operation that were small compared with the between-animal variance could thus be detected, and conversely an absence of effect demonstrated more convincingly. METHOD
Subjects The subjects used were 5 immature rhesus monkeys, 2 male and 3 female. They
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
453
had previously been trained on object and pattern discriminations, and had had extensive experience of delayed matching from sampleL Two were unoperated, but the other 3 had bilateral lesions of the superior temporal gyrus, sparing primary auditory cortex 9. However such lesions appear to have no effect on visual tasks 7,1°,1a, and these particular animals had been shown to be no worse than normals on delayed matching from sampleL All the animals were fed about 22 h before testing, being given as much food as was consistent with their working reliably.
.Apparatus The animals were tested in a transport cage, one side of which was removed to allow access to a 61 cm × 61 cm testing display. Throughout the experiment the cage was lit by dim overhead light (5-8 W) and masking white noise was provided. The testing display consisted of 5 circular transparent response keys mounted in a horizontal row 25 cm above the transport cage floor. Each key was 3.3 cm in diameter, and was mounted 7.5 cm, centre to centre, from its neighbours. There was also a foodwell, 17 cm below the centre key. A Grason-Stadler in-line digital read-out unit (E-4580/3) was mounted behind each response key and programmed to give any one of the following colours: blue (Ilford filter 304), green (Ilford 404), red (Ilford 204 plus Wratten 29) and yellow (Ilford 104). The unit behind the centre key was also programmed to give a white star, which was the 'ready' signal. An Advance SC-2 Timer was used to measure the animals' reaction times to the match stimuli. This timer was started when the match stimuli appeared and stopped when a response to them was made. All programming equipment used was G r a s o n Stadler series 1200, except for 5 switches that determined which colour appeared on each response key, and these were set by hand. The animals' behaviour during testing was watched on closed circuit television.
Procedure The animals were first trained to a criterion of 90 correct out of 100 trials on zero-delay matching from sample with 4 alternatives. The start of a trial was signalled by the appearance of the white star on the centre key. When this was pressed one of the colours (red, blue, green or yellow) appeared in its place as the sample and remained for at least 0.5 sec, after which a second press turned offthe sample and immediately (i.e., after 0 sec delay) turned on the match stimuli. These were all the 4 colours, and they appeared on the 4 outside response keys in positions that varied randomly from trial to trial. A correct response was a press to that response panel which was the same colour as the sample; an incorrect response, one to any other panel. Either response produced a 7.5 sec time-out in which no panel was lit, and no further press effective; in addition, a correct press was rewarded with a CIBA 190 mg banana pellet, and 2 sec of background illumination in the foodwell, whereas an incorrect press turned the overhead light out for 7.5 sec. At the end of the time-out the white star reappeared on the centre key. When the animals had reached the criterion on this problem they were put on the
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constant delay schedule. In this, the daily session consisted of 160 trials, preceded by 10 warm-up trials at zero delay, details of which were not recorded. The programming of the sessions was arranged as follows. Each daily session consisted of an 80-trial block, repeated once. The 80 trials in turn comprised 10 8-trial blocks. Either 2 or 4 retrieval cues could appear at the end of 4 different delays (O, A, B and C) giving rise to 8 possible conditions, 2-0, 2-A, 2-B, 2-C, 4-0, 4-A, 4-B and 4-C. Every 8-trial block consisted of one trial from each of these conditions in random order. In the two-alternative condition, the sample was paired at the retrieval stage with one of the other 3 colours at random, and the position of the 2 on the 4-response panels was also random. Over the first 20 daily sessions, for every condition (a) each of the 4 colours appeared equally as often as the sample, and (b) the correct match colour, and each incorrect match colour, appeared equally as often at each of the 4 response positions. These 20 sessions were then repeated in the same order indefinitely. All animals were started off with A -- 1 sec, B = 2 sec, and C = 5 sec (O was always 0 sec for all conditions). These were increased after a block of 5 160-trial sessions if during that block the animal had averaged fewer than 20 errors per session. Five sets of delay values were used: (0, 1, 2, 5), (0, 2, 5, 10), (0, 5, 10, 20), (0, 7.5, 15, 30) and (0, 15, 30, 50). It turned out that no animal deteriorated with time such that he had to be put back on easier delay values. For two animals, ST-5 and N-7, the delays of the two retrieval conditions were adjusted differently so as to give approximately the same number of errors under each. For the others, the delay values were kept the same under the two conditions. The selection of a suitable criterion of stable performance posed certain problems, since on delay tasks monkeys continue to improve for long periods of time 1,7, 1s,19. In this particular experiment it was found that animals initially improved rather rapidly, then much more slowly. A stability criterion was therefore selected that admitted only the slow improvement. This was that, in 40 consecutive sessions, the mean overall percentage correct for the last 20 should not be more than 5 ~ greater than for the first 20. As can be seen from Table I, this amount of improvement is small compared to the drop in performance caused by inferotemporal lesions. It is also apparent from the table that ST-10 averaged fewer than 20 errorsper session over its criterion run. This was because there was not enough time within days available to test it on the next set o f delays (in its case 0, 15, 30 and 50 sec).
Surgeo, All animals were operated 1 week after completing their criterion run. N-11 was given a bilateral superior temporal lesion to become ST-11 ; N-7, ST-5, ST-6 and ST-10 were given bilateral inferotemporal lesions to become IT-7, IST-5, IST-6 and IST-10 respectively. The intended locus of the lesions and the surgical procedures were as described in Dean and Weiskrantz 9. It was assumed that the effects of inferotemporal lesions would not be altered by prior superior temporal removal. This has been shown to be true for pattern discrimination learning and retentionlL
455
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
Histology W h e n p o s t o p e r a t i v e testing h a d been c o m p l e t e d , the monkeys, except IT-7 a n d ST-11, were anaesthetised with a large overdose o f N e m b u t a l a n d then perfused t h r o u g h the d o r s a l a o r t a with 0 . 9 ~ saline followed by 10~o formalin. IT-7 died o f b l o a t 22 before testing c o u l d be finished. Its head was r e m o v e d as s o o n as possible after discovery o f the b o d y , the d o r s a l skull a n d d u r a removed, a n d the whole immersed in 10 ~ formalin. ST-11 went on to a n o t h e r experiment, a n d was given an a d d i t i o n al i n f e r o t e m p o r a l lesion. Details o f this c o m b i n e d r e m o v a l are given elsewhere v; the s u p e r i o r t e m p o r a l lesion was as intended, and very similar to those described below for IST-5, 6 a n d 10. F o r all animals the h e a d was subsequently placed in a stereotaxic machine (and the d o r s a l skull a n d d u r a r e m o v e d in the case o f IST-5, 6 a n d 10). A cut was m a d e in f r o n t o f a n d b e h i n d the lesions in stereotaxic vertical planes a n d a steel p i n was passed h o r i z o n t a l l y t h r o u g h each hemisphere, m a k i n g a small hole which p r o v i d e d a baseline
21
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33
33
45
45
37
39
41
ta) IT-7
Fig. 1. a-e: reconstructions of lateral and ventral views of the brains of (a) IT-7, (b) IST-5, (c) IST-6 and (d) IST-10, with representative coronal sections through the lateral geniculate bodies and pulvihats. On the reconstructions the lesions are shown in black. On the coronal sections the borders of the lesions are indicated by dotted lines, and damage not visible on the surface shown in black. Sections through the lateral geniculate bodies are shown immediately beneath the brain sections, and sections through the pulvinar in (e). Total retrograde degeneration in these nuclei is shown in black, partial degeneration by stippling. All cross-sections are drawn with the left of the brain on the left. e, labelling of thalamic nuclei: LG -- lateral geniculate; MG medial geniculate; PI, PL and PM = pulvinar inferior, lateralis and medialis, respectively.
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EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
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for reconstructing the brain from coronal sections. The brain was then removed, photographed, placed in 1 0 ~ formalin for about 3 months, and then in sucrose formalin (10 ~ formalin, 30 ~ sucrose) until it sank. Frozen coronal sections were cut at 50/zm, of which 1 in 10 were kept. Alternate sections were stained with thionin and cresyl violet and used to reconstruct the lesion and to examine the lateral geniculate bodies and pulvinar. Fig. 1 gives reconstructions of the lesions, representative cross-sections, and sections through the lateral geniculate and pulvinar nuclei of the thalami for IST-5, IST-6, IST-10 and IT-7. All the superior temporal lesions, performed as control removals for the experiment described in Dean and Weiskrantz 9, conformed to the intended locus, and probably gave rise to what appeared to be small amounts of light degeneration in the medial pulvinar. Possibly because they were in three cases second operations, the inferotemporal lesions were in general slightly too posterior, as is reflected by the degeneration in the inferior pulvinar, and also somewhat too deep. Thus only IST-5 had intact hippocampi on both sides. The lesions also crossed the occipito-temporal sulcus bilaterally in IST-5, IST-6 and IST-10 and on the right side in IT-7. IST-10 showed clear degeneration in both lateral geniculate nuclei, and IST-6 in that on the left. This degeneration appeared to correspond to damage to white matter posterior to the ascending part of the inferior occipital sulcus. Finally IST-10 had a rather small lesion on the left side extending only a short distance anteriorly, and undercutting but not destroying cortex in the inferior bank of the superior temporal sulcus. Postoperative testing
One week after operation the animals were tested on the constant delay task, at those values of delay which they had reached on their preoperative stable run. It was initially proposed to continue testing them until they again reached stability. However, 3 of the 4 animals with inferotemporal lesions made so many errors that they began to be reluctant to complete a session. Since there seemed no point in forcing them to work at long delays when they were near chance at 0 sec (see below), all animals were therefore initially tested for 7 postoperative constant delay sessions only.
