Physiology & Behavior, Vol. 20, pp. 331-338. Pergamon Press and Brain Research Pubi., 19"/8. Printed in the U.S.A.
Successful Interocular Transfer of Visual Pattern Discriminations in Split-Chiasm Cats With Section of the Intertectal and Posterior Commissures I G. BERLUCCHI, H. A. BUCHTEL 2 AND F. LEPORE a
Istituto di Fisiologia dell'UniversiM di Pisa e Laboratorio di Neurofisiologia del C N . R . di Pisa (Received 10 November 1977) BERLUCCHI, G., H. A. BUCHTEL AND F. LEPORE. Successful interocular transfer of visual pattern discriminations in split-chiasm cats with section of the intertectal and posterior commissures. PHYSIOL. BEHAV. 20(3) 331-338, 1978. Interocular transfer of visual pattern discriminations is absent in split-chiasm cats with a section of cortical commissures and one might conclude that the exchange of visual information necessary for interhemispheric transfer of such discriminations is carded out exclusively at a cortical level. However, section of the cortical commissures influences the activity of the superior colliculus, and the absence of interhemispheric transfer of pattern discriminations following commissurotomy may reflect cortical as well as subcortical modifications. In an attempt to test this poss~llity sections of the posterior, intertectal and habenular commissures were made in split chiasm cats and interocular transfer was tested and found to be intact. Thus these pathways for across-the-midline transfer of information are not essential in interocular transfer. Tectal commissures
Interocular transfer
Split-chiasm cats
Pattern discrimination
Cats
superior coUiculus; and the posterior commissure which contains crossed tecto-fugal fibers ascending from one superior coUiculus to the contralateral thalamus [14]. In the present experiment we have investigated the possibility of an involvement of these across-the-midline subcortical connections in the interhemispheric transfer of visual pattern discriminations. For this purpose we have tested interocular transfer in split-chiasm cats with an additional section of the intertectal and posterior commissures. For comparison, we have used pattern discriminations which could be successfully transferred between the eyes of otherwise intact split-chiasm cats, but not of split-chiasm cats with a section of the cortical commissures (split-brain cats).
IT has been shown that lesions of the superior colliculus impair the learning of visual pattern discriminations in the cat [6], but it is not known if this subcortical visual center is also involved in the interhemispheric transfer of such discriminations. The critical role played by the corpus callosum in interocular transfer of pattern discriminations in split-chiasm cats [12, 13, 21] suggests that the interhemispheric communication necessary for such a transfer is basically a cortical process. However, the ablation of cortical areas receiving visual information from the tectothalamic system produces deficits in visual learning which are similar to those resulting from lesions of the superior colliculi [23]. Thus, the normal learning of visual pattern discriminations appears to require both the superior colliculus and the cortical areas receiving visual information from it. By analogy, it can be suggested that the interhemispheric transfer of pattern discriminations depends on the integrity of both corpus callosum and lower across-the-midline connections conveying visual information to and from the superior colliculi. Among these connections are the commissure of the superior colliculi which, in addition to true commissural fibers [8], contains crossed cortico-tectal projections from the cortical areas 17, 18 and 19 [ 16] and from the lateral suprasylvian area [2] to the opposite
METHOD
Surgical and Histological Pro cedures All surgical procedures were performed under Nembutal anesthesia ( 3 5 - 4 0 mg/kg of body weight, IP). Three adult cats (Sub 1, Sub 3, Sub 5) first underwent a midsagittal section of t h e optic chiasm through the transbuccal approach described by Myers [ 11 ]. In one cat (Sub 5) the anterior commissure was visualized after sectioning the
1Research supported in part by U.S.P.H.S. grant 2R01 EY005711 and by Contratto 70.01687/18 of the Consiglio Nazionale delle Ricerche, Roma. 2Present address: Istituto di Fisiologia Umana, Universit~ di Parma, Parma, Italy. 3Present address: Institut de Psychologic, Universit6 de Montreal, Montreal, Canada. 331
332 optic chiasm and cut. A Zeiss operating stereomicroscope was used for the finer steps in the surgery. The second operation was carried out several days later. It involved the exposure of the quadrigeminal plate and the habenular and posterior commissures after making a large flap in the cranial vault overlying the occipital lobes, removing the left half of the bony tentorium, lifting by gentle retraction the posterior pole of the left hemisphere, and cutting the dura at the bottom of the fissure between cerebrum and cerebellum. Under continuous microscopic control the posterior end of the intertectat commissure was separated from the anterior lobe of the cerebellum, thus opening the fourth ventricle, and the quadrigeminal plate was sectioned along the midline down to the ventricular space by means of a sharpened aspirator tip. Therefore the section included the upper part of the periventricular gray, which may contain commissural fibers of the superior colliculi [18]. For exposing the posterior commissure, the pineal gland was displaced to one side of the midline; both the habenular commissure, which rests on the upper side of the pineal gland, and the posterior commissure were pinched in two with a jeweler's forceps. Bleeding was controlled by continuous aspiration and by the application of small pieces of a fibrin sponge. The defect in the dura was then covered with Gelfilm, the bone flap reapposed and the cranial muscles and skin sutured. At the end of the experiment the animals were anesthetized with Nembutal and perfused through the aorta with saline followed by Formalin. The brain was removed, dehydrated, embedded in paraffin and cut in frontal section 15 ~ thick. Every other section was stained with either the Nissl or the Weil methods, except for the sections containing the optic chiasm which were all kept and stained.
