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Behavioural Brain Research, 7 (1983) 211-227 211 Elsevier Biomedical Press
EFFECTS OF UNILATERAL AND BILATERAL LESIONS OF THE LATERAL SUPRASYLVIAN AREA ON LEARNING AND INTERHEMISPHERIC TRANSFER OF PATTERN DISCRIMINATION IN THE CAT
MAURICE PTITO and FRANCO LEPORE
Groupe de Recherche en Neuropsychologie Exp~rimentale, Universit~ du Quebec C.P. 500 Trois-RiviEres, Que. G9A 5H7; and (F.L.) DEpartement de Psychologie, Centre de Recherche en Sciences Neurologiques,
Universit( de Montreal. C.P. 6128. Montreal, Que. H3C 3J7 (Canada)
(Received June 1st, 1982)
(Revised version received August 19th, 1982)
(Accepted September 16th, 1982)
Key words: lateral suprasylvian lesion - form discrimination - interhemispheric transfer - vision -
split-chiasma cat
SUMMARY
The aim of the present experiment was to evaluate the hypothesis that the lateral suprasylvian area is involved in the interhemispheric transfer of visual information. This area was surgically removed in 10 cats which had previously undergone a midsagittal transection of their optic chiasmas. The animals then learned a pattern discrimination using either one or the other hemisphere and were tested for transfer using the other, untrained hemisphere. The lateral suprasylvian area in the intact hemisphere was next ablated in 6 of these cats. Each hemisphere was trained on a new pattern discrimination and tested for transfer using the other. The results obtained with the unilaterally lesioned animals indicated that: (a) learning with the lesioned hemisphere was as rapid as with the intact hemi- sphere; and (b) that transfer in either direction was normal although slightly retarded, but not significantly so, when the information proceeded from the intact to the lesioned hemisphere. Learning with either hemisphere of the bilaterally lesioned animals also appeared to be normal. Learning with the hemisphere which was lesioned second and transferring to the one which was ablated first was within normal range whereas transfer was generally not as immediate when the procedure was reversed. As a whole, the results, when coupled with those of others, would tend to indicate that the lateral suprasylvian area is involved in interhemispheric
0166-4328/83/0000-0000/$03.00 © 1983 Elsevier Biomedical Press
212
transfer but shares this function with other callosally connected areas of the primary visual cortex.
INTRODUCTION
Since the pioneering work of Sperry et al. [26] and Myers [19], which demonstrated that the fibers contained in the posterior third of the corpus callosum were responsible for the interocular transfer of monocularly learned pattern discriminations in split chiasma cats, numerous studies have attempted to identify their cortical areas of origin and termination. Anatomical studies have demonstrated that areas 17, 18 and 19 project through this structure to homotopic contralateral areas. The lateral suprasylvian area, which has been shown by both anatomy [7, 11, 15, 21, 23, 24] and physiology [8, 16, 25] to be involved in vision also sends strong callosal projections to the corresponding contralateral area throughout most of its extent. This area, moreover, is innervated via the callosum with fibers originating in contralateral areas 17, 18 and 19 [14, 15, 17, 24].
Various neurobehavioral studies have been carried out to evaluate the relative importance of these different areas for interhemispheric transfer of visual information. In one experiment, Berlucchi et al. [4] made both unilateral and bilateral lesions of the callosally connected portions of 17, 18 and 19 in split- chiasma cats. They found little or no difference in the degree ofinterocular transfer in these cats as compared to non-lesioned split-chiasma cats. In a second experiment, these researchers sectioned, besides the optic chiasma, the intertectal and posterior commissures while leaving intact the forebrain commissures and the cortical visual areas [5]. Interocular transfer was also found to be perfect when compared to appropriate controls. A conclusion which could be drawn from these experiments was that cortical areas other than 17, 18 and 19 and innervated through the callosum, were sufficient to mediate transfer. The most likely region, based on the anatomical considerations presented above, was the suprasylvian area. This hypothesis was tested by Berlucchi and collaborators [6], They lesioned, in split-chiasma cats, the crown and lateral bank of this gyrus on one side of the brain and tested for interocular transfer. Their results indicated that the resection interfered in a specific manner with this capacity: a pattern discrimination learned with the eye projecting to the intact hemisphere did not transfer to the lesioned side while transfer in the opposite direction was unaffected. These results would tend to attest to the essential nature of this area for transfer.