TABLE I OVERALLPERCENTAGECORRECTSCORESFORPREOPERATIVECRITERIONRUN(FIRSTANDLAST20 SESSIONS) ANDPOST-OPERATIVETESTING(CHANCE-- 37.5~) Animal
Pre-op. first 20
Pre-op. last 20
Post-op. 7
ST-11
74.9
79.4
78.6
IT-7 IST-5 IST-6 IST-10
77.7 78.2 67.8 88.8
79.6 80.0 69.5 92.2
41.3 42.0 35.8 66.4
459
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY 2o-
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Fig. 2. a - c : n u m b e r correct plotted against delay for (a) ST-11, (b) IT-7 a n d (c) IST-10. In each graph the ordinate s h o w s average n u m b e r correct per session (i.e., m a x i m u m score -- 20). T h e abscissa shows delay in seconds. Unfilled circles - the 40 preoperative stable sessions; filled circles ~ the 7 postoperative sessions. T h e upper g r a p h o f each pair represents p e r f o r m a n c e on 2 alternatives, the lower, p e r f o r m a n c e on 4 alternatives.
RESULTS
The overall percentage correct scores for the first and last 20 sessions of the preoperative criterion run and for the 7 postoperative sessions are shown in Table I. The pre- and postoperative scores for the individual conditions (expressed as mean number correct per session) are plotted in Fig. 2 for ST-11, IT-7 and IST-10. The graphs of the remaining animals, IST-5 and IST-6, are very similar to those for IT-7. The significance levels (derived from t-tests) for the differences between the pre- and postoperative scores are given in Table II. The raw material for these tests was the individual session scores for a given condition. Apart from a small postoperative improvement at the 2-0 condition the control operation had no effect on delayed matching. In contrast, 3 of the experimental animals (IT-7, IST-5 and IST-6) were reduced to performing almost at chance, and the fourth, IST-10, was markedly impaired. Differences between pre- and postoperative performance were significant for all animals with inferotemporal lesions at all delay values and for both retrieval conditions, although for IT-7, IST-5 and IST-6 this meant only that they could hardly do the task at all after operation. The experimental animal that did not have a prior superior temporal removal was as badly impaired as those that did, as was predicted from Ettlinger et al. 13. Observation of the animals on closed-circuit television revealed two items of
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T A B L E II SIGNIFICANCE LEVELS (USING t-TESTS) FOR DIFFERENCES BETWEEN PRE- AND POST-OPERATIVE DELAYED MATCHING-FROM-SAMPLE SCORES FOR ALL 8 CONDITIONS, FOR INDIVIDUAL ANIMALS
ST-11
IT-7
IST-5
1ST-6
IST-IO
2-0 A B C
0.05* N.S. * N.S. N.S. *
0.001 0.001 0.001 0.01
0.001 0.00l 0.001 0.001
0.001 0.001 0.001 0.001
0.05 0.02 0.02 0.01
4-0 A B C
N.S.* N.S.* N.S. N.S. *
0.001 0.001 0.001 0.001
0.001 0.001 0.001 0.001
0.001 0.001 0.001 0.001
0.0l 0.02 0.01 0.001
* D e n o t e s p o s t - o p e r a t i v e score better than pre-operative.
interest. Firstly, no animal showed any sign of an overt mediating response during the delay interval. Secondly, the experimental animals' general behaviour in the apparatus was the same after operation as before, that is, they looked as if they remembered the nature of the testing array and the task. In particular, they appeared to look at the retrieval cues before responding to them. This is supported by the fact that all animals with inferotemporal lesions scored at least 50 ~ overall in the 2-alternative condition, which is only possible if they look to see which 2 of the 4 response keys light up at the end of the delay. DISCUSSION
The preoperative behaviour of the animals in this experiment was in general similar to that observed in other studies of delayed matching from sample in monkeys. Thus performance declined monotonically with delay and there were no overt mediating responses (cf. Jarrard and Moise18). And, as expected, the effects of the control operation were negligible on all measures of delayed matching performance. What was not expected was the severity of the defect that occurred after inferotemporal removal, with 3 of the 4 animals performing at close to chance for all delays including zero, and for both 2- and 4-retrieval alternatives. This was despite an enormous amount of overtraining before operation, with at least 10,000 trials for this experiment alone, as well as 13,300 trials of matching with the retrieval cues fixed in position given before that 7. The first question to be asked about this surprising defect was whether it reflected the change in asymptotic performance that the experiment was designed to detect. It seemed very unlikely that this was the case. Three of the inferotemporals were unable to perform above chance even at zero delay, yet in Buffery's experiment they were able to reach 90 ~. So were two other animals with inferotemporal lesions, tested in the same apparatus as that used in the present experiment 7. It was therefore decided to try and retrain the animals in 4-alternative matching at zero delay and then to assess
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
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their ability to perform the task at longer delays. This retraining will be described in the next section. Other questions o f interest raised by the data will be considered in the discussion at the end of the paper. RETRAINING
Introduction A preliminary attempt at retraining was unsuccessful. The 4 animals with inferotemporal lesions were given zero delay matching with only 2 colours, blue and green. They were tested for 100 trials a day, on a re-run correction schedule. Criterion was 90 ~ correct, counting non-correction trials only, on 2 successive days. Only one animal, IST- 10, met this criterion in 4000 trials, taking 600 trials (97 errors); the others failed, their percentage correct for the last 5 sessions being 73.6 ~ (IST-5), 54.7 (IST-6) and 53.5 ~ (IT-7). IST-10 went on to solve 3-alternative zero-delay matching (blue, green, red; 800 trials, 182 errors) but then failed to solve 4 alternatives in 4000 trials (blue, green, red, yellow; score for the last 5 sessions 77.6 ~). It was therefore decided to take the animals up to zero-delay matching in easy stages, starting with a simple task like that used in the animals' initial training 7, i.e., two-alternative simultaneous matching with retrieval cues fixed in position. This procedure had the advantages of being similar to that successfully used with animals that had inferotemporal lesions in a previous experiment 7 and, if the animals did fail to learn, of allowing the particular stage at which breakdown occurred to be located.
Method Subjects. The subjects were the 4 animals with inferotemporal lesions, 1T-7, IST-5, IST-6 and IST-10. Apparatus. The only alteration to the apparatus used in the preceding section was to cover 2 response keys on the extreme right and left of the array for IT-7, IST-5 and IST-6. Procedure. The 3 animals who failed the 2-alternative task were started on the task designated 2/S-FP-1.5. Only 2 alternatives were used (2), blue and green as before, and the sample stayed on until the matching response had been made, that is, the condition was simultaneous (S). The retrieval cues blue and green were fixed in position (FP), with green always appearing to the left o f the sample key and blue to the right. The sample hold was increased from 0.5 to 1.5 sec (1.5.) The animals were run, on this and all other tasks to be described in this section, for 100 correction trials per day to a criterion of 90 ~ (on non-correction trials only) for 2 successive days. When 2/S-FP-1.5 had been mastered, the animals were transferred to the same task, first with zero-delay (2/0-FP-1.5) then with zero delay and 0.5 sec sample hold (2/0FP-0.5). They were then brought back to simultaneous and 1.5 sec hold and trained on proper matching (M), in which the retrieval cues appeared at the same 2 response keys as before, but their position varied randomly from trial to trial (2/S-2M-1.5). Again zero-delay (2/0-FP-1.5)and 0.5 sec hold (2/0-2M-0.5) were successively introduced. Then, with simultaneous and 1.5 sec hold, the retrieval cues were allowed to appear on
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TABLE III TRIALS(ANDERRORS)TO CRITERIONFOR PROBLEMSIN SECONDATTEMPTAT RETRAINING For explanation of 2S-FP-1.5, etc., see text. Problem
2S-FP-1.5 20-FP-1.5 20-FP-0.5 2S-2M-1.5 20-2M-1.5 20-2M-0.5 2S-4M-1.5 20-4M-1.5 20-4M-0.5 3S-FP-1.5 30-FP-1.5 30-FP-0.5 3S-4M-1.5 30-4M-1.5 30-4M-0.5 4S-FP-1.5 40-FP-1.5 40-FP-0.5 4S-M-1.5 40-M-1.5 40-M-0.5 Simultaneous: Red vs. yellow Green vs. blue
Animals IT-7
1ST-5
IST-6
3500 (938) 300 (39) Died
800 (152) 0 (0) 0 ( 0) 200 (34) 300 (35) 0 ( 0) 0 ( 0) 0 ( 0) 100 (15) 200 (38) 0 (0) 0 (0) 400 (85) 200 (13) 200 (26) 200 (34) 200 (29) 700 (109) 700 (124) 1100 (128) 0 ( 0)
4000 (1628)*
IST-IO
4o0 (53) 0(0) o(o) o(o) o(o) o(o) 1600 (480) 2400 (592)
* Denotes failure to reach criterion.
any two o f the 4 possible response panels, the outside two being uncovered for this purpose (2/S-4M-1.5). The final task reached via 2/0-4M-1.5, was 2/0-4M-0.5, i.e., that task on which the 3 animals had failed in the first retraining attempt. Red and yellow were then introduced one at a time, the exact sequence o f tasks being that shown in the left hand c o l u m n o f Table III. Since IST-10 had already reached criterion on 3/04M-0.5, he was started immediately on 4/S-FP-1.5. One animal, IST-6, failed on the simplest task, 2/S-FP-1.5. It was therefore transferred to a straightforward simultaneous colour discrimination, red v e r s u s yellow. F o r this task, only the 2 keys used for the matching stimuli on the 2-FP tasks were uncovered. The colours red and yellow appeared on these with a 7.5 sec intertrial interval, their positions varying r a n d o m l y f r o m trial to trial (except for correction trials). The correct response was to the red key. The nature o f the reward and punishment, the n u m b e r o f trials per day, the correction schedule, and the criterion were as in the retraining on matching. W h e n IST-6 had reached criterion on this task, red and yellow were replaced by green (positive) and blue.