Training Apparatus and Testing Pro cedure The training apparatus has been described in detail elsewhere [3, 4, 6]. Briefly, the discriminanda were presented on two side-by-side hinged doors which could be illuminated from behind. In order to obtain a reward consisting of a small piece of beef kidney, the cat, which had been food deprived for about 23-1/2 hr, had to push open the door displaying the positive stimulus. 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. Following the attainment of the reward the animal was placed again in the apparatus and the next trial began immediately. A daily session consisted of 40 trials, 20 of which were run with the positive stimulus on the right door and 20 with the positive stimulus on the left door. The two stimulus conditions were alternated in a quasi-random order according to a modified Gellermann [9] sequence. Before any surgical procedures all cats were trained on a simple light-dark discrimination. The locked door was illuminated from behind (mean luminance 39 cd m-~ ) while the unlocked door received no direct illumination (mean luminance due to reflected light: 0.3 cd m -2). Training was first binocular, until the animal performed two consecutive sessions with less than 5 errors in each session, and then monocular with either eye. A black scleral occluder was placed on one eye and as many sessions were run as were necessary to reattain the same learning criterion with either eye. After each of the two operations the animals were allowed to recover for at least two weeks and then retested on the light-dark discrimina-
BERLUCCHI, BUCHTEI. AND LEPORF tion both binocularly and monocularly with either eye This allowed us to make sure that they could perform m the discrimination apparatus using each eye. Following tilt' retesting on the light-dark discrimination after the second operation, the cats were trained monocularly on pattern discriminations. The two doors were equally illuminated from behind (mean luminance 39 cd m -2 ) and a patterned stimulus made of black paper or tape was displayed on the center of each door. The stimuli concurrently shown on the two doors were equated for area but differed in form or orientation (see Fig. 1). For most discriminations learning with the first eye proceeded until the animal performed two consecutive sessions of forty trials with less than five errors in each session, following which there were five overtrainin'g sessions with the same eye. Interocular transfer was then tested by putting the occluder on the eye used for learning and by testing until the same learning criterion was reattained with the other eye. A less stringent criterion was used on one discrimination with cat Sub 1 (cross-circle) and on two discriminations with cat Sub 3 (upright versus inverted triangle and reversal learning of the same discrimination). On these discriminations training with the first eye proceeded until reaching a criterion of 18 correct responses out of 20 trials. The other eye was then trained to the same criterion, after which the first eye was brought to the more difficult criterion (two sessions with 90% or more correct res!~onses), followed by training to the same criterion with the second eye. Thus, on each of these discriminations interocular transfer was tested at two different levels of competence with the first eye. Results from tests of interocular transfer on the same discriminations and using the same apparatus were available from previous experiments [3,5] on several split-chiasm cats with no other neural damage and split-chiasm cats with a section of the corpus callosum, hippocampal commissure and anterior commissure (split-brain cats). On these tests the more difficult learning criterion was consistently adopted and the first eye was overtrained for five sessions before transfer to the other eye. RESULTS
Histology The optic chiasm was found to be completely sectioned in all cats. The habenular, posterior and intertectal commissures were also totally sectioned, as shown i n Fig, 2. The section of the anterior commissure was complete in cat Sub 5. The completeness of the sections of the optic chiasm and forebrain commissure was histologically verified in the control split-chiasm and split-brain cats. In the cats with tectal splittings, some damage to the tissue near the midline in both tectum and pretectum was consistently apparent, with no obvious asymmetry between the two sides.