The aim of the present experiment was twofold. The anatomical data available in the literature seemed to indicate that the most important subdivision of the suprasylvian gyrus, in terms of its callosal innervation, was the lateral suprasylvian area or LSA [3, 14, 15, 24]. The first purpose was therefore to determine whether restricting the lesion as much as possible to this apparently
213
critical area was sufficient to block interhemispheric transfer along the lines suggested by the experiment reported above [6]. However, LSA has been shown under some circumstances to be important for learning [ 1, 2, 6, 9, 13, 22, 27]. The possibility existed, therefore, that transfer tests in unilaterally lesioned animals might be contaminated, when examining that side, by learning deficits. To circumvent the problem posed by these potential hemispheric differences in learning ability, the second aim of the experiment was to evaluate the transfer capacity of bilaterally LSA lesioned animals. If LSA were really essential for transfer, then its bilateral removal should completely abolish interocular transfer in either directions.
METHODS
Surgery and histology Surgery was carried out in 10 adult cats using halothane anesthesia under
conditions of partial asepsis. The splitting of the chiasma was performed using the transbuccal approach described by Myers [20]. Cortical lesions were made by subpial aspiration. Following the lesions, the animals were given antibiotics and other post-operative care for at least two weeks.
After completing the behavioral tests, they were anesthetized and perfused through the heart with isotonic saline followed by 10~o formalin. The brains were removed, photographed and blocked in paraffin. Each brain was cut into coronal sections 10 ~m thick. For most of the brain, only one slice every 200/~m was retained whereas in that portion of the block containing the optic chiasma, every second slice was kept. The retained sections were colored using the Kltlver-Bar- rera [ 18 ] method.
Apparatus and testing procedure The training apparatus (see also ref. 22) consisted of a Thompson-like
two-choice discrimination box made up of three compartments: a holding section, a choice section and a reinforcement section. The stimuli were presented on two side-by-side hinged doors separating these last two sections and illuminated from behind. These consisted of pairs of patterns made out of black tape affixed to the front and center of the choice doors. Each stimulus of a pair subtended approximately 5 ° of visual angle when viewed from the start of the choice chamber, had the same surface area but differed either in orientation or configuration (see insets of Figs. 2-5).
A session consisted of 40 trials and the animals were tested 6 days a week. The average session took approximately 15 min to complete. The stimuli were presented at random on the two doors according to Gellerman's [ 12] table so that the positive stimulus was presented 20 times on the right and 20 times on the left. Positive reinforcement (pieces of palatable food), which the cat could obtain
214
by pushing open the door bearing the positive stimulus, was used throughout the experiment. If on any particular trial it pushed on the incorrect, locked door, the animal could correct its choice and have access to the reward via the other door (correction method). In general, they did not have to be food deprived; on the rare occasions when the performance of an animal was slow, its food was witheld for 22 h and, following testing, it was allowed to feed for about 2 h.
The animals were first familiarized with the experimenters and the apparatus. They were then taught to go through the choice doors, followed by training on a simple black-white discrimination, first carried out binocularly and then mono- cularly. The black stimulus was positive. The learning criterion was set at 36 correct responses out of 40 trials (90~o correct) for two consecutive days. Upon reaching the criterion with each eye, the animals underwent the splitting of the optic chiasma. They were then retested on the black-white discrimination, first binocularly and then monocularly. After reaching the learning criterion in all conditions a unilateral lesion was performed on the lateral suprasylvian area, either of the right (n -- 8) or of the left (n = 2) hemisphere. The target areas were the AMLS and PMLS of Palmer et al. [21]. They were then retested binocularly and monocularly on the dark-white discrimination to make certain that the operation had not interfered with their ability to perform the task.
