- Email: [email protected]
Interocular transfer of extinction of visual pattern discriminations in split-chiasm and split-brain cats
EXPERIMENTALNEUROLOGY
101,276-287
(1988)
Interocular Transfer of Extinction of Visual Pattern Discriminations in Split-Chiasm and Split-Brain Cats GIAN G. MASCETTI
AND JORGE R. ARRIAGADA’
Laboratorio de Neurobiologia, Facultad de Ciencias Biolbgicas, P. Universidad Catblica de Chile, Santiago, Chile Received September 29, 1987; revision received December 2,1987 The interocular transfer of the extinction of visual pattern discriminations was studied in cats with either section of optic chiasm (split-chiasm cats) or combined sections of chiasm and forebrain commissures (split-brain cats). Visual pattern discriminations were monocularly learned and their interocular transfer was assessed through the opposite eye. Then, learning was unilaterally extinguished and interocular transfer of extinction was tested on the other side. In split-chiasm cats, the total number of trials to extinction criterion (EC) was significantly lower with the second eye than with the first eye, indicating a successful interocular transfer. In split-brain cats, EC with the second eye was attained faster than with the first in some performances; it was similar with both eyes in other tasks, and with the second eye was higher than with the first in still other tasks. Statistical analysis applied to this group of split-brain cats pointed out that extinction performances with the two eyes were not significantly different. These findings suggest that interocular transfer of extinction was abolished in split-brain cats and that memory for extinction was unilaterally established in the absence of forebrain commissures. o 1988 Academic press, IIIC.
INTRODUCTION The processes of interhemispheric communication and transference of memory are of great interest in understanding brain function. Most studies of such phenomena have been performed on human subjects or experimental animals with partial or complete interruption of neural connections between both hemispheres. In cats, the midsagittal section of the optic chiasm Abbreviations: E-transference efficiency, EC-extinction criterion, S-saving, SB-split brain, SC-split-chiasm. ’ Supported by Grant 72/82 of Dire&on de Investigacibn, Universidad Cat&a de Chile (DIUC). We are grateful to Dr. Patricia Zapata for the critical reading of the manuscript. 276 0014-4886/88 $3.00 Copyright 0 1988 by Academic F’res, Inc. All rights of reproduction in any form reserved
INTEROCULAR
TRANSFER
277
leaves the neural output of each eye limited to the ipsilateral hemisphere. Consequently, interocular transfer becomes equivalent to interhemispheric transference of neural information ( 14). It is well known that the interocular transfer of visual pattern discriminations is successful in split-chiasm cats (17) and that it is abolished after the additional section of corpus callosum (18,23). Several studies have confirmed the important role of callosal commissure in the interhemispheric integration of visual learning (5, 7, 15, 19,20). The interocular transfer of visual pattern discrimination has been studied in relation to both acquisition (3, 14, 17) and reversal learning (16). However, several studies suggest that extinction would be mediated by a neural system distinct from that of acquisition and reversal learning (6, 10, 13, 24, 25). Therefore, in this work we studied the interocular transfer of extinction of visual pattern discriminations. For this purpose, visual discriminative behavior was learned in both hemispheres in split-chiasm and split-brain cats. Then, the animals were submitted to unilateral extinction and interocular transfer was assessed on the other side. METHODS Experiments were performed in two groups of adult cats: four with section of the optic chiasm (split-chiasm (SC) cats) and five with sections of the optic chiasm and corpus callosum (split-brain (SB) cats). Also, the hippocampal and habenular commissures laying in close apposition with corpus callosum were sectioned. These cats will be named SC 1 to SC4 and SB 1 to SB5, respectively. The operations were performed under Na pentobarbitone anesthesia (Nembutal, 36 mg/kg), with the aid of a stereomicroscope and with the use of surgical procedures described by Myers (17) for optic-chiasm and by Sperry (22) for corpus callosum. Experimental testing was done in a two-choice apparatus. After leaving the starting chamber (68 X 48 cm), the animal entered a decision chamber (75 X 48 cm) and faced two side-by-side plexiglass doors equally illuminated from behind and bearing the discriminanda (patterns made with black tape and equated for area). The decision chamber was divided in two alleys by a partition (last 45 cm) except at its beginning (initial 30 cm). Each alley led to one door and in order to change alleys, the animal had to return to the beginning of the decision chamber, turn around the partition, and enter the other alley. After crossing the door, the animal returned to the starting chamber through a returning alley ( 195 X 25 cm). The position of the two stimuli was changed according to a Gellerman sequence (9). A 40-trial daily session was carried out 5-6 days per week. The animals were food-deprived for 23 h before training sessions.
278
MASCETTI
AND ARRIAGADA
FIG. 1. Pairs of patterns used for discriminations, each pair having the same area. Patterns on the left were chosen as positive stimuli in acquisition, relearning, and Test Problem. A-Test Problem; B and C-problems B and C, respectively.