Behavior After the tectal splitting all cats showed a striking neglect of the upper visual fields accompanied by a severe limitation of upwards eye movements. The head was held in a peculiar posture of moderate hyperextension, perhaps to compensate for the deficit in ocular movements. These disturbances were permanent and were similar to those described in monkeys with section of the posterior commissure [15]. Other symptoms such as forced circling, head
lay
SPLIT-CHIASM INTEROCULAR TRANSFER
333 and split-brain cats on the other hand. It is obvious that split-chiasm cats with tectal splittings and otherwise intact split-chiasm cats showed a similar capacity for interocular transfer, whereas split-brain cats were generally incapable of transferring discriminations from one e y e to the other. In the cats with tectal splittings, interocular transfer was successful even when tested after the attainment of easy criteria of learning with the first eye (Sub 1, Sub 3) and on a problem of reversal learning (Sub 3). DISCUSSION
2
3
1
0
FIG. 1. Pairs of patterns used for discrimination. The size of the stimuli has been reduced to 1/3 of the original. tilting and stepping gait were seen for only a few days following the operation. The permanent deficits had no apparent effect on the performance in the discrimination apparatus. Cat Sub 5 was very slow in acquiring the discriminations; its learning deficit, which was more pronounced when using the left eye, may be related to the extent of incidental damage to superior colliculus and pretectum [6]. The following learning scores were adopted: ( a ) n u m b e r of errors committed before reaching the learning criterion and ( b ) n u m b e r of trials necessary to perform the first sequence of correct responses, allowing for one error, with a probability of chance occurrence equal to or lower than 0.01 (significant run: see [7,19]). Interocular transfer was measured by using the formula of Murdock [10] : Score for the first eye - score for the second eye x 100 sum of the two scores In addition to the two learning scores above we also used a score for initial performance (number of errors in first 40 trials). The monocular learning curves for each discrimination for each of the three cats with tectal splitting are shown in Figs. 3, 4 and 5. Table 1 allows a comparison between the interocular transfer scores of the cats with tectal splittings on one hand and the corresponding scores of split-chiasm
The findings show that the posterior, habenular and intertectal commissures are not necessary for the interhemispheric transfer of visual pattern discriminations. Since split-chiasm cats with a section of these commissures showed an interocular transfer of pattern discriminations as successful as that of otherwise intact split-chiasm cats, it follows that the interhemispheric exchange of information necessary for the transfer must take place through other commissures. Transfer was in fact absent in split-chiasm cats with an additional section of the forebrain commissures, confirming the classical results of Myers [12] and Sperry et al. [21]. The fact that the section of the anterior commissure in cat Sub 5 had also no apparent effect on interocular transfer suggests that in the split-chiasm cat the corpus callosum, and possibly only its posterior part (see [13]), is the exclusive route subserving the interhemispheric transfer of visual pattern discriminations. The results do not rule out the possibility that the intertectal and other subcortical commissures may have a role in the interhemispheric transfer of pattern discriminations under conditions differing from those of the present experiment. Thus, it has been reported that split-chiasm monkeys [24] and cats [3] with a section of the forebrain commissures may show some residual capacity for interocular transfer of pattern discriminations when commissurotomy is made in stages or is preceded by practice with tasks of interocular transfer. In a split-brain monkey with an additional section of the intertectal commissure such residual capacity for transfer was not observed [24]. However, the transfer effects observed following forebrain commissurotomy were very limited, and their significance for the mechanisms of interhemispheric integration of visual information is still to be assessed. The question remains open as to the importance of across-the-midline connections from and to the superior colliculus for visually guided behavior in the cat. Voneida [25] has implicated the commissure of the superior coUiculi in the performance of simple visuomotor responses requiring neural activity on both sides of the midline. However, Robinson and Voneida [17] have found that this commissure does not significantly facilitate the central cross integration of visual inputs separately presented to the two eyes. The work of Sprague [22] and that of Sherman [20] suggests that the mechanisms of visual orientation and localization may involve a reciprocal inhibition between the superior colliculi, an inhibition mediated by the intertectal connections. On the basis of anatomical findings pointing to a limitation of the commissural connections to the deep layers of the superior colliculi, Edwards [8] has argued for an involvement of these connections in eye and head movements, whether these movements are visually guided or not. The intertectal connections also contain crossed projections from the visual cortical areas 17, 18 and 19 of
334
BERLUCCHI, BUCHTEI. AND L[ PORf
SUB 1
SUB 3
SUB 5
A 6.5
A 5
A 3.5
A 2.5
A 1
FIG. 2. Coronal sections of the brain stem showing the splitting of the habenular, posterior and intertectal commissures (Weil method). For each of the three cats the numbers to the left indicate the approximate AP Horsley-Clarke level. Note that the transection includes the upper part of the periventricular gray.