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
463
Results Trials and errors to criterion for individual animals on the various problems are shown in Table III. Two animals, IST-5 and IST-10, were able to reach criterion on the 4-alternative zero-delay task (4/0-M-0.5) necessary for a return to the constant delay paradigm. Of the other two, IT-7 died of 'bloat '22 while still on task 2/0-FP-0.5, and so it is not possible to say whether it would have eventually mastered 4/0-M-0.5. Finally, IST-6 failed the simplest problem in the progression, 2/S-FP-1.5, and was in fact still performing at chance at the end of 4000 trials. Nonetheless this animal was able to learn to discriminate red from yellow, and green from blue, when those colours were presented in a simultaneous discrimination paradigm. It is conceivable that having done so it would have then been able to learn the 2/S-FP-1.5 task, but time was not available to test this.
Discussion The results of the second attempt at retraining support the idea that the animals' initial postoperative failure was not caused by an inability to perform the basic delayed matching from sample task. Thus both IST-5 and IST-10 reached criterion on tasks they had formerly failed, and indeed reached the stage at which they could be returned to the constant delay paradigm. Hence for these animals the purpose of the experiment, to measure delayed matching from sample capacity before and after inferotemporal lesions, could be carried out. This will be described in the next section. It is not clear why IST-6 did so poorly. It may have been because its lesion was rather deep, damaging the hippocampus on both sides (Fig. 1). It was also the worst animal at delayed matching from sample before operation, (scoring only 50 ~ at 10 sec with 4 alternatives) and might for this reason have been the most affected by the lesion. POSTOPERATIVE DELAYED MATCHING FROM SAMPLE CAPACITY
Subjects The subjects were the 2 animals, IST-5 and IST-10, that reached criterion on 4alternative zero-delay matching from sample in the previous section.
Apparatus The apparatus was that used in the first part of this experiment, as were the colours (red, green, blue and yellow) for sample and retrieval cues.
Procedure The animals were first overtrained on 4-alternative zero delay matching with a 0.5 sec sample hold and using a non-correction procedure, to 5 successive days at 90 each. Thereafter they were started on the (0, 1, 2, 5) sec condition previously described. The procedure followed was identical to that used in the first part of this experiment, except that these animals' performance on (0, 1, 2, 5) was so good that they were transferred after 5 sessions to their postoperative delay values, that is (0, 7.5, 15, 30)
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Fig. 3. a and b: number correct plotted against delay for (a) IST-5 and (b) IST-10. In each graph the ordinate shows average number correct per session (i.e., maximum score = 20). The abscissa shows delay in seconds. The upper graph of each pair represents performance on 2 alternatives, the lower graph performance on 4 alternatives. Unfilled circles -- the 40 preoperative stable sessions. Filled circles = the 20 postoperative sessions at preoperative delay values.
for IST-10, (0, 15, 30, 50) for IST-5 with 2 alternatives, and (0, 5, 10, 20) with 4. They were tested for 20 sessions at these delays. N o criterion o f stable performance was used since it was clear that as soon as the animals encountered these delay values they were able to do at least as well on them as during the preoperative stable run.
Results On pretraining, IST-5 t o o k 1500 trials, 213 errors, and IST-10 200 trials, 21 errors, to reach the criterion. F o r delayed matching f r o m sample the p e r f o r m a n c e delay curves for pre- and postoperative performance are shown in Fig. 3. These are derived f r o m the 40 preoperative stable sessions, and the 20 postoperative ones. As can be seen, IST-10 tends to do about as well after operation as before, although in one condition, 2-0, it is significantly worse after (t ~ 2.296, df = 58, P < 0.05). IST-5, on the other hand, does better after operation for longer delays than before: the differences in performance are significant for the 2-B condition (t = 3.59, P < 0.001), the 2-C (t = 2.57, P < 0.02) and the 4-C (t = 3.05, P < 0.01). Pre- and postoperative reaction times tu the match stimuli are plotted for the 2 animals in Fig. 4. These were calculated f r o m the first and last 10 sessions o f the preoperative stable run and from all 20 postoperative sessions. IST-5 (Fig. 4a) was significantly slower after operation for all conditions. The significance level is 0.001 except for the 2-A (0.002), 2-B (0.05) and 2-C (0.02) conditions. (Since each point on
465
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY 2.5-
2.5
f~
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15 ..
1.0
1.0. ~/
IST-5
IST- I0
2 ALTERNATIVES
0.5
0"5 ()
1~5
3.0
5'0
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1'5
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1"5-
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4 ALTERNATIVES
I'O (a)
2'o
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7:5
4 ALTERNATIVES
1~
io
(b)
Fig. 4. a and b: reaction time plotted against delay for (a) IST-5 and (b) 1ST-10. In each graph the ordinate shows the mean reaction time in seconds, the abscissa the delay in seconds. Reaction times are for correct responses only. The upper graph of each pair gives times for 2 matching alternatives, the lower for 4. Unfilled squares -- the first and last 10 sessions of preoperative stable run. Filled squares = the 20 postoperative sessions.
the graphs is derived from more than 300 reaction times, the test used for these levels was that based on the normal distribution.) For IST-10 (Fig. 4b) the postoperative reaction times were slower for only some conditions: 2-0, 2-A, 4-0 and 4-A (in all cases P < 0.001), and 4-B (P < 0.02). There was no significant difference between the times for 2-B, 2-C and 4-C. Errors were also analysed for the 20 postoperative sessions and the first and last 10 sessions of the preoperative stable run. Table IV shows those proportions of errors that were to the sample of the preceding trial, when this was correct. These were significantly above the chance value of 25 ~ for both animals, both before and after operation (chi-squared test; 3rd and 5th columns). Both animals made a smaller proportion of such errors after operation, but this difference was significant for IST-10 alone (6th column). Discussion
This experiment was designed to measure the effects of inferotemporal removal on the asymptotic performance of 4-alternative delayed matching from sample. These effects are clear from the accuracy data plotted in Fig. 3; once the animals have been retrained after operation to a stringent criterion at zero delay, they can perform at their preoperative levels at all delays. These results therefore provide no evidence of impaired asymptotic performance after inferotemporal lesions.
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TABLE IV PERCENTAGE OF TOTAL ERRORS THAT THERE WERE TO THE SAMPLE COLOUR OF THE PRECEDING TRIAL (CHANCE ~
Animal
25~)
Pre-op.
Vs. chance
( %J IST-5 IST-10
50.6 55.2
Post-op.
Vs. chance
Pre vs. post
0.001 0.001
N.S. 0.01
( %J 0.001 0.001
44.1 41.2
The experiment also provides evidence in support of an interpretation of Buffery's results1, 2, suggested in the Introduction. This was that although inferotemporal lesions might affect the retention and learning of the basic 4-alternative matching task, they did not selectively impair its performance at long delays. In agreement with this interpretation, the rapid adjustment of IST-5 and IST-10 to long delays was in striking contrast to their difficulty in reaching criterion at zero delay, and also to the trouble normal rhesus monkeys have when encountering delay in matching tasks for the first timeT,11,is. Even in preoperative overtraining in this experiment, when IST-5 and IST-10 had already had considerable experience with delay7, they required 10 and 35 sessions respectively to reach their stable delay values. But post-operatively they could perform at these values after, at most, 5 sessions, once they had reached criterion at zero delay. It seems likely, therefore, that Buffery's results were caused at least in part by his operated animals not having learnt the 4-alternative task as well as the normal animals at zero delay. The fact that inferotemporal lesions do not affect the asymptotic performance of delayed matching from sample is powerful evidence against the hypothesis mentioned in the Introduction, that animals with inferotemporal ablations have a reduced capacity to remember visual stimuli. The hypothesis might still be correct if the sort of visual memory used in discrimination learning differed in some important way from that tested by delayed matching from sample. Three potential differences can be excluded. (1) The unimpaired postoperative performance in this experiment was obtained with colours that were very easy to discriminate. But Wilson e t al. ~6 also found no impairment, even immediately after operation, on delayed matching with patterns as stimuli. Animals with inferotemporal lesions show very clear learning impairments on simultaneous pattern discrimination. (2) It is not the case that interference is present only in discrimination learning, and not matching. Error analysis showed that after operation IST-5 and IST-10 made a greater than chance proportion of their errors to the sample of the preceding (correct) trial (Table IV), i.e., there was proactive interference. Also, D'Amato and O'Neill 6 have shown that illumination during the intratrial delay worsens performance, an effect they attribute to interference. Such illumination was used in the present experiment. (3) It cannot easily be maintained that delayed matching from sample tests only 'short-term memory' (while discrimination learning involves longer term pro-
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
467
cesses) - - even allowing that the long-term/short-term distinction is applicable to monkey memory. Depending on the circumstances, monkeys can perform delayed matching with substantial intratrial delays: in this experiment, two animals showed clear signs of retention at 50 sec delay, and Mello 19 has reported 95 ~ correct matching after 232 sec. These intervals are long compared with those normally used in shortterm memory experiments with people. Furthermore, it has been argued by Waugh and Norman 23 that when retention is measured after even short periods, information is retrieved from both 'short-term' (or more accurately 'primary') memory and 'long-term' (or 'secondary') memory. By this argument, defective secondary memory should be revealed by a delayed matching from sample paradigm. It can thus be concluded that, in certain important respects, the kind of visual memory involved in delayed matching from sample resembles that concerned in discrimination learning. It is correspondingly improbable that animals with inferotemporal lesions learn visual discriminations slowly because their memory for visual stimuli is defective. This conclusion does not of course apply to visual association memory, which, as pointed out in the Introduction, is not tested in delayed matching from sample. Two other features of the results require comment. One is that the inferotemporal lesions produced what appeared to be an almost total retrograde amnesia for delayed matching from sample with 4 samples. Similar effects of inferotemporal removal have also been found by BufferyI and by Wilson et al. 26, at least for colours. However, only in the present experiment were the animals very extensively overtrained for more than 10,000 trials before operation. For simultaneous discriminations much less overtraining than this (i.e., not more than 500 trials) abolishes the retrograde amnesia normally accompanying inferotemporal removal4, ~1. It is not clear which features of the delayed matching from sample paradigm confer this resistance to the effects of preoperative overtraining, but one possibility is that the samples are presented one at a time. The animal must therefore identify them without benefit of the relational cues available in simultaneous discriminations. If inferotemporal removal interfered with the processes responsible for stimulus identification, the vulnerability of delayed matching from sample to its effects would be explained. More direct tests of this hypothesis are currently being carried out in this laboratory. Secondly, both IST-5 and IST-10 had substantially longer reaction times to the matching stimuli after operation (Fig. 4). It is not clear what this difference means. There are discrepancies, which may be important, between the reaction time changes for the two animals: thus the reaction times of IST-5 increase more for 4 than for 2 alternatives, but those of IST-10 increase about the same for both conditions, and while IST-10's increase vanishes when the delay reaches 30 sec, IST-5's increase seems to reach asymptote with long delays. Moreover the animals were not made to respond as fast as they could, so their slow reaction times do not necessarily reflect an inability to respond at preoperative speeds (cf. DeanS). This also applied to Buffery's1 reaction time results, which agree with those here in showing animals with inferotemporal lesions to be slower than normals at the matching stage of 4-alternative delayed matching from sample, even at zero-delay. Nonetheless, the slower reaction times are not
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inconsistent with the possibility that animals with inferotemporal lesions have a smaller capacity for identifying visual stimuli, so that dealing with 4 samples is a more difficult task for them than for normal animals. ACKNOWLEDGEMENTS
This research was supported by MRC Grants G 967/2/B and G 971/397/B. I thank Mr. J. P. Broad and Mr. C. Blackmore for photographing the figures, and Mr. I. H. Lloyd and Miss M. McAnulty for preparing the histological material. I am especially grateful to Professor L. Weiskrantz for performing the surgery, and for much helpful discussion and advice.