After surgery, all animals learned to work in the apparatus after being trained with both eyes in dark-light discrimination (one door lit and the other dark). Subsequently, pattern discriminations were learned with one eye (first eye) while the other one (second eye) was covered with a black plastic occlusive device. The animals were submitted to three discriminative tasks in the sequence corresponding to the correlative letters of the problem shown in Fig. 1. Problem A (test problem) was learned and interocularly transferred, but not extinguished. Problems B and C were learned and then extinguished. In the acquisition stage, a correct choice was scored when the animal pushed and opened the door with a positive stimulus, thus gaining access to a piece of bovine kidney. The other door was locked and colliding against it was the punishment for making an error. After an error, however, the cat was allowed to go through the correct door to have access to the food. In other words, a correction procedure was used at all stages. Final learning criterion was attained when 90% or more correct responses were obtained on 2 consecutive days. Then, 200 overtraining trials were given after which interocular transfer was tested with the second eye (the black plastic occlusive device was placed on the first eye) until the learning criterion was reattained. Reinforcement. A positive reinforcement (piece of kidney) was given at the end of each trial, being indispensable for the completion of this task. If this reward was not given for a few consecutive trials, the animal refused to work in the apparatus. When committing errors, cats collided against the locked door (sometimes twice or thrice) and they must then return to the beginning of the decision chamber, turn around the partition, and push to open the door with positive stimulus. The collision and the excessive delay in gaining access to the endtrial reward were considered negative reinforcement or punishment. Extinction. The extinction procedure consisted of removing the punishment, i.e., unlocking the two doors (free-choice condition) to eliminate the
INTEROCULAR
TRANSFER
279
significance of the discriminanda (4). The position of the patterns was still changed according to the Gellerman sequence. The cats trained monocularly (the occlusive device was placed on the second eye) stopped discriminating and progressively acquired a preference for the door on one side (position habit or side preference). The extinction criterion (EC) was attained when preference for one side was exhibited during 20 consecutive trials (4). If the EC was reached in the middle of a row of 10 trials, that row was completed. Then, the open eye was changed (the device was placed on the first eye) and training continued until the EC was reattained with the second eye. After bilateral extinction was reached, problem specificity of extinction was tested by submitting the animals to the Test Problem (40 trials with each eye) in free-choice conditions but with correct responses and errors being computed as during acquisition. Finally, the extinguished problem was monocularly relearned (relearning), alternating the open eye every 40 trials until the learning criterion was reattained. Analysis ofdata. Performances of the two eyes on each pattern’s discrimination were assessed on the basis of the following indexes: ( 1) Total number of trials before attaining learning or extinction criteria were included. For acquisition, the total number of errors was also computed. Once criteria were reached trials and errors were not included. Differences between both groups of animals were ascertained by the Wilcoxon matched pairs test. (2) Saving (S) was assessed according to the formula S = (total trials with the second eye/total trials with the first eye) X 100. An S value approaching 100 meant little or no saving with the second eye, while a value approaching 0 indicated saving. The saving values in the extinction of both groups of cats were compared by means of the Mann-Whitney test. The same test was employed where scores of acquisition and relearning were compared. Histology. After completion of the studies, completeness of commissurotomies and damage caused by surgery were ascertained by histological examination of the brains. The animals were perfused through the heart with 10% Formalin and the brains were serially sectioned with a freezing microtome to obtain IO-pm slices. A modified Nissl technique for staining cells and fibers was employed. RESULTS Split-chiasm cats. All these animals showed a positive interocular transfer of the acquisition (initial learning) of visual pattern discriminations. Table 1 shows the scores to criterion of both eyes. The total number of trials and errors were significantly lower with the second eye than with the first; in addition, S values were low, indicating a saving with the second eye. These results are in agreement with those reported by Myers ( 17, 18) Berlucchi et al. (3), and Lepore et al. ( 14).
280
MASCETTI
AND ARRIAGADA TABLE 1
Trials and Errors to Learning Criterion and Saving(S) in Split-Chiasm Cats Problem A
Problem B
Problem C
Cat
First eye
Second eye
S
First eye
Second eye
S
First eye
Second eye
S
SC1 SC2 SC3 SC4
320/Z 24019 1 360162 400187
80/15 4019 8019 4019
25 17 22.2 9
680/ 198 7601214 12901368 800/279
240/58 4801112 o/o o/o
35 63 0 0
1280/317 120122 400/8 1 200/60
680/131 4019 80/11 120129
53 33 20 60
Note. Trials and errors at criterion are not included.
Table 2 summarizes the scores of extinction of visual pattern discriminations in split-chiasm cats. In all animals, the EC with the second eye was reached with fewer trials than with the first, the difference being statistically significant (P < 0.005, Wilcoxon test). In addition, there was a significant saving with the second eye as indicated by the low S values. Figure 2A illustrates the interocular transfer of extinction of cat SC3. The sequence shown in the bar histogram and the scores indicates that the EC TABLE 2 Trials to Extinction Criterion (EC) and Saving(S) in Split-Chiasm Cats (SC) and Split-Brain Cats (SB) Problem B
Problem C
Cat
First eye
Second eye
S
First eye
Second eye
S
SC1 SC2 SC3 SC4 SBl SB2 SB3 SB4 SBS
800 320 260 160 290 440 130 120 90
140 70 0 0 90 50 150 150 240
17.5 21.8 0 0 31 11.3 115.3 125 266
480 100 320 130 280 200 470 290 100
50 50 20 70 160 370 20 50 240
10.5 50 6.2 53.8 57 185 4.2 17.2 240
Note. Trials to EC of the two eyes are significantly different in split-chiasm cats (P < 0.005, Wilcoxon test), but they are not significantly different in split-brain cat (P > 0.05, Wilcoxon test). Saving scores of split-chiasm cats are significantly different from those of split-brain cats (P c 0.05 Mann-Whitney test).
INTEROCULAR
TRANSFER
281
FIG. 2. A-interocular transfer of extinction of split-chiasm cat SC3 in problem C. Bar histograms, each bar corresponds to 10 consecutive trials. First, middle, and last groups of four bars with the first eye correspond to beginning, middle, and end of extinction with that eye (total trials to EC = 320). Extinction with the second eye is shown entirely (total trials to EC = 20). Ordinate, side preference for left or right door. B-discriminative performance in the Test Problem, showing errors with each eye (40 trials per eye). Trials and errors to learning criterion in relearning were: first eye, 80/24, and second eye, 80/2 1.
with the second eye was attained faster than with the first. Also, the same side preference was adopted for extinction by both eyes: the left door was selected with the first eye, and the same one was preferred by the second eye. The equivalence of side preference with both eyes was observed in all animals with the exception of cat SC2 in problem B. Statistical analysis showed that side preference of the second eye was not random and that it coincided with that of the first eye (P < 0.025, chi-square test). The learning of problem C was specifically extinguished because scores obtained in the test problem were above 90% of correct responses (Fig. 2B). Correct trials and errors were 38/2 and 38/2 for the first and second eye, respectively. All the split-chiasm cats showed a high level of discrimination when submitted to the test problem. Scores obtained in the relearning of the criterion for problems B and C are shown in Table 3. Relearning with the first eye was carried out with fewer trials and errors compared with the scores obtained in the acquisition with the same eye. Statistical analysis indicated that total trials and errors of both learning processes were different (P < 0.025, Mann-Whitney test, one tail). On the other hand, since the interocular transfer of acquisition was successful in these animals, scores of acquisition and relearning with the second eye were not statistically different (P > 0.10 Mann-Whitney test, one tail). Split-brain cats. The interocular transfer of acquisition of problems B and C was abolished in these animals. Table 4 shows the scores to criterion of
282
MASCETTI
AND ARRIAGADA TABLE 3
Trials and Errors to Learning Criterion following Extinction (Relearning) in Split-Chiasm (SC) and Split-Brain Cats (SB) Problem B Cat
First eye
SC1 SC2 SC3 SC4 SBl SB2 SB3 SB4 SB5
40112 240139 40114 4018 4015 4018 160/52 120136 80117
Problem C
Second eye
First eye
Second eye
4016
4017 4018 80124 o/o 4015 120136 4019
80/14 4018 80/2 1 120/21 80/11 80/13
16OJ37
120132 120/18
160/13 120/30 120129 o/o 120120 16OJ40
120135 4019
4oJ6
120128
Note. Trials and errors at criterion are not included.