one side to the superior colliculus of the other side [ 16]. Since the superior colliculus gives rise to ascending projections which reach the cortex after a relay in the thalamus [14,23], it has been pointed out that the crossed corticotectal projection may be used for the indirect transmission of visual information between the cortices of the t w o sides even after section of the cortical commissures [16].
However, the present results make it clear that this indirect pathway for the interhemispheric transmission of visual information is unessential for interocular transfer o f pattern discriminations in split-chiasm cats, since the crossed cortico-tectal connection was obviously interrupted by our intertectal sections. While indicating that the corpus callosum is the crucial
1
22 (21--26) 16.5 (13-26)
Split chiasm (N = 4)
Split brain (N = 6)
22 (17-27) 21 (16-25)
Split chiasm (N = 3)
Split brain (N = 5)
19 (18--24) 21 (19--26)
Split chiasm (N = 4)
Split brain (N = 5)
23 (15-33)
5.5 (4--12)
17 12
25 (17-29)
10 (9-14)
8 19
22 (20-24)
-5 (-12-23)
58 (23--66)
6 31
-14 (-24-11)
31 (22-46)
45 22
(-30-4)
-11.5
37 (23--64)
33
33 3 26
score
Transfer
240 (110--242)
196.5 (164-718)
237 1837
143 (26-410)
149 (104-385)
178 560
(109-364)
178.5
270.5 (145--583)
1028
98 351 610
First eye
98 (62--255)
10 (4-25)
44 78
227 (70-644)
(0-69)
11
24 241
(74-361)
177
19 (0-469)
27
24 124 142
Second eye
Trials to first significant run
6 (-3-69)
94 (89--96)
69 92
-22 (-72-22)
81 (70-100)
76 40
8.5 (-41-20)
80 (10--100)
95
61 48 62
score
Transfer
88 (58--139)
141 (64--245)
90 825
60 (23-229)
90 (58-215)
96 446
78.5 (51-171)
143 (72--364)
610
36 148 244
First eye
46 (25-150)
16 (4--46)
29 43
87 (39-341)
27 (9-66)
15 319
81.5 (50-153)
26 (5--217)
108
16 63 55
Second eye
Errors to final criterion
12 (-31--56)
78 (57--91)
51 90
-20 (-58-30)
54 (53--73)
73 17
3.5 (-44-8)
63.5 (25--88)
70
38 40 63
score
Transfer
The initial performance score is the n u m b e r of errors committed during the initial 40 trials. A significant run is the first sequence of correct responses, including at most one error, with a chance probability o f occurrence equal to or less than 0.01. The difficult learning criterion required the performance of at least 36 correct responses in each of two consecutive 40 trial sessions. For each score of the split-chiasm and split-brain cats the table indicates the median value and, in parentheses, the range. For the easy learning criterion (18 correct responses out of 20 trials) no data from split-chiasm and split-brain cats were available. It is clear that in the cats with tectal splitting interocular transfer was successful also on these tests with a reduced training with the first eye, although there the transfer was not immediate. The low transfer scores for cat Sub 5 or Problem I-- are best attributed to a reduction of the visual ability of the eye receiving the transfer, as indicated by the p o o r performance o f the animal when using that eye for initial learning. In the cats with tectal splittings, an asterisk indicates problems learned with the right eye, and a dagger indicates problems learned to the easier criterion (18 correct responses out o f 20 trials).
19 23
Sub l * t Sub 5
Problem +0
21 30
Sub 1 Sub 5*
Problem l--
10
20 9.5 (5--16)
9 17 20
18 18 34
Second eye
Sub 1" Sub 3 t Sub 3 * t ~eversed problem) Sub 5
Problem AV
First eye
Initial performance
SCORES FOR LEARNING AND INTEROCULAR T R A N S F E R IN SPL1T-CHIASM CATS, SPLIT-CHIASM CATS WITH TECTAL SPLITTINGS AND SPLIT-BRAIN CATS
TABLE
ta~
Z
r~ >
0
~3
I
B E R L U C C H I , B U C H T E L AND L[!POI~,t
336
100
!00
,9 ~
so
I
~ ,t~,~
80
d
-~"
~
?