The 10 animals were then randomly divided into two equal subgroups. The 5 subjects of Subgroup 1 (cats CB 19, 30, 21, 4 and 16) learned a pattern discrimination using the eye connected to the normal hemisphere and those of Subgroup 2 (cats CB 18, 26, 8, 20 and 22) did so using the eye which projected to the lesioned hemisphere. In all cases, the learning criterion was fixed at 36 correct responses out of 40 trials (90~o correct) for two consecutive days. Interocular transfer was next evaluated by occluding the previously trained eye and testing with the naive eye until the above criterion was reached.
Once this phase of the experiment was completed, 4 animals, CB 19 and 30* from Subgroup 1 and CB 18" and 26 from Subgroup 2, were subjected to the inverse procedure, that is, each animal was trained on another pattern using the eye previously involved in evaluating transfer and tested for transfer using the other eye. Thus, as a result of this strategy, 7 animals in all learned a pattern with the intact hemisphere and transferred to the lesioned hemisphere and an equal number of patterns was first learned with the lesioned side and had to transfer
to the intact side. The remaining 6 animals (CB 21, 4 and 16 from Subgroup 1 and CB 8, 20
and 22 from Subgroup 2) underwent symmetrical removal of the lateral supra- sylvian area of the intact hemisphere. Following recovery, the animals In'st learned to discriminate a new pattern using one eye. Upon reaching criterion, interocular transfer was assessed using the other eye. This eye was then used to learn another discrimination and transfer was evaluated using the untrained eye.
215
A
B
2B l I
CB 'F
Fig. 1. Histological verification of the extent of the lateral suprasylvian lesion. A: photographs of
the dorsal view of the brain. B: selected coronal sections through the cortical lesion.
RESULTS
Histological results
A microscopic examination of the KlOver-B arrera stained material indicated that the optic chiasmas were completely transected in all animals. The cortical lesions, moreover, were generally circumscribed to the target area. Because the , histological material is rather abundant, we have decided to summarize it under two general forms. First, in Fig. 1, are presented the photographs of the brains of the 10 cats used in this experiment. Each brain is shown (a) in its dorsal extent and (b) in a coronal section taken at the level which included the optic chiasma*. An inspection of this figure indicates that most lesions were centered around the target areas and that they were fairly symmetrical.
* Cats CB 18 and CB 30 underwent the additional transection of the corpus callosum after the
completion of testing for the present experiment and were subsequently used in another study.
216
Table I presents, on the other hand, a summary of the anatomical findings for the major visual structures of all 10 cats.
In summary, all these histological results, despite their differences, point to one general conclusion, namely, that the target visual areas were, in fact, essentially extirpated by the surgery.
Behavioral results
Two measures were used to assess learning and interocular transfer. One measure consisted of the total number of errors committed during the first session of 40 trials when a new pattern was presented to an animal or when the occluder was switched from the first to the second eye. This value, referred to as I.P., gives an indication of the initial performance of the cat. The comparison between the I.P. of the first eye versus the I.P. of the second eye on a particular pattern is generally regarded as a sensitive measure of the degree of transfer. However, the initial performance of an animal during transfer may be affected by contaminating factors, the most important of which is the fact that the hemianopia is in a different hemifield, possibly necessitating different scanning and approach strategies. Moreover, an animal may not show immediate transfer but may be able to profit from its past experience with the pattern to attain criterion more rapidly. This 'saving' effect would not be shown if only I.P. were considered. Therefore, another measure, T.E., which evaluates total performance in terms of the number of errors committed before attaining the final criterion was also used to assess transfer.