both eyes. The total number of trials and errors with each eye were not different; in addition, S scoreswere high and in some casesthey surpassedthe value of 100. These resultsare in accordancewith those reported by Sperry et al. (23), Myers ( 18), Berlucchi et al. (3), and Mascetti et al. (16). The extinction behavior of split-brain cats is summarized in Table 2. In certain cases,the EC with the second eye was attained with fewer trials than with the first (SB1and SB2 in problem B and SB1, SB3, and SB4 in problem C); S scoreswere low, In other cases,there was no difference between both TABLE 4 Trials and Errors to Learning Criterion and Saving(S) in Split-Brain Cats Problem A
Problem B
Problem C
Cat
First eye
Second eye
S
First eye
Second eye
S
First eye
Second we
S
SBl SB2 SB3 SB4 SBS
11601467 400/l 14 240158 400/116 5601155
10801527 480/160 160146 5601252 7601204
93 120 67 140 136
280171 440/138 3201116 240154 880/343
240/66 640/160 4401164 280166 5601230
86 145 138 116.5 64
6401180 680/149 6001153 400/102 5201200
5201159 840/181 5601148 320/81 6401273
88 123.5 93 80 123
Note. Trials and errors at criterion are not included.
INTEROCULAR
TRANSFER
283
FIG. 3. A-interocular transfer of extinction of split-brain cat SB2 in problems C (upper) and B (lower). Bar histograms, each bar corresponds to 10 consecutive trials. First, middle, and last groups of four bars with each eye correspond to the beginning, middle, and end of extinction. Extinction with the second eye in problem B is shown entirely. Ordinate, side preference for left or right door. B-discriminative performance in the Test Problem, showing errors with each eye (40 trials per eye). Trials and errors to learning criterion were: problem C, first eye, 120/36, second eye, 80/l 3; problem B, first eye, 40/8, second eye, 120/20.
eyes (SB3 and SB4 in problem B) or even more trials were needed with the second eye (SB2 in problem C and SB5 in both problems); S scores were at or well above 100. However, the performance with both eyes for the entire group was not statistically different (P > 0.05, Wilcoxon test). Figure 3A shows the extinction behavior of cat SB2. The EC with the second eye was attained with more trials than with the first in problem C (upper part), but that level was reached with the second eye with fewer trials than with the first in problem B (lower part). An interesting finding was that side preference with each eye was opposite in 6 of the 10 interocular transfer testings of split-brain cats. Statistical analysis showed that side preference with the second eye was random and that it did not coincide with that of the first eye (P > 0.5, chi-square test). For example, Fig. 3A shows that side preference with both eyes was to the left in problem C; in problem B, with the first eye, side preference was to the left, while with the second one it was to the right. In this cat, scores for the Test Problem were above 90% of correct responses, indicating that extinction was problem-specific (Fig. 3B); correct responses and errors in the 40 trials were 39/l and 38/2 (upper part) for the first and second eye, respectively, in problem C, and were 38/2 and 39/l (lower part), respectively, in problem B. Both problems B and C were relearned with each eye with fewer trials and fewer errors committed than during acquisition (Table 3). Statistical analyses
284
MASCETTI
A
AND ARRIAGADA
B
SC
,.’
SB2
k
“pu.
FIG. 4. Selected coronal brain sections of one split-chiasm cat (SC3) and one split-brain cat (SB2). A-medial part of optic chiasms. B-caudal part of optic chiasm (SC3) and level of posterior commissure (SB2). Arrows indicate the sections. Cat SC3 had the forebrain commissures sectioned after completion of the present behavioral studies, because it was subsequently used in another series. Anterior commissure was left intact in SB cats.
indicated that total trials and errors of SB cats in both learning processes were significantly different: for the first eye, P < 0.005; for the second eye, P < 0.005 (Mann-Whitney test, one tail). Histological results. The optic chiasm was found completely sectioned in all cats. In addition, corpora callosa and the hippocampal and habenular commissures were also found totally sectioned in split-brain cats. Representative sections of the brain of cats SC3 and SB2 are shown in Fig. 4. The anterior commissure was not sectioned (Fig. 4, cat SB2). DISCUSSION The findings of this study indicated that the extinction of visual pattern discriminations was successfully transferred from one eye to the other in
INTEROCULAR
TRANSFER
285
split-chiasm cats. In fact, scores and statistical analyses showed that the EC with the second eye was reached faster than with the first. Here, we propose that the transference efficiency (E) for a given capability from one hemisphere to the other may be estimated as E = 100 - S (100 meaning perfect transfer). With the application of this measurement, the efficiency of the interhemispheric transfer of extinction of visual pattern discriminations varied between 46.2 and 100 in split-chiasm cats. In addition, the strategy that splitchiasm cats used for extinction (side preference) with both eyes was the same in each discriminative problem, suggesting that the processes underlying extinction would be related in both hemispheres. Opposite results were found after additional section of forebrain commissures (split-brain cats). With the application of the efficiency estimate to these cats in problem B and C performances, E varied between 95.8 and - 166, i.e., between nearly perfect transfer to a total absence of interocular transfer of extinction. In fact, in only one cat (SBl) out of five, trials to the EC with the second eye were fewer than those with the first. In the opposite extreme, in another cat (SB5) the number of trials to the EC with the second eye was more than twice that required with the first eye. The remaining three cats showed apparently more or less similar efficiency in one task but were less effective in the other one. As an entire group, trials to the EC in split-brain cats were not significantly different for both eyes (P > 0.05, Wilcoxon test). Therefore, we propose that the transference of extinction was absent in splitbrain cats. In other words, memory for extinction remained lateralized on the hemisphere connected with the first eye, although the time course of extinction with the second eye was faster in certain cases and slower in others. Two findings support this interpretation. First, statistical analysis applied to the group showed that scores with the second eye were not significantly different from those with the first eye. Statistical analysis also pointed out that S values of split-brain cats were different from those of split-chiasm cats where interocular transfer of extinction was successful (P < 0.05, MannWhitney test). Second, side preference with the second eye was random and it did not coincide with that of the first eye (P > 0.5, chi-square test). In fact, side preference of the two eyes was opposite in six tasks and the same in four. This finding would suggest that the processes underlying extinction were independent in both hemispheres. The findings of this study are similar to those previously reported for acquisition (3, 17, 18, 19) and reversal learning (16). In general, they confirm that the commissural system mediated the transference of learning and memory from one hemisphere to the other. On the other hand, they point out that forebrain commissures mediate the transference of extinction, although the neural mechanism and anatomical systems involved in extinction seem to be different from those involved in acquisition (6, 10, 13,24,25).