'
S
3 o
8:
60
60
40
4O
Successful Interocular Transfer of Visual Pattern Discriminations in Split-Chiasm Cats With Section of the Intertectal and Posterior Commissures I G. BERLUCCHI, H. A. BUCHTEL 2 AND F. LEPORE a
Istituto di Fisiologia dell'UniversiM di Pisa e Laboratorio di Neurofisiologia del C N . R . di Pisa (Received 10 November 1977) BERLUCCHI, G., H. A. BUCHTEL AND F. LEPORE. Successful interocular transfer of visual pattern discriminations in split-chiasm cats with section of the intertectal and posterior commissures. PHYSIOL. BEHAV. 20(3) 331-338, 1978. Interocular transfer of visual pattern discriminations is absent in split-chiasm cats with a section of cortical commissures and one might conclude that the exchange of visual information necessary for interhemispheric transfer of such discriminations is carded out exclusively at a cortical level. However, section of the cortical commissures influences the activity of the superior colliculus, and the absence of interhemispheric transfer of pattern discriminations following commissurotomy may reflect cortical as well as subcortical modifications. In an attempt to test this poss~llity sections of the posterior, intertectal and habenular commissures were made in split chiasm cats and interocular transfer was tested and found to be intact. Thus these pathways for across-the-midline transfer of information are not essential in interocular transfer. Tectal commissures
Interocular transfer
Split-chiasm cats
Pattern discrimination
Cats
superior coUiculus; and the posterior commissure which contains crossed tecto-fugal fibers ascending from one superior coUiculus to the contralateral thalamus [14]. In the present experiment we have investigated the possibility of an involvement of these across-the-midline subcortical connections in the interhemispheric transfer of visual pattern discriminations. For this purpose we have tested interocular transfer in split-chiasm cats with an additional section of the intertectal and posterior commissures. For comparison, we have used pattern discriminations which could be successfully transferred between the eyes of otherwise intact split-chiasm cats, but not of split-chiasm cats with a section of the cortical commissures (split-brain cats).
IT has been shown that lesions of the superior colliculus impair the learning of visual pattern discriminations in the cat [6], but it is not known if this subcortical visual center is also involved in the interhemispheric transfer of such discriminations. The critical role played by the corpus callosum in interocular transfer of pattern discriminations in split-chiasm cats [12, 13, 21] suggests that the interhemispheric communication necessary for such a transfer is basically a cortical process. However, the ablation of cortical areas receiving visual information from the tectothalamic system produces deficits in visual learning which are similar to those resulting from lesions of the superior colliculi [23]. Thus, the normal learning of visual pattern discriminations appears to require both the superior colliculus and the cortical areas receiving visual information from it. By analogy, it can be suggested that the interhemispheric transfer of pattern discriminations depends on the integrity of both corpus callosum and lower across-the-midline connections conveying visual information to and from the superior colliculi. Among these connections are the commissure of the superior colliculi which, in addition to true commissural fibers [8], contains crossed cortico-tectal projections from the cortical areas 17, 18 and 19 [ 16] and from the lateral suprasylvian area [2] to the opposite
METHOD
Surgical and Histological Pro cedures All surgical procedures were performed under Nembutal anesthesia ( 3 5 - 4 0 mg/kg of body weight, IP). Three adult cats (Sub 1, Sub 3, Sub 5) first underwent a midsagittal section of t h e optic chiasm through the transbuccal approach described by Myers [ 11 ]. In one cat (Sub 5) the anterior commissure was visualized after sectioning the
1Research supported in part by U.S.P.H.S. grant 2R01 EY005711 and by Contratto 70.01687/18 of the Consiglio Nazionale delle Ricerche, Roma. 2Present address: Istituto di Fisiologia Umana, Universit~ di Parma, Parma, Italy. 3Present address: Institut de Psychologic, Universit6 de Montreal, Montreal, Canada. 331
332 optic chiasm and cut. A Zeiss operating stereomicroscope was used for the finer steps in the surgery. The second operation was carried out several days later. It involved the exposure of the quadrigeminal plate and the habenular and posterior commissures after making a large flap in the cranial vault overlying the occipital lobes, removing the left half of the bony tentorium, lifting by gentle retraction the posterior pole of the left hemisphere, and cutting the dura at the bottom of the fissure between cerebrum and cerebellum. Under continuous microscopic control the posterior end of the intertectat commissure was separated from the anterior lobe of the cerebellum, thus opening the fourth ventricle, and the quadrigeminal plate was sectioned along the midline down to the ventricular space by means of a sharpened aspirator tip. Therefore the section included the upper part of the periventricular gray, which may contain commissural fibers of the superior colliculi [18]. For exposing the posterior commissure, the pineal gland was displaced to one side of the midline; both the habenular commissure, which rests on the upper side of the pineal gland, and the posterior commissure were pinched in two with a jeweler's forceps. Bleeding was controlled by continuous aspiration and by the application of small pieces of a fibrin sponge. The defect in the dura was then covered with Gelfilm, the bone flap reapposed and the cranial muscles and skin sutured. At the end of the experiment the animals were anesthetized with Nembutal and perfused through the aorta with saline followed by Formalin. The brain was removed, dehydrated, embedded in paraffin and cut in frontal section 15 ~ thick. Every other section was stained with either the Nissl or the Weil methods, except for the sections containing the optic chiasm which were all kept and stained.