REFERENCES 1 BUFFERY,A. W. H., The Effects of Frontal and Temporal Lesions upon the Behaviour of Baboons, Unpublished Ph.D. Dissertation, University of Cambridge, England, 1964, 412 pp. 2 BUFFERY,A. W. H., Attention and retention following frontal and temporal lesions in the baboon. In Proceedings of the 73rd Annual Convention of the American Psychological Association, Washington, 1965, pp. 103-104. 3 BUTLER, C. R., Is there a memory impairment in monkeys after inferotemporal lesions? Brain Research, t3 (1969) 383-393. 4 CHOW, K. L., AND SURVlS,J., Retention of overlearned visual habit after temporal cortical ablation in monkey, Arch. Neurol. Psychiat. (Chic.), 79 (1958) 640-646. 5 COWEY, A., AND GROSS, C. G., Effects of foveal prestriate and inferotemporal lesions on visual discriminations by rhesus monkeys, Exp. Brain Res., 11 (1970) 128-144. 6 D'AMATO, M. R., AND O'NEILL, W., Effect of delay interval illumination on matching behaviour in the capuchin monkey, J. exp. Anal. Behav., 15 (1971) 327-333. 7 DEAN, P., Functions of the Temporal Lobe in Visual Discrimination and Memory in Macaca mulatta, Unpublished D. Phil. Dissertation, University of Oxford, 1972, 373 pp. 8 DEAN, P., Choice reaction times for pattern discriminations in monkeys with inferotemporal lesions, Neuropsyehologia, (1974), in press. 9 DEAN,P., AND WEISKRANTZ,L., Loss of preoperative habits in rhesus monkeys with inferotemporal lesions: recognition failure or relearning deficit? Neuropsychologia, (1974), in press. 10 DEWSON, J. H., III, PRIBRAM, K. H., AND LYNCH, J. C,, Effects of ablations of temporal cortex upon speech sound discrimination in the monkey, Exp, Neurol., 24 (1969) 579-591. 11 DRACHMAN, D. A., AND OMMAYA, A. K., Memory and the hippocampal complex, Arch. Neurol. (Chic.), 10 (1964) 411-425. 12 ETKIN, H., AND D'AMATO, M. R., Delayed matching to sample and short-term memory in the capuchin monkey, J. comp. physiol. Psychol., 16 (1969) 544-549. 13 ETTLINGER, G., IWAI, E., MISHKIN, M., AND ROSVOLD, H. E., Visual discrimination in the monkey following serial ablation of inferotemporal and pre-occipital cortex, J. comp. physiol. Psychol., 65 0968) 110-117. 14 GROSS, C. G., Visual functions of inferotemporal cortex, In R. JUNG (Ed.), Handbook of Sensory Physiology, Vol. VII/3, part B. Central Visual It~formation, Springer, Berlin, 1973, pp. 451482. 15 GRoss, C. G., COWEY, A., AND MANNING, F. J., Further analysis of visual discrimination deficits following foveal prestriate and inferotemporal lesions in monkeys, J. comp. physiol. Psychok, 76 (1971) 1-7. 16 IVERSEN, S. D., AND WEISKRANTZ, L., Temporal lobe lesions and memory in the monkey, Nature (Lond.), 201 (1964) 740-742. 17 IVERSEN, S. D., AND WEISKRANTZ, L., An investigation of a possible memory defect produced by inferotemporal lesions in the baboon, Neuropsychologia, 8 (1970) 21-36. 18 JARRARD,L. E., AND MOISE, S. L., Short-term memory in the monkey. In L. E. JARRARD(Ed.), Cognitive Processes of Non-Human Primates, Academic Press, New York, 1971, pp. 1-24.
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19 MELLO, N, K., Alcohol effects on delayed matching to sample performance by rhesus monkey, Physiol. Behav., 7 (1971) 77-101. 20 MISHKIN, M., Cortical visual areas and their interactions. In A. G. KARCZMAR AND J. C. ECCLES (Eds.), The Brain and Human Behaviour, Springer, Berlin, 1972, pp. 187-208. 21 ORBACH,J., AND FANTZ, R. L., Differential effects of temporal neo-cortical resections on overtrained and non-overtrained visual habits in monkeys, J. comp. physiol. Psychol., 51 (1958) 126-129.
22 TURNER,A. E., AND COWEY, A., Bloat syndrome in captive rhesus monkeys: report on twelve cases, J. Inst. Anita. Techn., 22 (1971) 181-186. 23 WAUGH, N. C., AND NORMAN, D. A., Primary memory, Psychol. Rev., 72 (1965) 89-104. 24 WEISKRANTZ,L., Experimental studies of amnesia. In C. W. M. WHITTV AND O. L. ZANGWILL (Eds.), Amnesia, Butterworth, London, 1966, pp. 1-35. 25 WEISKRANTZ,L., Central nervous system and the organization of behaviour. In D. P. KIMBLE (Ed.), The Organization of Recall, New York Academy of Science, 1967, pp. 234-293. 26 WILSON,M., KAUFMAN, W. M., ZIELER,R. E., AND LIEB, J. P., Visual identification and memory in monkeys with circumscribed inferotemporal lesions, J. comp. physiol. Psychol., 78 (1972) 173-183.
451
© Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands
THE EFFECT OF I N F E R O T E M P O R A L LESIONS ON MEMORY VISUAL STIMULI IN RHESUS MONKEYS
FOR
P. D E A N
Department of Experimental Psychology, Oxford OX1 3PS (Great Britain) (Accepted April 24th, 1974)
SUMMARY
To test the hypothesis that inferotemporal ablations impair memory for visual stimuli, rhesus monkeys were trained to a criterion of stable performance on delayed matching from sample. Four colours were used as samples, and either 2 or 4 as retrieval cues. Inferotemporal removal initially affected matching performance at all delays, including zero, and for both retrieval conditions. However, when animals had been retrained to criterion on zero delay 4-alternative matching, they very rapidly achieved preoperative levels of performance at all delays. It is concluded that the deficit obtained by Bufferya on 4-alternative delayed matching reflected the inferotemporals' inadequate learning of the basic zero delay 4-alternative task; and that inferotemporal removal probably has no effect on the ability to remember visual stimuli.