286
MASCETTI
AND ARRIAGADA
In chicks, Benowitz (2) reported that memory for extinction can be established only in the hemisphere contralateral to the eye trained. In other words, monocularly learned extinction was found not to be retrievable through the untrained eye. Instead, acquisition led down memory traces in both hemispheres and it could be retrievable through the untrained eye. On the basis that the two learning processes are mediated by distinct neural systems (6, 10, 13, 24, 25) the crucial point seems to be the presence of commissural connections in both systems. The absence of neocommissures in chicks (1) meant that extinction was not transmitted through the midline. The splitbrain cats of this study would show a similar condition since memory for extinction could be established only in one hemisphere. It is difficult to identify the commissures involved in the transference of extinction because multiple interhemispheric pathways that were intact in SC cats were cut in SB cats. However, it is well known that the corpus callosum plays an important role in the interhemispheric integration of visual learning (5,7, 15, 19,20) and it could be suggested that the commissure participates in the process of interocular transfer of extinction. The mechanisms underlying extinction have been the subject of great interest and many studies. Pavlov (2 1) and Hull (12) proposed that extinction could be caused by an internal buildup of inhibitory processes which eliminate previous responses. Guthrie (11) and Estes (8) attributed extinction to the acquisition of a competing response. Thus, when the animals stop responding in a certain way they may be learning alternative responses to those conditioned during original learning. In the present study, the discriminative response was replaced by side preference during extinction. Thus, we may argue that side preference was the alternative response causing the extinction of a visual pattern discriminative behavior. That response was successfully transferred from one hemisphere to the other in split-chiasm cats and it remained lateralized on the hemisphere connected with the first eye in splitbrain cats. We also argue that side preference was not an inspecific position habit because scores obtained for the Test Problem were at or above 90% of correct responses. In addition, side preference response was quickly eliminated in relearning. In this last stage, animals started discriminating again after a few trials and attained learning criterion with significantly fewer trials and errors than in the acquisition stage. REFERENCES 1. ARIENS-UPPERS, C. U., C. HUBER, AND E. C. CROSBY. 1936. The Comparative Anatomy of the Nervous System of Vertebrates, including Man. Macmillan, New York. 2. BENOWITZ, L. 1974. Conditions for the bilateral transfer of monocular learning in chicks. Brain Res. 65: 203-2 13. 3. BERLUCCHI, G., E. BUCHTEL, C. A. MARZI, G. G. MASCETTI, AND A. SIMONI. 1978. Effect of experience on interocular transfer of pattern discriminations in split-chiasm and splitbrain in cats. J. Comp. Physiol. Psychol. 92: 532-543.
INTEROCULAR
TRANSFER
287
4. BERLUCCHI, G., AND C. A. MARZI. 1970. Veridical interocular transfer of lateral mirrorimage discriminations in split-chiasm cats. J. Comp. Physiol. Psychol. 72: l-7. 5. BERLUCCHI, G., AND C. A. MARZI. 1982. Interocular and interhemispheric transfer of visual discriminations in the cat. In D. J. INGLE, M. A. GOODALE, AND R. J. W. MANS. FIELD, Eds., Analysis of Visual Behavior. MIT Press, Cambridge, MA. 6. DOUGLAS, R. J. 1967. The hippocampus and behavior. Psychol. BUN. 67: 416-442. 7. DOWNER, J. L., DE C. 1958. Role of corpus callosum in transfer of training in Macacca Mulatta. Fed. Proc. 17: 37. 8. ESTES, W. K. 1959. The statistical approach to learning theory. In S. KOCH, Ed. Psychology A study ofa Science, Vol. 2. McGraw-Hill, New York. 9. GELLERMAN, L. V. 1933. Chance orders of alternating stimuli in visual discrimination experiments. .I. Genet. Psychol. 42: 206-208. 10. GODDARD, G. V. 1964. Functions of the amydgdala. Psychol. Bull. 62: 89-109. 11. GUTHRIE, E. R. 1952. The Psychology oflearning. Harper & Row, New York. 12. HULL, C. L. 1943. Principles ofBehavior. Yale Univ. Press, New Haven, CT. 13. mMBLE, D. P. f968. Hippocampus and internal inhibition. Psychoi. But/. 70: 285-295. 14. LEPORE, F., J. PHANEUF, A. SAMSON, AND J. P. GUILLEMOT. 1982. Interhemispheric transfer of visual pattern discriminations: Evidence for a bilateral storage of the engram. Behav. Brain Res. 5: 359-374. 15. LEVINSON, D. M., AND C. H. SHERIDAN. 1969. Monocular acquisition and interocular transfer of two types of pattern discriminations in hooded rats. J. Comp. Physiol. Psycho/. 67: 486-492. 16. MASCETTI, G. G., C. M. WITTVER, F. A. ROJAS, AND J. R. ARRIAGADA. 198 1. Interocular transfer of reversal learning in split-chiasm and split-brain cats. Res. Commun. Psycho/. Psychiatry Behav. 8: 243-255. 17. MYERS, R. E. 1955. Interocular transfer of pattern discriminations in cats following section of crossed optic fibers. J. Camp. Physiol. Psychol. 48: 470-473. 18. MYERS, R. E. 1956. Function of corpus callosum in interocular transfer. Brain 79: 350363. 19. MYERS, R. R. 1962. Transmission of visual information within and between the hemispheres: A behavioral study. Pages 5 l-74 in V. B. MOUNTCASTLE, Ed., Interhemispheric Relations and Cerebral Dominance. Johns Hopkins Press, Baltimore. 20. MYERS, R. E. 1965. The neocortical commissures and interhemispheric transmission of information. Pages l- I7 in E. C. E-~TLINGER, Ed., Functions ofthe Corpus Cahosum. Little, Brown, Boston. 2 1. PAVLOV, I. P. 1927. Conditioned Reflexes. Translated by G. V. ANREP. Oxford Univ. Press, London. 22. SPERRY, R. W. 1968. Mental unity following surgical disconnection of the cerebral hemispheres. Harvey Lect. 62: 293-323. 23. SPERRY,R. W., J. S. STAMM, AND N. MINER. 1956. Relearning tests for interocular transfer following division of optic chiasm and corpus callosum. J. Comp. Physiol. Psychol. 49: 529-533. 24. URSIN, H. 1965. Effect of amygdaloid lesions on avoidance behavior and visual discriminations in cats. Exp. Neurol. 11: 298-3 17. 25. WEISKRANTZ, L. 1956. Behavioral changes associated with ablations of the amygdaloid complex in monkeys. J. Comp. Physiol. Psycho/. 49: 38 l-39 I.