Training Apparatus and Testing Pro cedure The training apparatus has been described in detail elsewhere [3, 4, 6]. Briefly, the discriminanda were presented on two side-by-side hinged doors which could be illuminated from behind. In order to obtain a reward consisting of a small piece of beef kidney, the cat, which had been food deprived for about 23-1/2 hr, had to push open the door displaying the positive stimulus. 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. Following the attainment of the reward the animal was placed again in the apparatus and the next trial began immediately. A daily session consisted of 40 trials, 20 of which were run with the positive stimulus on the right door and 20 with the positive stimulus on the left door. The two stimulus conditions were alternated in a quasi-random order according to a modified Gellermann [9] sequence. Before any surgical procedures all cats were trained on a simple light-dark discrimination. The locked door was illuminated from behind (mean luminance 39 cd m-~ ) while the unlocked door received no direct illumination (mean luminance due to reflected light: 0.3 cd m -2). Training was first binocular, until the animal performed two consecutive sessions with less than 5 errors in each session, and then monocular with either eye. A black scleral occluder was placed on one eye and as many sessions were run as were necessary to reattain the same learning criterion with either eye. After each of the two operations the animals were allowed to recover for at least two weeks and then retested on the light-dark discrimina-
BERLUCCHI, BUCHTEI. AND LEPORF tion both binocularly and monocularly with either eye This allowed us to make sure that they could perform m the discrimination apparatus using each eye. Following tilt' retesting on the light-dark discrimination after the second operation, the cats were trained monocularly on pattern discriminations. The two doors were equally illuminated from behind (mean luminance 39 cd m -2 ) and a patterned stimulus made of black paper or tape was displayed on the center of each door. The stimuli concurrently shown on the two doors were equated for area but differed in form or orientation (see Fig. 1). For most discriminations learning with the first eye proceeded until the animal performed two consecutive sessions of forty trials with less than five errors in each session, following which there were five overtrainin'g sessions with the same eye. Interocular transfer was then tested by putting the occluder on the eye used for learning and by testing until the same learning criterion was reattained with the other eye. A less stringent criterion was used on one discrimination with cat Sub 1 (cross-circle) and on two discriminations with cat Sub 3 (upright versus inverted triangle and reversal learning of the same discrimination). On these discriminations training with the first eye proceeded until reaching a criterion of 18 correct responses out of 20 trials. The other eye was then trained to the same criterion, after which the first eye was brought to the more difficult criterion (two sessions with 90% or more correct res!~onses), followed by training to the same criterion with the second eye. Thus, on each of these discriminations interocular transfer was tested at two different levels of competence with the first eye. Results from tests of interocular transfer on the same discriminations and using the same apparatus were available from previous experiments [3,5] on several split-chiasm cats with no other neural damage and split-chiasm cats with a section of the corpus callosum, hippocampal commissure and anterior commissure (split-brain cats). On these tests the more difficult learning criterion was consistently adopted and the first eye was overtrained for five sessions before transfer to the other eye. RESULTS
Histology The optic chiasm was found to be completely sectioned in all cats. The habenular, posterior and intertectal commissures were also totally sectioned, as shown i n Fig, 2. The section of the anterior commissure was complete in cat Sub 5. The completeness of the sections of the optic chiasm and forebrain commissure was histologically verified in the control split-chiasm and split-brain cats. In the cats with tectal splittings, some damage to the tissue near the midline in both tectum and pretectum was consistently apparent, with no obvious asymmetry between the two sides.