INTRODUCTION
Why do inferotemporal lesions in monkeys impair visual discrimination learning? Present evidence indicates that they do not cause sensory or perceptual disturbances 8,14. Perhaps, therefore, the defect is in remembering visual stimuli, as has frequently been suggestedS,20, z4. Tests of this idea have typically measured the retention of previously learnt object discriminations3,15-17, with results that are not easy to interpret. However, such tests require the animal to remember at least two different kinds of information: purely visual information about the appearance of the objects (which object is which), and information about object-reward associations (which object is the positive one). Memory for the first may be called visual stimulus memory, for the second, visual association memory. A task that would seem to test visual stimulus memory but not visual association memory is delayed matching from sample, since in this paradigm no one sample is more associated with reward than any other. The animal cannot, therefore, use stimulus-reward information to bridge the delay
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between sample presentation and the appearance of the matching cues, but must relay on visual stimulus memory alone. Delayed matching from sample may thus be a suitable paradigm for testing the hypothesis that inferotemporal ablations impair memory for visual stimuli. A series of experiments using this idea was carried out by Buffery1,2 (described in ref. 25). His most interesting finding was obtained with 4-alternative delayed matching from sample, in which the sample could be any one of 4 colours, all of which appeared at the end of the delay. Length o f delay was titrated, i.e., it was increased when an animal got two consecutive matching responses correct, and decreased when it made an error. This had the effect of stabilizing the animals at those delays after which they could score about 70 ~ correct. Buffery found that baboons with inferotemporal lesions could not tolerate such long delays as normal animals. This was only true for 4 alternatives; with 2 or 3 alternatives the animals with irlferotemporal lesions were not significantly worse than the controls. This suggested that inferotemporal ablation did indeed cause a defect in visual memory which became apparent when the amount of information to be remembered increased. However, another interpretation of these results is possible. Four-alternative delayed matching from sample is more difficult to learn than 2- or 3-alternative matching. It has been clearly established that the learning impairment produced by inferotemporal ablation is more pronounced the more difficult the task. It is therefore possible that the operated animals in Buffery's experiment were worse than normal animals because they had not learnt the basic 4-alternative task so well, an effect obscured by the use of the titration schedule. If this were true, no conclusion about the effect of inferotemporal lesions on visual memory could be drawn from Buffery's results. The present experiment was designed to allow for the effects of slow learning by the operated animals. Firstly, they were required to meet a very stringent criterion at zero delay with 4-alternative matching, to ensure that they had learnt the basic task. Secondly, a constant delay paradigm was used, so that performance could be measured at several values of delay. If, despite the stringent criterion, the animals with inferotemporal lesions were nonetheless insufficiently familiar with the basic task, they would be impaired at all values of delay, not just at long ones. Thirdly, an attempt was made to measure asymptotic delay performance, i.e. delay performance that was no longer improving, by having the animals meet a criterion of stable performance on the constant delay paradigm. One other change was made from Buffery's experiment. Delay performance was measured in the same animals before and after inferotemporal removal. Effects of the operation that were small compared with the between-animal variance could thus be detected, and conversely an absence of effect demonstrated more convincingly. METHOD
Subjects The subjects used were 5 immature rhesus monkeys, 2 male and 3 female. They
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
453
had previously been trained on object and pattern discriminations, and had had extensive experience of delayed matching from sampleL Two were unoperated, but the other 3 had bilateral lesions of the superior temporal gyrus, sparing primary auditory cortex 9. However such lesions appear to have no effect on visual tasks 7,1°,1a, and these particular animals had been shown to be no worse than normals on delayed matching from sampleL All the animals were fed about 22 h before testing, being given as much food as was consistent with their working reliably.
.Apparatus The animals were tested in a transport cage, one side of which was removed to allow access to a 61 cm × 61 cm testing display. Throughout the experiment the cage was lit by dim overhead light (5-8 W) and masking white noise was provided. The testing display consisted of 5 circular transparent response keys mounted in a horizontal row 25 cm above the transport cage floor. Each key was 3.3 cm in diameter, and was mounted 7.5 cm, centre to centre, from its neighbours. There was also a foodwell, 17 cm below the centre key. A Grason-Stadler in-line digital read-out unit (E-4580/3) was mounted behind each response key and programmed to give any one of the following colours: blue (Ilford filter 304), green (Ilford 404), red (Ilford 204 plus Wratten 29) and yellow (Ilford 104). The unit behind the centre key was also programmed to give a white star, which was the 'ready' signal. An Advance SC-2 Timer was used to measure the animals' reaction times to the match stimuli. This timer was started when the match stimuli appeared and stopped when a response to them was made. All programming equipment used was G r a s o n Stadler series 1200, except for 5 switches that determined which colour appeared on each response key, and these were set by hand. The animals' behaviour during testing was watched on closed circuit television.
Procedure The animals were first trained to a criterion of 90 correct out of 100 trials on zero-delay matching from sample with 4 alternatives. The start of a trial was signalled by the appearance of the white star on the centre key. When this was pressed one of the colours (red, blue, green or yellow) appeared in its place as the sample and remained for at least 0.5 sec, after which a second press turned offthe sample and immediately (i.e., after 0 sec delay) turned on the match stimuli. These were all the 4 colours, and they appeared on the 4 outside response keys in positions that varied randomly from trial to trial. A correct response was a press to that response panel which was the same colour as the sample; an incorrect response, one to any other panel. Either response produced a 7.5 sec time-out in which no panel was lit, and no further press effective; in addition, a correct press was rewarded with a CIBA 190 mg banana pellet, and 2 sec of background illumination in the foodwell, whereas an incorrect press turned the overhead light out for 7.5 sec. At the end of the time-out the white star reappeared on the centre key. When the animals had reached the criterion on this problem they were put on the
454
v. I~EAN
constant delay schedule. In this, the daily session consisted of 160 trials, preceded by 10 warm-up trials at zero delay, details of which were not recorded. The programming of the sessions was arranged as follows. Each daily session consisted of an 80-trial block, repeated once. The 80 trials in turn comprised 10 8-trial blocks. Either 2 or 4 retrieval cues could appear at the end of 4 different delays (O, A, B and C) giving rise to 8 possible conditions, 2-0, 2-A, 2-B, 2-C, 4-0, 4-A, 4-B and 4-C. Every 8-trial block consisted of one trial from each of these conditions in random order. In the two-alternative condition, the sample was paired at the retrieval stage with one of the other 3 colours at random, and the position of the 2 on the 4-response panels was also random. Over the first 20 daily sessions, for every condition (a) each of the 4 colours appeared equally as often as the sample, and (b) the correct match colour, and each incorrect match colour, appeared equally as often at each of the 4 response positions. These 20 sessions were then repeated in the same order indefinitely. All animals were started off with A -- 1 sec, B = 2 sec, and C = 5 sec (O was always 0 sec for all conditions). These were increased after a block of 5 160-trial sessions if during that block the animal had averaged fewer than 20 errors per session. Five sets of delay values were used: (0, 1, 2, 5), (0, 2, 5, 10), (0, 5, 10, 20), (0, 7.5, 15, 30) and (0, 15, 30, 50). It turned out that no animal deteriorated with time such that he had to be put back on easier delay values. For two animals, ST-5 and N-7, the delays of the two retrieval conditions were adjusted differently so as to give approximately the same number of errors under each. For the others, the delay values were kept the same under the two conditions. The selection of a suitable criterion of stable performance posed certain problems, since on delay tasks monkeys continue to improve for long periods of time 1,7, 1s,19. In this particular experiment it was found that animals initially improved rather rapidly, then much more slowly. A stability criterion was therefore selected that admitted only the slow improvement. This was that, in 40 consecutive sessions, the mean overall percentage correct for the last 20 should not be more than 5 ~ greater than for the first 20. As can be seen from Table I, this amount of improvement is small compared to the drop in performance caused by inferotemporal lesions. It is also apparent from the table that ST-10 averaged fewer than 20 errorsper session over its criterion run. This was because there was not enough time within days available to test it on the next set o f delays (in its case 0, 15, 30 and 50 sec).
Surgeo, All animals were operated 1 week after completing their criterion run. N-11 was given a bilateral superior temporal lesion to become ST-11 ; N-7, ST-5, ST-6 and ST-10 were given bilateral inferotemporal lesions to become IT-7, IST-5, IST-6 and IST-10 respectively. The intended locus of the lesions and the surgical procedures were as described in Dean and Weiskrantz 9. It was assumed that the effects of inferotemporal lesions would not be altered by prior superior temporal removal. This has been shown to be true for pattern discrimination learning and retentionlL
455
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
Histology W h e n p o s t o p e r a t i v e testing h a d been c o m p l e t e d , the monkeys, except IT-7 a n d ST-11, were anaesthetised with a large overdose o f N e m b u t a l a n d then perfused t h r o u g h the d o r s a l a o r t a with 0 . 9 ~ saline followed by 10~o formalin. IT-7 died o f b l o a t 22 before testing c o u l d be finished. Its head was r e m o v e d as s o o n as possible after discovery o f the b o d y , the d o r s a l skull a n d d u r a removed, a n d the whole immersed in 10 ~ formalin. ST-11 went on to a n o t h e r experiment, a n d was given an a d d i t i o n al i n f e r o t e m p o r a l lesion. Details o f this c o m b i n e d r e m o v a l are given elsewhere v; the s u p e r i o r t e m p o r a l lesion was as intended, and very similar to those described below for IST-5, 6 a n d 10. F o r all animals the h e a d was subsequently placed in a stereotaxic machine (and the d o r s a l skull a n d d u r a r e m o v e d in the case o f IST-5, 6 a n d 10). A cut was m a d e in f r o n t o f a n d b e h i n d the lesions in stereotaxic vertical planes a n d a steel p i n was passed h o r i z o n t a l l y t h r o u g h each hemisphere, m a k i n g a small hole which p r o v i d e d a baseline
21
-
-
2,
33
33
45
45
37
39
41
ta) IT-7
Fig. 1. a-e: reconstructions of lateral and ventral views of the brains of (a) IT-7, (b) IST-5, (c) IST-6 and (d) IST-10, with representative coronal sections through the lateral geniculate bodies and pulvihats. On the reconstructions the lesions are shown in black. On the coronal sections the borders of the lesions are indicated by dotted lines, and damage not visible on the surface shown in black. Sections through the lateral geniculate bodies are shown immediately beneath the brain sections, and sections through the pulvinar in (e). Total retrograde degeneration in these nuclei is shown in black, partial degeneration by stippling. All cross-sections are drawn with the left of the brain on the left. e, labelling of thalamic nuclei: LG -- lateral geniculate; MG medial geniculate; PI, PL and PM = pulvinar inferior, lateralis and medialis, respectively.