101,276-287
(1988)
Interocular Transfer of Extinction of Visual Pattern Discriminations in Split-Chiasm and Split-Brain Cats GIAN G. MASCETTI
AND JORGE R. ARRIAGADA’
Laboratorio de Neurobiologia, Facultad de Ciencias Biolbgicas, P. Universidad Catblica de Chile, Santiago, Chile Received September 29, 1987; revision received December 2,1987 The interocular transfer of the extinction of visual pattern discriminations was studied in cats with either section of optic chiasm (split-chiasm cats) or combined sections of chiasm and forebrain commissures (split-brain cats). Visual pattern discriminations were monocularly learned and their interocular transfer was assessed through the opposite eye. Then, learning was unilaterally extinguished and interocular transfer of extinction was tested on the other side. In split-chiasm cats, the total number of trials to extinction criterion (EC) was significantly lower with the second eye than with the first eye, indicating a successful interocular transfer. In split-brain cats, EC with the second eye was attained faster than with the first in some performances; it was similar with both eyes in other tasks, and with the second eye was higher than with the first in still other tasks. Statistical analysis applied to this group of split-brain cats pointed out that extinction performances with the two eyes were not significantly different. These findings suggest that interocular transfer of extinction was abolished in split-brain cats and that memory for extinction was unilaterally established in the absence of forebrain commissures. o 1988 Academic press, IIIC.
INTRODUCTION The processes of interhemispheric communication and transference of memory are of great interest in understanding brain function. Most studies of such phenomena have been performed on human subjects or experimental animals with partial or complete interruption of neural connections between both hemispheres. In cats, the midsagittal section of the optic chiasm Abbreviations: E-transference efficiency, EC-extinction criterion, S-saving, SB-split brain, SC-split-chiasm. ’ Supported by Grant 72/82 of Dire&on de Investigacibn, Universidad Cat&a de Chile (DIUC). We are grateful to Dr. Patricia Zapata for the critical reading of the manuscript. 276 0014-4886/88 $3.00 Copyright 0 1988 by Academic F’res, Inc. All rights of reproduction in any form reserved
INTEROCULAR
TRANSFER
277
leaves the neural output of each eye limited to the ipsilateral hemisphere. Consequently, interocular transfer becomes equivalent to interhemispheric transference of neural information ( 14). It is well known that the interocular transfer of visual pattern discriminations is successful in split-chiasm cats (17) and that it is abolished after the additional section of corpus callosum (18,23). Several studies have confirmed the important role of callosal commissure in the interhemispheric integration of visual learning (5, 7, 15, 19,20). The interocular transfer of visual pattern discrimination has been studied in relation to both acquisition (3, 14, 17) and reversal learning (16). However, several studies suggest that extinction would be mediated by a neural system distinct from that of acquisition and reversal learning (6, 10, 13, 24, 25). Therefore, in this work we studied the interocular transfer of extinction of visual pattern discriminations. For this purpose, visual discriminative behavior was learned in both hemispheres in split-chiasm and split-brain cats. Then, the animals were submitted to unilateral extinction and interocular transfer was assessed on the other side. METHODS Experiments were performed in two groups of adult cats: four with section of the optic chiasm (split-chiasm (SC) cats) and five with sections of the optic chiasm and corpus callosum (split-brain (SB) cats). Also, the hippocampal and habenular commissures laying in close apposition with corpus callosum were sectioned. These cats will be named SC 1 to SC4 and SB 1 to SB5, respectively. The operations were performed under Na pentobarbitone anesthesia (Nembutal, 36 mg/kg), with the aid of a stereomicroscope and with the use of surgical procedures described by Myers (17) for optic-chiasm and by Sperry (22) for corpus callosum. Experimental testing was done in a two-choice apparatus. After leaving the starting chamber (68 X 48 cm), the animal entered a decision chamber (75 X 48 cm) and faced two side-by-side plexiglass doors equally illuminated from behind and bearing the discriminanda (patterns made with black tape and equated for area). The decision chamber was divided in two alleys by a partition (last 45 cm) except at its beginning (initial 30 cm). Each alley led to one door and in order to change alleys, the animal had to return to the beginning of the decision chamber, turn around the partition, and enter the other alley. After crossing the door, the animal returned to the starting chamber through a returning alley ( 195 X 25 cm). The position of the two stimuli was changed according to a Gellerman sequence (9). A 40-trial daily session was carried out 5-6 days per week. The animals were food-deprived for 23 h before training sessions.
278
MASCETTI
AND ARRIAGADA
FIG. 1. Pairs of patterns used for discriminations, each pair having the same area. Patterns on the left were chosen as positive stimuli in acquisition, relearning, and Test Problem. A-Test Problem; B and C-problems B and C, respectively.