Behavior After the tectal splitting all cats showed a striking neglect of the upper visual fields accompanied by a severe limitation of upwards eye movements. The head was held in a peculiar posture of moderate hyperextension, perhaps to compensate for the deficit in ocular movements. These disturbances were permanent and were similar to those described in monkeys with section of the posterior commissure [15]. Other symptoms such as forced circling, head
lay
SPLIT-CHIASM INTEROCULAR TRANSFER
333 and split-brain cats on the other hand. It is obvious that split-chiasm cats with tectal splittings and otherwise intact split-chiasm cats showed a similar capacity for interocular transfer, whereas split-brain cats were generally incapable of transferring discriminations from one e y e to the other. In the cats with tectal splittings, interocular transfer was successful even when tested after the attainment of easy criteria of learning with the first eye (Sub 1, Sub 3) and on a problem of reversal learning (Sub 3). DISCUSSION
2
3
1
0
FIG. 1. Pairs of patterns used for discrimination. The size of the stimuli has been reduced to 1/3 of the original. tilting and stepping gait were seen for only a few days following the operation. The permanent deficits had no apparent effect on the performance in the discrimination apparatus. Cat Sub 5 was very slow in acquiring the discriminations; its learning deficit, which was more pronounced when using the left eye, may be related to the extent of incidental damage to superior colliculus and pretectum [6]. The following learning scores were adopted: ( a ) n u m b e r of errors committed before reaching the learning criterion and ( b ) n u m b e r of trials necessary to perform the first sequence of correct responses, allowing for one error, with a probability of chance occurrence equal to or lower than 0.01 (significant run: see [7,19]). Interocular transfer was measured by using the formula of Murdock [10] : Score for the first eye - score for the second eye x 100 sum of the two scores In addition to the two learning scores above we also used a score for initial performance (number of errors in first 40 trials). The monocular learning curves for each discrimination for each of the three cats with tectal splitting are shown in Figs. 3, 4 and 5. Table 1 allows a comparison between the interocular transfer scores of the cats with tectal splittings on one hand and the corresponding scores of split-chiasm
The findings show that the posterior, habenular and intertectal commissures are not necessary for the interhemispheric transfer of visual pattern discriminations. Since split-chiasm cats with a section of these commissures showed an interocular transfer of pattern discriminations as successful as that of otherwise intact split-chiasm cats, it follows that the interhemispheric exchange of information necessary for the transfer must take place through other commissures. Transfer was in fact absent in split-chiasm cats with an additional section of the forebrain commissures, confirming the classical results of Myers [12] and Sperry et al. [21]. The fact that the section of the anterior commissure in cat Sub 5 had also no apparent effect on interocular transfer suggests that in the split-chiasm cat the corpus callosum, and possibly only its posterior part (see [13]), is the exclusive route subserving the interhemispheric transfer of visual pattern discriminations. The results do not rule out the possibility that the intertectal and other subcortical commissures may have a role in the interhemispheric transfer of pattern discriminations under conditions differing from those of the present experiment. Thus, it has been reported that split-chiasm monkeys [24] and cats [3] with a section of the forebrain commissures may show some residual capacity for interocular transfer of pattern discriminations when commissurotomy is made in stages or is preceded by practice with tasks of interocular transfer. In a split-brain monkey with an additional section of the intertectal commissure such residual capacity for transfer was not observed [24]. However, the transfer effects observed following forebrain commissurotomy were very limited, and their significance for the mechanisms of interhemispheric integration of visual information is still to be assessed. The question remains open as to the importance of across-the-midline connections from and to the superior colliculus for visually guided behavior in the cat. Voneida [25] has implicated the commissure of the superior coUiculi in the performance of simple visuomotor responses requiring neural activity on both sides of the midline. However, Robinson and Voneida [17] have found that this commissure does not significantly facilitate the central cross integration of visual inputs separately presented to the two eyes. The work of Sprague [22] and that of Sherman [20] suggests that the mechanisms of visual orientation and localization may involve a reciprocal inhibition between the superior colliculi, an inhibition mediated by the intertectal connections. On the basis of anatomical findings pointing to a limitation of the commissural connections to the deep layers of the superior colliculi, Edwards [8] has argued for an involvement of these connections in eye and head movements, whether these movements are visually guided or not. The intertectal connections also contain crossed projections from the visual cortical areas 17, 18 and 19 of
334
BERLUCCHI, BUCHTEI. AND L[ PORf
SUB 1
SUB 3
SUB 5
A 6.5
A 5
A 3.5
A 2.5
A 1
FIG. 2. Coronal sections of the brain stem showing the splitting of the habenular, posterior and intertectal commissures (Weil method). For each of the three cats the numbers to the left indicate the approximate AP Horsley-Clarke level. Note that the transection includes the upper part of the periventricular gray.