The results found following a unilateral lesion are shown in Table II. It is quite clear from this table that transfer is present, whether information is proceeding from the intact to the lesioned hemisphere or in the inverse direction. Transfer performance appears to be slightly worse in the intact to lesioned condition than in the opposite direction. This tendency is also evident from the individual results presented in Figs. 2 and 3, On 5 of the 7 discriminations in the intact to lesioned condition (Fig. 2) the animals required various sessions to attain criterion during transfer testing. This was the case on only two occasions for the
lesioned to intact condition (Fig. 3). The results were also treated statistically and various comparisons were
made. First the performance of the eye on the injured side was compared to that of the eye on the intact side in terms of their relative ability to learn a new discrimination. The raw data on I.P. and T.E. shown in Table II were logarithmically transformed to render them homogeneous. To compare the learning scores of the lesioned versus the intact hemisphere an analysis of variance (ANOVA) was carried out. However, because the results under each condition contained both related (n = 4) and independent measures (n = 3) a modified ANOVA [ 10] was employed. The analysis showed that the learning scores for the two hemispheres at both I.P. and T.E. were not significantly different, indicating
TA
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218
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Fig. 2. Learning curves for all unilaterally lateral suprasylvian lesioned cats. The discrimination was
first learned with one eye and then with the other. In this case the first eye is on the intact side and the second eye on the lesioned side. • . .0, first eye; A - - A , second eye, Abscissa: blocks of
40 trials. Ordinate: percent of correct responses on each block of 40 trials. Inset: pairs of patterns
used in the discrimination.
219
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Fig. 3. Learning curves for all unilaterally lateral suprasylvian lesioned cats. The discrimination was
performed first with the eye on the lesioned side and then with the eye on the intact side. See legend
Fig. 2.
220
TABLE I1
Learning (Learn.) and interocular transfer (Transf ) of various pattern discriminations qfier a unilateral
lateral suprasylvian lesion
I.P., mean initial performance (number of errors in first 40 trials); T.E., number of errors to final
criterion.
Cats Intact to lesioned Lesioned to intact
I.P. T.E. I.P. T.E.
Learn. Transf Learn. Transf Learn. Transf Learn. Tran~f
18 11 5 149
19 15 9 44
26 20 14 589
30 17 18 401
21 19 4 81
4 22 20 564
16 18 8 134
8
20
22
X 17.4 11.1 280.3
3.6 6.3 232.6
13
18
131
41
5
108
62
24 3 130 5
21 2 162 2
17 18 401 41
20 6 107 8
19 8 145 21
26 1 209 1
19 1 210 1
54 20.8 5.6 194.8 11.3
49.1 3.1 6.1 98.7 14.9
that the lesion per se did not affect the ability of an animal to learn the
discrimination with either hemisphere. A second analysis compared the ability to transfer a learned discrimination
from the intact to the lesioned hemisphere and vice-versa. A t-test for related samples [28 ] was carried out for both I.P. and T.E. and compared the performance of the first eye versus the performance of the second eye on the same pattern discrimination. In all cases, t-tests showed the differences to be significant (intact to lesioned s i d e - I.P., t = 3.50, df = 6, P < 0.02; T.E., t = 6.05, df = 6, P < 0.01. Lesioned to intact side - I.P., t = 4.00, df --- 6, P < 0.01 ; T.E., t = 6.41, df = 6, P < 0.01). This confirms the qualitative analysis carried out above on Table II and Figs. 2 and 3 to the effect that transfer is not perturbed in either direction by the unilateral LSA lesions. It shows, moreover, that the poorer transfer performance in the intact to lesioned condition does not attain statistical significance.
The results obtained from the bilaterally lesioned animals are presented in Table III and Figs. 4 and 5**. It is clear from this data that the ablation of the
** Cat CB 21 which we had planned to include in this group became extremely neurotic. It was
thereby discarded and the bilateral group contained therefore only 5 animals.
221
TABLE I l i
Learning (Learn.) and interocular transfer (Transf ) of various pattern discriminations after a bilateral lateral suprasylvian lesion
I.P., mean initial performance (number of errors in first 40trials); T.E., number of
errors to final criterion.
Ca ts First lesion to second lesion Second lesion to first lesion
I.P. T.E. I.P. T.E.