After surgery, all animals learned to work in the apparatus after being trained with both eyes in dark-light discrimination (one door lit and the other dark). Subsequently, pattern discriminations were learned with one eye (first eye) while the other one (second eye) was covered with a black plastic occlusive device. The animals were submitted to three discriminative tasks in the sequence corresponding to the correlative letters of the problem shown in Fig. 1. Problem A (test problem) was learned and interocularly transferred, but not extinguished. Problems B and C were learned and then extinguished. In the acquisition stage, a correct choice was scored when the animal pushed and opened the door with a positive stimulus, thus gaining access to a piece of bovine kidney. The other door was locked and colliding against it was the punishment for making an error. After an error, however, the cat was allowed to go through the correct door to have access to the food. In other words, a correction procedure was used at all stages. Final learning criterion was attained when 90% or more correct responses were obtained on 2 consecutive days. Then, 200 overtraining trials were given after which interocular transfer was tested with the second eye (the black plastic occlusive device was placed on the first eye) until the learning criterion was reattained. Reinforcement. A positive reinforcement (piece of kidney) was given at the end of each trial, being indispensable for the completion of this task. If this reward was not given for a few consecutive trials, the animal refused to work in the apparatus. When committing errors, cats collided against the locked door (sometimes twice or thrice) and they must then return to the beginning of the decision chamber, turn around the partition, and push to open the door with positive stimulus. The collision and the excessive delay in gaining access to the endtrial reward were considered negative reinforcement or punishment. Extinction. The extinction procedure consisted of removing the punishment, i.e., unlocking the two doors (free-choice condition) to eliminate the
INTEROCULAR
TRANSFER
279
significance of the discriminanda (4). The position of the patterns was still changed according to the Gellerman sequence. The cats trained monocularly (the occlusive device was placed on the second eye) stopped discriminating and progressively acquired a preference for the door on one side (position habit or side preference). The extinction criterion (EC) was attained when preference for one side was exhibited during 20 consecutive trials (4). If the EC was reached in the middle of a row of 10 trials, that row was completed. Then, the open eye was changed (the device was placed on the first eye) and training continued until the EC was reattained with the second eye. After bilateral extinction was reached, problem specificity of extinction was tested by submitting the animals to the Test Problem (40 trials with each eye) in free-choice conditions but with correct responses and errors being computed as during acquisition. Finally, the extinguished problem was monocularly relearned (relearning), alternating the open eye every 40 trials until the learning criterion was reattained. Analysis ofdata. Performances of the two eyes on each pattern’s discrimination were assessed on the basis of the following indexes: ( 1) Total number of trials before attaining learning or extinction criteria were included. For acquisition, the total number of errors was also computed. Once criteria were reached trials and errors were not included. Differences between both groups of animals were ascertained by the Wilcoxon matched pairs test. (2) Saving (S) was assessed according to the formula S = (total trials with the second eye/total trials with the first eye) X 100. An S value approaching 100 meant little or no saving with the second eye, while a value approaching 0 indicated saving. The saving values in the extinction of both groups of cats were compared by means of the Mann-Whitney test. The same test was employed where scores of acquisition and relearning were compared. Histology. After completion of the studies, completeness of commissurotomies and damage caused by surgery were ascertained by histological examination of the brains. The animals were perfused through the heart with 10% Formalin and the brains were serially sectioned with a freezing microtome to obtain IO-pm slices. A modified Nissl technique for staining cells and fibers was employed. RESULTS Split-chiasm cats. All these animals showed a positive interocular transfer of the acquisition (initial learning) of visual pattern discriminations. Table 1 shows the scores to criterion of both eyes. The total number of trials and errors were significantly lower with the second eye than with the first; in addition, S values were low, indicating a saving with the second eye. These results are in agreement with those reported by Myers ( 17, 18) Berlucchi et al. (3), and Lepore et al. ( 14).
280
MASCETTI
AND ARRIAGADA TABLE 1
Trials and Errors to Learning Criterion and Saving(S) in Split-Chiasm Cats Problem A
Problem B
Problem C
Cat
First eye
Second eye
S
First eye
Second eye
S
First eye
Second eye
S
SC1 SC2 SC3 SC4
320/Z 24019 1 360162 400187
80/15 4019 8019 4019
25 17 22.2 9
680/ 198 7601214 12901368 800/279
240/58 4801112 o/o o/o
35 63 0 0
1280/317 120122 400/8 1 200/60
680/131 4019 80/11 120129
53 33 20 60
Note. Trials and errors at criterion are not included.
Table 2 summarizes the scores of extinction of visual pattern discriminations in split-chiasm cats. In all animals, the EC with the second eye was reached with fewer trials than with the first, the difference being statistically significant (P < 0.005, Wilcoxon test). In addition, there was a significant saving with the second eye as indicated by the low S values. Figure 2A illustrates the interocular transfer of extinction of cat SC3. The sequence shown in the bar histogram and the scores indicates that the EC TABLE 2 Trials to Extinction Criterion (EC) and Saving(S) in Split-Chiasm Cats (SC) and Split-Brain Cats (SB) Problem B
Problem C
Cat
First eye
Second eye
S
First eye
Second eye
S
SC1 SC2 SC3 SC4 SBl SB2 SB3 SB4 SBS
800 320 260 160 290 440 130 120 90
140 70 0 0 90 50 150 150 240
17.5 21.8 0 0 31 11.3 115.3 125 266
480 100 320 130 280 200 470 290 100
50 50 20 70 160 370 20 50 240
10.5 50 6.2 53.8 57 185 4.2 17.2 240
Note. Trials to EC of the two eyes are significantly different in split-chiasm cats (P < 0.005, Wilcoxon test), but they are not significantly different in split-brain cat (P > 0.05, Wilcoxon test). Saving scores of split-chiasm cats are significantly different from those of split-brain cats (P c 0.05 Mann-Whitney test).
INTEROCULAR
TRANSFER
281
FIG. 2. A-interocular transfer of extinction of split-chiasm cat SC3 in problem C. Bar histograms, each bar corresponds to 10 consecutive trials. First, middle, and last groups of four bars with the first eye correspond to beginning, middle, and end of extinction with that eye (total trials to EC = 320). Extinction with the second eye is shown entirely (total trials to EC = 20). Ordinate, side preference for left or right door. B-discriminative performance in the Test Problem, showing errors with each eye (40 trials per eye). Trials and errors to learning criterion in relearning were: first eye, 80/24, and second eye, 80/2 1.
with the second eye was attained faster than with the first. Also, the same side preference was adopted for extinction by both eyes: the left door was selected with the first eye, and the same one was preferred by the second eye. The equivalence of side preference with both eyes was observed in all animals with the exception of cat SC2 in problem B. Statistical analysis showed that side preference of the second eye was not random and that it coincided with that of the first eye (P < 0.025, chi-square test). The learning of problem C was specifically extinguished because scores obtained in the test problem were above 90% of correct responses (Fig. 2B). Correct trials and errors were 38/2 and 38/2 for the first and second eye, respectively. All the split-chiasm cats showed a high level of discrimination when submitted to the test problem. Scores obtained in the relearning of the criterion for problems B and C are shown in Table 3. Relearning with the first eye was carried out with fewer trials and errors compared with the scores obtained in the acquisition with the same eye. Statistical analysis indicated that total trials and errors of both learning processes were different (P < 0.025, Mann-Whitney test, one tail). On the other hand, since the interocular transfer of acquisition was successful in these animals, scores of acquisition and relearning with the second eye were not statistically different (P > 0.10 Mann-Whitney test, one tail). Split-brain cats. The interocular transfer of acquisition of problems B and C was abolished in these animals. Table 4 shows the scores to criterion of
282
MASCETTI
AND ARRIAGADA TABLE 3
Trials and Errors to Learning Criterion following Extinction (Relearning) in Split-Chiasm (SC) and Split-Brain Cats (SB) Problem B Cat
First eye
SC1 SC2 SC3 SC4 SBl SB2 SB3 SB4 SB5
40112 240139 40114 4018 4015 4018 160/52 120136 80117
Problem C
Second eye
First eye
Second eye
4016
4017 4018 80124 o/o 4015 120136 4019
80/14 4018 80/2 1 120/21 80/11 80/13
16OJ37
120132 120/18
160/13 120/30 120129 o/o 120120 16OJ40
120135 4019
4oJ6
120128
Note. Trials and errors at criterion are not included.