one side to the superior colliculus of the other side [ 16]. Since the superior colliculus gives rise to ascending projections which reach the cortex after a relay in the thalamus [14,23], it has been pointed out that the crossed corticotectal projection may be used for the indirect transmission of visual information between the cortices of the t w o sides even after section of the cortical commissures [16].
However, the present results make it clear that this indirect pathway for the interhemispheric transmission of visual information is unessential for interocular transfer o f pattern discriminations in split-chiasm cats, since the crossed cortico-tectal connection was obviously interrupted by our intertectal sections. While indicating that the corpus callosum is the crucial
1
22 (21--26) 16.5 (13-26)
Split chiasm (N = 4)
Split brain (N = 6)
22 (17-27) 21 (16-25)
Split chiasm (N = 3)
Split brain (N = 5)
19 (18--24) 21 (19--26)
Split chiasm (N = 4)
Split brain (N = 5)
23 (15-33)
5.5 (4--12)
17 12
25 (17-29)
10 (9-14)
8 19
22 (20-24)
-5 (-12-23)
58 (23--66)
6 31
-14 (-24-11)
31 (22-46)
45 22
(-30-4)
-11.5
37 (23--64)
33
33 3 26
score
Transfer
240 (110--242)
196.5 (164-718)
237 1837
143 (26-410)
149 (104-385)
178 560
(109-364)
178.5
270.5 (145--583)
1028
98 351 610
First eye
98 (62--255)
10 (4-25)
44 78
227 (70-644)
(0-69)
11
24 241
(74-361)
177
19 (0-469)
27
24 124 142
Second eye
Trials to first significant run
6 (-3-69)
94 (89--96)
69 92
-22 (-72-22)
81 (70-100)
76 40
8.5 (-41-20)
80 (10--100)
95
61 48 62
score
Transfer
88 (58--139)
141 (64--245)
90 825
60 (23-229)
90 (58-215)
96 446
78.5 (51-171)
143 (72--364)
610
36 148 244
First eye
46 (25-150)
16 (4--46)
29 43
87 (39-341)
27 (9-66)
15 319
81.5 (50-153)
26 (5--217)
108
16 63 55
Second eye
Errors to final criterion
12 (-31--56)
78 (57--91)
51 90
-20 (-58-30)
54 (53--73)
73 17
3.5 (-44-8)
63.5 (25--88)
70
38 40 63
score
Transfer
The initial performance score is the n u m b e r of errors committed during the initial 40 trials. A significant run is the first sequence of correct responses, including at most one error, with a chance probability o f occurrence equal to or less than 0.01. The difficult learning criterion required the performance of at least 36 correct responses in each of two consecutive 40 trial sessions. For each score of the split-chiasm and split-brain cats the table indicates the median value and, in parentheses, the range. For the easy learning criterion (18 correct responses out of 20 trials) no data from split-chiasm and split-brain cats were available. It is clear that in the cats with tectal splitting interocular transfer was successful also on these tests with a reduced training with the first eye, although there the transfer was not immediate. The low transfer scores for cat Sub 5 or Problem I-- are best attributed to a reduction of the visual ability of the eye receiving the transfer, as indicated by the p o o r performance o f the animal when using that eye for initial learning. In the cats with tectal splittings, an asterisk indicates problems learned with the right eye, and a dagger indicates problems learned to the easier criterion (18 correct responses out o f 20 trials).
19 23
Sub l * t Sub 5
Problem +0
21 30
Sub 1 Sub 5*
Problem l--
10
20 9.5 (5--16)
9 17 20
18 18 34
Second eye
Sub 1" Sub 3 t Sub 3 * t ~eversed problem) Sub 5
Problem AV
First eye
Initial performance
SCORES FOR LEARNING AND INTEROCULAR T R A N S F E R IN SPL1T-CHIASM CATS, SPLIT-CHIASM CATS WITH TECTAL SPLITTINGS AND SPLIT-BRAIN CATS
TABLE
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60
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