456
P. DEAN
21 27 33--
21 2"/ 33
23
25
27
(b) i S T - 5
2 4 - 3 1 - 38"--
-
-
24
- - 3 1 38
'"
22
38
24 (c) i S T - 6
26
457
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
32 38 44
32 38 44
~,.~ ~,1~; ~,,~ (d) IST- 10
IT-7
IST-5
,,Q~
IST-10
IST-6
,,
%
,,O%
"@ %
(e) p u l v i n a r s
458
P. DEAN
for reconstructing the brain from coronal sections. The brain was then removed, photographed, placed in 1 0 ~ formalin for about 3 months, and then in sucrose formalin (10 ~ formalin, 30 ~ sucrose) until it sank. Frozen coronal sections were cut at 50/zm, of which 1 in 10 were kept. Alternate sections were stained with thionin and cresyl violet and used to reconstruct the lesion and to examine the lateral geniculate bodies and pulvinar. Fig. 1 gives reconstructions of the lesions, representative cross-sections, and sections through the lateral geniculate and pulvinar nuclei of the thalami for IST-5, IST-6, IST-10 and IT-7. All the superior temporal lesions, performed as control removals for the experiment described in Dean and Weiskrantz 9, conformed to the intended locus, and probably gave rise to what appeared to be small amounts of light degeneration in the medial pulvinar. Possibly because they were in three cases second operations, the inferotemporal lesions were in general slightly too posterior, as is reflected by the degeneration in the inferior pulvinar, and also somewhat too deep. Thus only IST-5 had intact hippocampi on both sides. The lesions also crossed the occipito-temporal sulcus bilaterally in IST-5, IST-6 and IST-10 and on the right side in IT-7. IST-10 showed clear degeneration in both lateral geniculate nuclei, and IST-6 in that on the left. This degeneration appeared to correspond to damage to white matter posterior to the ascending part of the inferior occipital sulcus. Finally IST-10 had a rather small lesion on the left side extending only a short distance anteriorly, and undercutting but not destroying cortex in the inferior bank of the superior temporal sulcus. Postoperative testing
One week after operation the animals were tested on the constant delay task, at those values of delay which they had reached on their preoperative stable run. It was initially proposed to continue testing them until they again reached stability. However, 3 of the 4 animals with inferotemporal lesions made so many errors that they began to be reluctant to complete a session. Since there seemed no point in forcing them to work at long delays when they were near chance at 0 sec (see below), all animals were therefore initially tested for 7 postoperative constant delay sessions only.
TABLE I OVERALLPERCENTAGECORRECTSCORESFORPREOPERATIVECRITERIONRUN(FIRSTANDLAST20 SESSIONS) ANDPOST-OPERATIVETESTING(CHANCE-- 37.5~) Animal
Pre-op. first 20
Pre-op. last 20
Post-op. 7
ST-11
74.9
79.4
78.6
IT-7 IST-5 IST-6 IST-10
77.7 78.2 67.8 88.8
79.6 80.0 69.5 92.2
41.3 42.0 35.8 66.4
459
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY 2o-
10. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Fig. 2. a - c : n u m b e r correct plotted against delay for (a) ST-11, (b) IT-7 a n d (c) IST-10. In each graph the ordinate s h o w s average n u m b e r correct per session (i.e., m a x i m u m score -- 20). T h e abscissa shows delay in seconds. Unfilled circles - the 40 preoperative stable sessions; filled circles ~ the 7 postoperative sessions. T h e upper g r a p h o f each pair represents p e r f o r m a n c e on 2 alternatives, the lower, p e r f o r m a n c e on 4 alternatives.
RESULTS
The overall percentage correct scores for the first and last 20 sessions of the preoperative criterion run and for the 7 postoperative sessions are shown in Table I. The pre- and postoperative scores for the individual conditions (expressed as mean number correct per session) are plotted in Fig. 2 for ST-11, IT-7 and IST-10. The graphs of the remaining animals, IST-5 and IST-6, are very similar to those for IT-7. The significance levels (derived from t-tests) for the differences between the pre- and postoperative scores are given in Table II. The raw material for these tests was the individual session scores for a given condition. Apart from a small postoperative improvement at the 2-0 condition the control operation had no effect on delayed matching. In contrast, 3 of the experimental animals (IT-7, IST-5 and IST-6) were reduced to performing almost at chance, and the fourth, IST-10, was markedly impaired. Differences between pre- and postoperative performance were significant for all animals with inferotemporal lesions at all delay values and for both retrieval conditions, although for IT-7, IST-5 and IST-6 this meant only that they could hardly do the task at all after operation. The experimental animal that did not have a prior superior temporal removal was as badly impaired as those that did, as was predicted from Ettlinger et al. 13. Observation of the animals on closed-circuit television revealed two items of
460
P. DEAN
T A B L E II SIGNIFICANCE LEVELS (USING t-TESTS) FOR DIFFERENCES BETWEEN PRE- AND POST-OPERATIVE DELAYED MATCHING-FROM-SAMPLE SCORES FOR ALL 8 CONDITIONS, FOR INDIVIDUAL ANIMALS
ST-11
IT-7
IST-5
1ST-6
IST-IO
2-0 A B C
0.05* N.S. * N.S. N.S. *
0.001 0.001 0.001 0.01
0.001 0.00l 0.001 0.001
0.001 0.001 0.001 0.001
0.05 0.02 0.02 0.01
4-0 A B C
N.S.* N.S.* N.S. N.S. *
0.001 0.001 0.001 0.001
0.001 0.001 0.001 0.001
0.001 0.001 0.001 0.001
0.0l 0.02 0.01 0.001
* D e n o t e s p o s t - o p e r a t i v e score better than pre-operative.
interest. Firstly, no animal showed any sign of an overt mediating response during the delay interval. Secondly, the experimental animals' general behaviour in the apparatus was the same after operation as before, that is, they looked as if they remembered the nature of the testing array and the task. In particular, they appeared to look at the retrieval cues before responding to them. This is supported by the fact that all animals with inferotemporal lesions scored at least 50 ~ overall in the 2-alternative condition, which is only possible if they look to see which 2 of the 4 response keys light up at the end of the delay. DISCUSSION
The preoperative behaviour of the animals in this experiment was in general similar to that observed in other studies of delayed matching from sample in monkeys. Thus performance declined monotonically with delay and there were no overt mediating responses (cf. Jarrard and Moise18). And, as expected, the effects of the control operation were negligible on all measures of delayed matching performance. What was not expected was the severity of the defect that occurred after inferotemporal removal, with 3 of the 4 animals performing at close to chance for all delays including zero, and for both 2- and 4-retrieval alternatives. This was despite an enormous amount of overtraining before operation, with at least 10,000 trials for this experiment alone, as well as 13,300 trials of matching with the retrieval cues fixed in position given before that 7. The first question to be asked about this surprising defect was whether it reflected the change in asymptotic performance that the experiment was designed to detect. It seemed very unlikely that this was the case. Three of the inferotemporals were unable to perform above chance even at zero delay, yet in Buffery's experiment they were able to reach 90 ~. So were two other animals with inferotemporal lesions, tested in the same apparatus as that used in the present experiment 7. It was therefore decided to try and retrain the animals in 4-alternative matching at zero delay and then to assess
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
461
their ability to perform the task at longer delays. This retraining will be described in the next section. Other questions o f interest raised by the data will be considered in the discussion at the end of the paper. RETRAINING
Introduction A preliminary attempt at retraining was unsuccessful. The 4 animals with inferotemporal lesions were given zero delay matching with only 2 colours, blue and green. They were tested for 100 trials a day, on a re-run correction schedule. Criterion was 90 ~ correct, counting non-correction trials only, on 2 successive days. Only one animal, IST- 10, met this criterion in 4000 trials, taking 600 trials (97 errors); the others failed, their percentage correct for the last 5 sessions being 73.6 ~ (IST-5), 54.7 (IST-6) and 53.5 ~ (IT-7). IST-10 went on to solve 3-alternative zero-delay matching (blue, green, red; 800 trials, 182 errors) but then failed to solve 4 alternatives in 4000 trials (blue, green, red, yellow; score for the last 5 sessions 77.6 ~). It was therefore decided to take the animals up to zero-delay matching in easy stages, starting with a simple task like that used in the animals' initial training 7, i.e., two-alternative simultaneous matching with retrieval cues fixed in position. This procedure had the advantages of being similar to that successfully used with animals that had inferotemporal lesions in a previous experiment 7 and, if the animals did fail to learn, of allowing the particular stage at which breakdown occurred to be located.