both eyes. The total number of trials and errors with each eye were not different; in addition, S scoreswere high and in some casesthey surpassedthe value of 100. These resultsare in accordancewith those reported by Sperry et al. (23), Myers ( 18), Berlucchi et al. (3), and Mascetti et al. (16). The extinction behavior of split-brain cats is summarized in Table 2. In certain cases,the EC with the second eye was attained with fewer trials than with the first (SB1and SB2 in problem B and SB1, SB3, and SB4 in problem C); S scoreswere low, In other cases,there was no difference between both TABLE 4 Trials and Errors to Learning Criterion and Saving(S) in Split-Brain Cats Problem A
Problem B
Problem C
Cat
First eye
Second eye
S
First eye
Second eye
S
First eye
Second we
S
SBl SB2 SB3 SB4 SBS
11601467 400/l 14 240158 400/116 5601155
10801527 480/160 160146 5601252 7601204
93 120 67 140 136
280171 440/138 3201116 240154 880/343
240/66 640/160 4401164 280166 5601230
86 145 138 116.5 64
6401180 680/149 6001153 400/102 5201200
5201159 840/181 5601148 320/81 6401273
88 123.5 93 80 123
Note. Trials and errors at criterion are not included.
INTEROCULAR
TRANSFER
283
FIG. 3. A-interocular transfer of extinction of split-brain cat SB2 in problems C (upper) and B (lower). Bar histograms, each bar corresponds to 10 consecutive trials. First, middle, and last groups of four bars with each eye correspond to the beginning, middle, and end of extinction. Extinction with the second eye in problem B is shown entirely. Ordinate, side preference for left or right door. B-discriminative performance in the Test Problem, showing errors with each eye (40 trials per eye). Trials and errors to learning criterion were: problem C, first eye, 120/36, second eye, 80/l 3; problem B, first eye, 40/8, second eye, 120/20.
eyes (SB3 and SB4 in problem B) or even more trials were needed with the second eye (SB2 in problem C and SB5 in both problems); S scores were at or well above 100. However, the performance with both eyes for the entire group was not statistically different (P > 0.05, Wilcoxon test). Figure 3A shows the extinction behavior of cat SB2. The EC with the second eye was attained with more trials than with the first in problem C (upper part), but that level was reached with the second eye with fewer trials than with the first in problem B (lower part). An interesting finding was that side preference with each eye was opposite in 6 of the 10 interocular transfer testings of split-brain cats. Statistical analysis showed that side preference with the second eye was random and that it did not coincide with that of the first eye (P > 0.5, chi-square test). For example, Fig. 3A shows that side preference with both eyes was to the left in problem C; in problem B, with the first eye, side preference was to the left, while with the second one it was to the right. In this cat, scores for the Test Problem were above 90% of correct responses, indicating that extinction was problem-specific (Fig. 3B); correct responses and errors in the 40 trials were 39/l and 38/2 (upper part) for the first and second eye, respectively, in problem C, and were 38/2 and 39/l (lower part), respectively, in problem B. Both problems B and C were relearned with each eye with fewer trials and fewer errors committed than during acquisition (Table 3). Statistical analyses
284
MASCETTI
A
AND ARRIAGADA
B
SC
,.’
SB2
k
“pu.
FIG. 4. Selected coronal brain sections of one split-chiasm cat (SC3) and one split-brain cat (SB2). A-medial part of optic chiasms. B-caudal part of optic chiasm (SC3) and level of posterior commissure (SB2). Arrows indicate the sections. Cat SC3 had the forebrain commissures sectioned after completion of the present behavioral studies, because it was subsequently used in another series. Anterior commissure was left intact in SB cats.
indicated that total trials and errors of SB cats in both learning processes were significantly different: for the first eye, P < 0.005; for the second eye, P < 0.005 (Mann-Whitney test, one tail). Histological results. The optic chiasm was found completely sectioned in all cats. In addition, corpora callosa and the hippocampal and habenular commissures were also found totally sectioned in split-brain cats. Representative sections of the brain of cats SC3 and SB2 are shown in Fig. 4. The anterior commissure was not sectioned (Fig. 4, cat SB2). DISCUSSION The findings of this study indicated that the extinction of visual pattern discriminations was successfully transferred from one eye to the other in
INTEROCULAR
TRANSFER
285
split-chiasm cats. In fact, scores and statistical analyses showed that the EC with the second eye was reached faster than with the first. Here, we propose that the transference efficiency (E) for a given capability from one hemisphere to the other may be estimated as E = 100 - S (100 meaning perfect transfer). With the application of this measurement, the efficiency of the interhemispheric transfer of extinction of visual pattern discriminations varied between 46.2 and 100 in split-chiasm cats. In addition, the strategy that splitchiasm cats used for extinction (side preference) with both eyes was the same in each discriminative problem, suggesting that the processes underlying extinction would be related in both hemispheres. Opposite results were found after additional section of forebrain commissures (split-brain cats). With the application of the efficiency estimate to these cats in problem B and C performances, E varied between 95.8 and - 166, i.e., between nearly perfect transfer to a total absence of interocular transfer of extinction. In fact, in only one cat (SBl) out of five, trials to the EC with the second eye were fewer than those with the first. In the opposite extreme, in another cat (SB5) the number of trials to the EC with the second eye was more than twice that required with the first eye. The remaining three cats showed apparently more or less similar efficiency in one task but were less effective in the other one. As an entire group, trials to the EC in split-brain cats were not significantly different for both eyes (P > 0.05, Wilcoxon test). Therefore, we propose that the transference of extinction was absent in splitbrain cats. In other words, memory for extinction remained lateralized on the hemisphere connected with the first eye, although the time course of extinction with the second eye was faster in certain cases and slower in others. Two findings support this interpretation. First, statistical analysis applied to the group showed that scores with the second eye were not significantly different from those with the first eye. Statistical analysis also pointed out that S values of split-brain cats were different from those of split-chiasm cats where interocular transfer of extinction was successful (P < 0.05, MannWhitney test). Second, side preference with the second eye was random and it did not coincide with that of the first eye (P > 0.5, chi-square test). In fact, side preference of the two eyes was opposite in six tasks and the same in four. This finding would suggest that the processes underlying extinction were independent in both hemispheres. The findings of this study are similar to those previously reported for acquisition (3, 17, 18, 19) and reversal learning (16). In general, they confirm that the commissural system mediated the transference of learning and memory from one hemisphere to the other. On the other hand, they point out that forebrain commissures mediate the transference of extinction, although the neural mechanism and anatomical systems involved in extinction seem to be different from those involved in acquisition (6, 10, 13,24,25).