Method Subjects. The subjects were the 4 animals with inferotemporal lesions, 1T-7, IST-5, IST-6 and IST-10. Apparatus. The only alteration to the apparatus used in the preceding section was to cover 2 response keys on the extreme right and left of the array for IT-7, IST-5 and IST-6. Procedure. The 3 animals who failed the 2-alternative task were started on the task designated 2/S-FP-1.5. Only 2 alternatives were used (2), blue and green as before, and the sample stayed on until the matching response had been made, that is, the condition was simultaneous (S). The retrieval cues blue and green were fixed in position (FP), with green always appearing to the left o f the sample key and blue to the right. The sample hold was increased from 0.5 to 1.5 sec (1.5.) The animals were run, on this and all other tasks to be described in this section, for 100 correction trials per day to a criterion of 90 ~ (on non-correction trials only) for 2 successive days. When 2/S-FP-1.5 had been mastered, the animals were transferred to the same task, first with zero-delay (2/0-FP-1.5) then with zero delay and 0.5 sec sample hold (2/0FP-0.5). They were then brought back to simultaneous and 1.5 sec hold and trained on proper matching (M), in which the retrieval cues appeared at the same 2 response keys as before, but their position varied randomly from trial to trial (2/S-2M-1.5). Again zero-delay (2/0-FP-1.5)and 0.5 sec hold (2/0-2M-0.5) were successively introduced. Then, with simultaneous and 1.5 sec hold, the retrieval cues were allowed to appear on
462
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TABLE III TRIALS(ANDERRORS)TO CRITERIONFOR PROBLEMSIN SECONDATTEMPTAT RETRAINING For explanation of 2S-FP-1.5, etc., see text. Problem
2S-FP-1.5 20-FP-1.5 20-FP-0.5 2S-2M-1.5 20-2M-1.5 20-2M-0.5 2S-4M-1.5 20-4M-1.5 20-4M-0.5 3S-FP-1.5 30-FP-1.5 30-FP-0.5 3S-4M-1.5 30-4M-1.5 30-4M-0.5 4S-FP-1.5 40-FP-1.5 40-FP-0.5 4S-M-1.5 40-M-1.5 40-M-0.5 Simultaneous: Red vs. yellow Green vs. blue
Animals IT-7
1ST-5
IST-6
3500 (938) 300 (39) Died
800 (152) 0 (0) 0 ( 0) 200 (34) 300 (35) 0 ( 0) 0 ( 0) 0 ( 0) 100 (15) 200 (38) 0 (0) 0 (0) 400 (85) 200 (13) 200 (26) 200 (34) 200 (29) 700 (109) 700 (124) 1100 (128) 0 ( 0)
4000 (1628)*
IST-IO
4o0 (53) 0(0) o(o) o(o) o(o) o(o) 1600 (480) 2400 (592)
* Denotes failure to reach criterion.
any two o f the 4 possible response panels, the outside two being uncovered for this purpose (2/S-4M-1.5). The final task reached via 2/0-4M-1.5, was 2/0-4M-0.5, i.e., that task on which the 3 animals had failed in the first retraining attempt. Red and yellow were then introduced one at a time, the exact sequence o f tasks being that shown in the left hand c o l u m n o f Table III. Since IST-10 had already reached criterion on 3/04M-0.5, he was started immediately on 4/S-FP-1.5. One animal, IST-6, failed on the simplest task, 2/S-FP-1.5. It was therefore transferred to a straightforward simultaneous colour discrimination, red v e r s u s yellow. F o r this task, only the 2 keys used for the matching stimuli on the 2-FP tasks were uncovered. The colours red and yellow appeared on these with a 7.5 sec intertrial interval, their positions varying r a n d o m l y f r o m trial to trial (except for correction trials). The correct response was to the red key. The nature o f the reward and punishment, the n u m b e r o f trials per day, the correction schedule, and the criterion were as in the retraining on matching. W h e n IST-6 had reached criterion on this task, red and yellow were replaced by green (positive) and blue.
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
463
Results Trials and errors to criterion for individual animals on the various problems are shown in Table III. Two animals, IST-5 and IST-10, were able to reach criterion on the 4-alternative zero-delay task (4/0-M-0.5) necessary for a return to the constant delay paradigm. Of the other two, IT-7 died of 'bloat '22 while still on task 2/0-FP-0.5, and so it is not possible to say whether it would have eventually mastered 4/0-M-0.5. Finally, IST-6 failed the simplest problem in the progression, 2/S-FP-1.5, and was in fact still performing at chance at the end of 4000 trials. Nonetheless this animal was able to learn to discriminate red from yellow, and green from blue, when those colours were presented in a simultaneous discrimination paradigm. It is conceivable that having done so it would have then been able to learn the 2/S-FP-1.5 task, but time was not available to test this.
Discussion The results of the second attempt at retraining support the idea that the animals' initial postoperative failure was not caused by an inability to perform the basic delayed matching from sample task. Thus both IST-5 and IST-10 reached criterion on tasks they had formerly failed, and indeed reached the stage at which they could be returned to the constant delay paradigm. Hence for these animals the purpose of the experiment, to measure delayed matching from sample capacity before and after inferotemporal lesions, could be carried out. This will be described in the next section. It is not clear why IST-6 did so poorly. It may have been because its lesion was rather deep, damaging the hippocampus on both sides (Fig. 1). It was also the worst animal at delayed matching from sample before operation, (scoring only 50 ~ at 10 sec with 4 alternatives) and might for this reason have been the most affected by the lesion. POSTOPERATIVE DELAYED MATCHING FROM SAMPLE CAPACITY
Subjects The subjects were the 2 animals, IST-5 and IST-10, that reached criterion on 4alternative zero-delay matching from sample in the previous section.
Apparatus The apparatus was that used in the first part of this experiment, as were the colours (red, green, blue and yellow) for sample and retrieval cues.
Procedure The animals were first overtrained on 4-alternative zero delay matching with a 0.5 sec sample hold and using a non-correction procedure, to 5 successive days at 90 each. Thereafter they were started on the (0, 1, 2, 5) sec condition previously described. The procedure followed was identical to that used in the first part of this experiment, except that these animals' performance on (0, 1, 2, 5) was so good that they were transferred after 5 sessions to their postoperative delay values, that is (0, 7.5, 15, 30)
464
v. DEAN 20-
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Fig. 3. a and b: number correct plotted against delay for (a) IST-5 and (b) IST-10. In each graph the ordinate shows average number correct per session (i.e., maximum score = 20). The abscissa shows delay in seconds. The upper graph of each pair represents performance on 2 alternatives, the lower graph performance on 4 alternatives. Unfilled circles -- the 40 preoperative stable sessions. Filled circles = the 20 postoperative sessions at preoperative delay values.
for IST-10, (0, 15, 30, 50) for IST-5 with 2 alternatives, and (0, 5, 10, 20) with 4. They were tested for 20 sessions at these delays. N o criterion o f stable performance was used since it was clear that as soon as the animals encountered these delay values they were able to do at least as well on them as during the preoperative stable run.
Results On pretraining, IST-5 t o o k 1500 trials, 213 errors, and IST-10 200 trials, 21 errors, to reach the criterion. F o r delayed matching f r o m sample the p e r f o r m a n c e delay curves for pre- and postoperative performance are shown in Fig. 3. These are derived f r o m the 40 preoperative stable sessions, and the 20 postoperative ones. As can be seen, IST-10 tends to do about as well after operation as before, although in one condition, 2-0, it is significantly worse after (t ~ 2.296, df = 58, P < 0.05). IST-5, on the other hand, does better after operation for longer delays than before: the differences in performance are significant for the 2-B condition (t = 3.59, P < 0.001), the 2-C (t = 2.57, P < 0.02) and the 4-C (t = 3.05, P < 0.01). Pre- and postoperative reaction times tu the match stimuli are plotted for the 2 animals in Fig. 4. These were calculated f r o m the first and last 10 sessions o f the preoperative stable run and from all 20 postoperative sessions. IST-5 (Fig. 4a) was significantly slower after operation for all conditions. The significance level is 0.001 except for the 2-A (0.002), 2-B (0.05) and 2-C (0.02) conditions. (Since each point on
465
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY 2.5-
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Fig. 4. a and b: reaction time plotted against delay for (a) IST-5 and (b) 1ST-10. In each graph the ordinate shows the mean reaction time in seconds, the abscissa the delay in seconds. Reaction times are for correct responses only. The upper graph of each pair gives times for 2 matching alternatives, the lower for 4. Unfilled squares -- the first and last 10 sessions of preoperative stable run. Filled squares = the 20 postoperative sessions.
the graphs is derived from more than 300 reaction times, the test used for these levels was that based on the normal distribution.) For IST-10 (Fig. 4b) the postoperative reaction times were slower for only some conditions: 2-0, 2-A, 4-0 and 4-A (in all cases P < 0.001), and 4-B (P < 0.02). There was no significant difference between the times for 2-B, 2-C and 4-C. Errors were also analysed for the 20 postoperative sessions and the first and last 10 sessions of the preoperative stable run. Table IV shows those proportions of errors that were to the sample of the preceding trial, when this was correct. These were significantly above the chance value of 25 ~ for both animals, both before and after operation (chi-squared test; 3rd and 5th columns). Both animals made a smaller proportion of such errors after operation, but this difference was significant for IST-10 alone (6th column). Discussion
This experiment was designed to measure the effects of inferotemporal removal on the asymptotic performance of 4-alternative delayed matching from sample. These effects are clear from the accuracy data plotted in Fig. 3; once the animals have been retrained after operation to a stringent criterion at zero delay, they can perform at their preoperative levels at all delays. These results therefore provide no evidence of impaired asymptotic performance after inferotemporal lesions.
466
P. DEAN
TABLE IV PERCENTAGE OF TOTAL ERRORS THAT THERE WERE TO THE SAMPLE COLOUR OF THE PRECEDING TRIAL (CHANCE ~
Animal
25~)
Pre-op.
Vs. chance
( %J IST-5 IST-10
50.6 55.2
Post-op.
Vs. chance
Pre vs. post
0.001 0.001
N.S. 0.01
( %J 0.001 0.001
44.1 41.2
The experiment also provides evidence in support of an interpretation of Buffery's results1, 2, suggested in the Introduction. This was that although inferotemporal lesions might affect the retention and learning of the basic 4-alternative matching task, they did not selectively impair its performance at long delays. In agreement with this interpretation, the rapid adjustment of IST-5 and IST-10 to long delays was in striking contrast to their difficulty in reaching criterion at zero delay, and also to the trouble normal rhesus monkeys have when encountering delay in matching tasks for the first timeT,11,is. Even in preoperative overtraining in this experiment, when IST-5 and IST-10 had already had considerable experience with delay7, they required 10 and 35 sessions respectively to reach their stable delay values. But post-operatively they could perform at these values after, at most, 5 sessions, once they had reached criterion at zero delay. It seems likely, therefore, that Buffery's results were caused at least in part by his operated animals not having learnt the 4-alternative task as well as the normal animals at zero delay. The fact that inferotemporal lesions do not affect the asymptotic performance of delayed matching from sample is powerful evidence against the hypothesis mentioned in the Introduction, that animals with inferotemporal ablations have a reduced capacity to remember visual stimuli. The hypothesis might still be correct if the sort of visual memory used in discrimination learning differed in some important way from that tested by delayed matching from sample. Three potential differences can be excluded. (1) The unimpaired postoperative performance in this experiment was obtained with colours that were very easy to discriminate. But Wilson e t al. ~6 also found no impairment, even immediately after operation, on delayed matching with patterns as stimuli. Animals with inferotemporal lesions show very clear learning impairments on simultaneous pattern discrimination. (2) It is not the case that interference is present only in discrimination learning, and not matching. Error analysis showed that after operation IST-5 and IST-10 made a greater than chance proportion of their errors to the sample of the preceding (correct) trial (Table IV), i.e., there was proactive interference. Also, D'Amato and O'Neill 6 have shown that illumination during the intratrial delay worsens performance, an effect they attribute to interference. Such illumination was used in the present experiment. (3) It cannot easily be maintained that delayed matching from sample tests only 'short-term memory' (while discrimination learning involves longer term pro-
EFFECT OF INFEROTEMPORAL LESIONS ON MEMORY
467
cesses) - - even allowing that the long-term/short-term distinction is applicable to monkey memory. Depending on the circumstances, monkeys can perform delayed matching with substantial intratrial delays: in this experiment, two animals showed clear signs of retention at 50 sec delay, and Mello 19 has reported 95 ~ correct matching after 232 sec. These intervals are long compared with those normally used in shortterm memory experiments with people. Furthermore, it has been argued by Waugh and Norman 23 that when retention is measured after even short periods, information is retrieved from both 'short-term' (or more accurately 'primary') memory and 'long-term' (or 'secondary') memory. By this argument, defective secondary memory should be revealed by a delayed matching from sample paradigm. It can thus be concluded that, in certain important respects, the kind of visual memory involved in delayed matching from sample resembles that concerned in discrimination learning. It is correspondingly improbable that animals with inferotemporal lesions learn visual discriminations slowly because their memory for visual stimuli is defective. This conclusion does not of course apply to visual association memory, which, as pointed out in the Introduction, is not tested in delayed matching from sample. Two other features of the results require comment. One is that the inferotemporal lesions produced what appeared to be an almost total retrograde amnesia for delayed matching from sample with 4 samples. Similar effects of inferotemporal removal have also been found by BufferyI and by Wilson et al. 26, at least for colours. However, only in the present experiment were the animals very extensively overtrained for more than 10,000 trials before operation. For simultaneous discriminations much less overtraining than this (i.e., not more than 500 trials) abolishes the retrograde amnesia normally accompanying inferotemporal removal4, ~1. It is not clear which features of the delayed matching from sample paradigm confer this resistance to the effects of preoperative overtraining, but one possibility is that the samples are presented one at a time. The animal must therefore identify them without benefit of the relational cues available in simultaneous discriminations. If inferotemporal removal interfered with the processes responsible for stimulus identification, the vulnerability of delayed matching from sample to its effects would be explained. More direct tests of this hypothesis are currently being carried out in this laboratory. Secondly, both IST-5 and IST-10 had substantially longer reaction times to the matching stimuli after operation (Fig. 4). It is not clear what this difference means. There are discrepancies, which may be important, between the reaction time changes for the two animals: thus the reaction times of IST-5 increase more for 4 than for 2 alternatives, but those of IST-10 increase about the same for both conditions, and while IST-10's increase vanishes when the delay reaches 30 sec, IST-5's increase seems to reach asymptote with long delays. Moreover the animals were not made to respond as fast as they could, so their slow reaction times do not necessarily reflect an inability to respond at preoperative speeds (cf. DeanS). This also applied to Buffery's1 reaction time results, which agree with those here in showing animals with inferotemporal lesions to be slower than normals at the matching stage of 4-alternative delayed matching from sample, even at zero-delay. Nonetheless, the slower reaction times are not
468
P. DEAN
inconsistent with the possibility that animals with inferotemporal lesions have a smaller capacity for identifying visual stimuli, so that dealing with 4 samples is a more difficult task for them than for normal animals. ACKNOWLEDGEMENTS
This research was supported by MRC Grants G 967/2/B and G 971/397/B. I thank Mr. J. P. Broad and Mr. C. Blackmore for photographing the figures, and Mr. I. H. Lloyd and Miss M. McAnulty for preparing the histological material. I am especially grateful to Professor L. Weiskrantz for performing the surgery, and for much helpful discussion and advice.
REFERENCES 1 BUFFERY,A. W. H., The Effects of Frontal and Temporal Lesions upon the Behaviour of Baboons, Unpublished Ph.D. Dissertation, University of Cambridge, England, 1964, 412 pp. 2 BUFFERY,A. W. H., Attention and retention following frontal and temporal lesions in the baboon. In Proceedings of the 73rd Annual Convention of the American Psychological Association, Washington, 1965, pp. 103-104. 3 BUTLER, C. R., Is there a memory impairment in monkeys after inferotemporal lesions? Brain Research, t3 (1969) 383-393. 4 CHOW, K. L., AND SURVlS,J., Retention of overlearned visual habit after temporal cortical ablation in monkey, Arch. Neurol. Psychiat. (Chic.), 79 (1958) 640-646. 5 COWEY, A., AND GROSS, C. G., Effects of foveal prestriate and inferotemporal lesions on visual discriminations by rhesus monkeys, Exp. Brain Res., 11 (1970) 128-144. 6 D'AMATO, M. R., AND O'NEILL, W., Effect of delay interval illumination on matching behaviour in the capuchin monkey, J. exp. Anal. Behav., 15 (1971) 327-333. 7 DEAN, P., Functions of the Temporal Lobe in Visual Discrimination and Memory in Macaca mulatta, Unpublished D. Phil. Dissertation, University of Oxford, 1972, 373 pp. 8 DEAN, P., Choice reaction times for pattern discriminations in monkeys with inferotemporal lesions, Neuropsyehologia, (1974), in press. 9 DEAN,P., AND WEISKRANTZ,L., Loss of preoperative habits in rhesus monkeys with inferotemporal lesions: recognition failure or relearning deficit? Neuropsychologia, (1974), in press. 10 DEWSON, J. H., III, PRIBRAM, K. H., AND LYNCH, J. C,, Effects of ablations of temporal cortex upon speech sound discrimination in the monkey, Exp, Neurol., 24 (1969) 579-591. 11 DRACHMAN, D. A., AND OMMAYA, A. K., Memory and the hippocampal complex, Arch. Neurol. (Chic.), 10 (1964) 411-425. 12 ETKIN, H., AND D'AMATO, M. R., Delayed matching to sample and short-term memory in the capuchin monkey, J. comp. physiol. Psychol., 16 (1969) 544-549. 13 ETTLINGER, G., IWAI, E., MISHKIN, M., AND ROSVOLD, H. E., Visual discrimination in the monkey following serial ablation of inferotemporal and pre-occipital cortex, J. comp. physiol. Psychol., 65 0968) 110-117. 14 GROSS, C. G., Visual functions of inferotemporal cortex, In R. JUNG (Ed.), Handbook of Sensory Physiology, Vol. VII/3, part B. Central Visual It~formation, Springer, Berlin, 1973, pp. 451482. 15 GRoss, C. G., COWEY, A., AND MANNING, F. J., Further analysis of visual discrimination deficits following foveal prestriate and inferotemporal lesions in monkeys, J. comp. physiol. Psychok, 76 (1971) 1-7. 16 IVERSEN, S. D., AND WEISKRANTZ, L., Temporal lobe lesions and memory in the monkey, Nature (Lond.), 201 (1964) 740-742. 17 IVERSEN, S. D., AND WEISKRANTZ, L., An investigation of a possible memory defect produced by inferotemporal lesions in the baboon, Neuropsychologia, 8 (1970) 21-36. 18 JARRARD,L. E., AND MOISE, S. L., Short-term memory in the monkey. In L. E. JARRARD(Ed.), Cognitive Processes of Non-Human Primates, Academic Press, New York, 1971, pp. 1-24.
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19 MELLO, N, K., Alcohol effects on delayed matching to sample performance by rhesus monkey, Physiol. Behav., 7 (1971) 77-101. 20 MISHKIN, M., Cortical visual areas and their interactions. In A. G. KARCZMAR AND J. C. ECCLES (Eds.), The Brain and Human Behaviour, Springer, Berlin, 1972, pp. 187-208. 21 ORBACH,J., AND FANTZ, R. L., Differential effects of temporal neo-cortical resections on overtrained and non-overtrained visual habits in monkeys, J. comp. physiol. Psychol., 51 (1958) 126-129.
22 TURNER,A. E., AND COWEY, A., Bloat syndrome in captive rhesus monkeys: report on twelve cases, J. Inst. Anita. Techn., 22 (1971) 181-186. 23 WAUGH, N. C., AND NORMAN, D. A., Primary memory, Psychol. Rev., 72 (1965) 89-104. 24 WEISKRANTZ,L., Experimental studies of amnesia. In C. W. M. WHITTV AND O. L. ZANGWILL (Eds.), Amnesia, Butterworth, London, 1966, pp. 1-35. 25 WEISKRANTZ,L., Central nervous system and the organization of behaviour. In D. P. KIMBLE (Ed.), The Organization of Recall, New York Academy of Science, 1967, pp. 234-293. 26 WILSON,M., KAUFMAN, W. M., ZIELER,R. E., AND LIEB, J. P., Visual identification and memory in monkeys with circumscribed inferotemporal lesions, J. comp. physiol. Psychol., 78 (1972) 173-183.