286
MASCETTI
AND ARRIAGADA
In chicks, Benowitz (2) reported that memory for extinction can be established only in the hemisphere contralateral to the eye trained. In other words, monocularly learned extinction was found not to be retrievable through the untrained eye. Instead, acquisition led down memory traces in both hemispheres and it could be retrievable through the untrained eye. On the basis that the two learning processes are mediated by distinct neural systems (6, 10, 13, 24, 25) the crucial point seems to be the presence of commissural connections in both systems. The absence of neocommissures in chicks (1) meant that extinction was not transmitted through the midline. The splitbrain cats of this study would show a similar condition since memory for extinction could be established only in one hemisphere. It is difficult to identify the commissures involved in the transference of extinction because multiple interhemispheric pathways that were intact in SC cats were cut in SB cats. However, it is well known that the corpus callosum plays an important role in the interhemispheric integration of visual learning (5,7, 15, 19,20) and it could be suggested that the commissure participates in the process of interocular transfer of extinction. The mechanisms underlying extinction have been the subject of great interest and many studies. Pavlov (2 1) and Hull (12) proposed that extinction could be caused by an internal buildup of inhibitory processes which eliminate previous responses. Guthrie (11) and Estes (8) attributed extinction to the acquisition of a competing response. Thus, when the animals stop responding in a certain way they may be learning alternative responses to those conditioned during original learning. In the present study, the discriminative response was replaced by side preference during extinction. Thus, we may argue that side preference was the alternative response causing the extinction of a visual pattern discriminative behavior. That response was successfully transferred from one hemisphere to the other in split-chiasm cats and it remained lateralized on the hemisphere connected with the first eye in splitbrain cats. We also argue that side preference was not an inspecific position habit because scores obtained for the Test Problem were at or above 90% of correct responses. In addition, side preference response was quickly eliminated in relearning. In this last stage, animals started discriminating again after a few trials and attained learning criterion with significantly fewer trials and errors than in the acquisition stage. REFERENCES 1. ARIENS-UPPERS, C. U., C. HUBER, AND E. C. CROSBY. 1936. The Comparative Anatomy of the Nervous System of Vertebrates, including Man. Macmillan, New York. 2. BENOWITZ, L. 1974. Conditions for the bilateral transfer of monocular learning in chicks. Brain Res. 65: 203-2 13. 3. BERLUCCHI, G., E. BUCHTEL, C. A. MARZI, G. G. MASCETTI, AND A. SIMONI. 1978. Effect of experience on interocular transfer of pattern discriminations in split-chiasm and splitbrain in cats. J. Comp. Physiol. Psychol. 92: 532-543.
INTEROCULAR
TRANSFER
287
4. BERLUCCHI, G., AND C. A. MARZI. 1970. Veridical interocular transfer of lateral mirrorimage discriminations in split-chiasm cats. J. Comp. Physiol. Psychol. 72: l-7. 5. BERLUCCHI, G., AND C. A. MARZI. 1982. Interocular and interhemispheric transfer of visual discriminations in the cat. In D. J. INGLE, M. A. GOODALE, AND R. J. W. MANS. FIELD, Eds., Analysis of Visual Behavior. MIT Press, Cambridge, MA. 6. DOUGLAS, R. J. 1967. The hippocampus and behavior. Psychol. BUN. 67: 416-442. 7. DOWNER, J. L., DE C. 1958. Role of corpus callosum in transfer of training in Macacca Mulatta. Fed. Proc. 17: 37. 8. ESTES, W. K. 1959. The statistical approach to learning theory. In S. KOCH, Ed. Psychology A study ofa Science, Vol. 2. McGraw-Hill, New York. 9. GELLERMAN, L. V. 1933. Chance orders of alternating stimuli in visual discrimination experiments. .I. Genet. Psychol. 42: 206-208. 10. GODDARD, G. V. 1964. Functions of the amydgdala. Psychol. Bull. 62: 89-109. 11. GUTHRIE, E. R. 1952. The Psychology oflearning. Harper & Row, New York. 12. HULL, C. L. 1943. Principles ofBehavior. Yale Univ. Press, New Haven, CT. 13. mMBLE, D. P. f968. Hippocampus and internal inhibition. Psychoi. But/. 70: 285-295. 14. LEPORE, F., J. PHANEUF, A. SAMSON, AND J. P. GUILLEMOT. 1982. Interhemispheric transfer of visual pattern discriminations: Evidence for a bilateral storage of the engram. Behav. Brain Res. 5: 359-374. 15. LEVINSON, D. M., AND C. H. SHERIDAN. 1969. Monocular acquisition and interocular transfer of two types of pattern discriminations in hooded rats. J. Comp. Physiol. Psycho/. 67: 486-492. 16. MASCETTI, G. G., C. M. WITTVER, F. A. ROJAS, AND J. R. ARRIAGADA. 198 1. Interocular transfer of reversal learning in split-chiasm and split-brain cats. Res. Commun. Psycho/. Psychiatry Behav. 8: 243-255. 17. MYERS, R. E. 1955. Interocular transfer of pattern discriminations in cats following section of crossed optic fibers. J. Camp. Physiol. Psychol. 48: 470-473. 18. MYERS, R. E. 1956. Function of corpus callosum in interocular transfer. Brain 79: 350363. 19. MYERS, R. R. 1962. Transmission of visual information within and between the hemispheres: A behavioral study. Pages 5 l-74 in V. B. MOUNTCASTLE, Ed., Interhemispheric Relations and Cerebral Dominance. Johns Hopkins Press, Baltimore. 20. MYERS, R. E. 1965. The neocortical commissures and interhemispheric transmission of information. Pages l- I7 in E. C. E-~TLINGER, Ed., Functions ofthe Corpus Cahosum. Little, Brown, Boston. 2 1. PAVLOV, I. P. 1927. Conditioned Reflexes. Translated by G. V. ANREP. Oxford Univ. Press, London. 22. SPERRY, R. W. 1968. Mental unity following surgical disconnection of the cerebral hemispheres. Harvey Lect. 62: 293-323. 23. SPERRY,R. W., J. S. STAMM, AND N. MINER. 1956. Relearning tests for interocular transfer following division of optic chiasm and corpus callosum. J. Comp. Physiol. Psychol. 49: 529-533. 24. URSIN, H. 1965. Effect of amygdaloid lesions on avoidance behavior and visual discriminations in cats. Exp. Neurol. 11: 298-3 17. 25. WEISKRANTZ, L. 1956. Behavioral changes associated with ablations of the amygdaloid complex in monkeys. J. Comp. Physiol. Psycho/. 49: 38 l-39 I.