Learn. Transf Learn. Transf Learn. Transf Learn. Transf
4 20 11 403 262 27 4 576 32
8 10 3 34 3 17 7 64 33
16 18 13 203 132 23 10 432 42
20 18 22 640 84 24 8 263 11
22 20 18 184 27 18 13 365 26
17.2 13.4 292.8 101.6 21.8 8.4 340 28.8
a 4.1 7.2 234.3 102.8 4.2 3.4 191.6 11.5
second LSA area perturbs to some degree the transfer behavior of the animals. In a sense, this confirms the importance of this structure for transfer. However, it is also quite evident that transfer is present in all cases, learning being always quicker with the second eye than with the first. These conclusions were also supported by the statistical comparisons carried out on the logarithmically transformed results presented in Table III. As shown in the table the 5 animals which constituted the bilateral group learned and were evaluated for transfer on two pattern discriminations. One of these learned with the hemisphere which had been lesioned first and had to transfer to the one which had been ablated second and the opposite procedure obtained for the other pattern. Comparisons of the performance of the first eye (learning) versus the second eye (transfer) for each pattern, in terms of I.P. and T.E., were carried out using t-tests for paired means [28]. The results of the analyses showed that transfer was present when going from the hemisphere lesioned second to the one ablated first, since the animals performed significantly better with the second eye than with the first (I.P., t = 3.89, df = 4, P < 0.05; T.E., t = 5.30, df = 4, P < 0.01). When going from the first lesion to the second lesion, however, the performance of the animals during transfer was statistically different from that during learning only for T.E. (t = 3.61, df = 4, P < 0.05) and not for I.P. (t = 1.73, df --- 4, P > 0.05). This indicates that although transfer is present when the total performance of the animal is considered, most animals required varied numbers of sessions to attain a satisfactory performance.
100. 100.
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222
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B L O C K S O F 4 0 T R I A L S
Fig. 4. Learn ing curves for 5 ca ts with bilateral lateral suprasy lv ian lesion. The d i sc r imina t ions were
m a d e first with the eye on the side o f the first lesion and then with the one on the side o f the second
lesion. See legend Fig. 2.
1 0 0 .
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223
C B 4
I I I I 1 | i i l i l i i l l h J i l l I I I l h i i i h i l i l i i i l l l l
Fig. 5. Learning curves for 5 cats with bilateral lateral suprasylvian lesion. The discrimination was
performed first with the eye on the side of the second lesion then with the one on the side of the
first lesion. See legend Fig. 2.
224
UNILATERAL LESIONS
i n tac t to les ioned
les ioned to intaCt
' t 27
O ~ lz. r - ]
Ih i l i a .
BILATERAL LESIONS
first lesion second lesion to second lesion to f i rst lesion
21 8
IZ2
400
--I ~ / <~ 14J 300 I 280.3 Z .
, rL 200 194.8
100
292.8 m
~OIZ)
340 m
28.8
Fig. 6. Learning scores obtained following unilateral and bilateral lesions of the lateral suprasylvian
area. Each histogram gives the mean number of errors in the first 40 trials (top) and the mean number
of errors to reach final criterion (bottom). The open histograms represent learning and the darkened
ones stand for transfer.
The results are also summarized in the form of bar charts in Fig. 6. Again this figure confirms that transfer is generally present in LSA lesioned animals. It however also tends to show that transfer is poorer in unilaterally lesioned animals when information is proceeding from the intact to the lesioned hemisphere and is worst when LSA is ablated in the two hemispheres.
DISCUSSION
The results obtained in the present experiment have given rise to a series of comparisons. The first, of only passing interest as far as the main objectives of this study are concerned, compared the ability of the animals to lem'n a new pattern discrimination using either the intact hemisphere or the lateral suprasylvian lesioned hemisphere. Both the graphical representations and the statistical results indicate quite clearly that the two hemispheres were equally c o m p e ~ t in learning the problems. This would indicate that the lateral syprasylvian per se is not essential for learning to discriminate visual patterns. This f'mding is in aSreement with the findings of various other researchers, namely, that cats having lesions limited to the lateral suprasylvian area do not show marked deficits in discrimina- tive abilities [2, 9, 13].
225
The second comparison evaluated, in the unilaterally lesioned animals, the amount of interhemispheric transfer from the lesioned to the intact hemisphere and in the opposite direction. Berlucchi et al. [6] showed that in suprasylvian lesioned animals transfer was perfect in the first direction but deficient in the opposite direction. The present experiment using LSA lesioned cats confirmed the first finding but not the second. Although transfer from the intact to the lesioned hemisphere was accompanied with noticeable difficulties in that the animals did not show immediate transfer on a total of 5 out of 7 discriminations, both the individual results and the overall statistical analyses indicate that ablating the lateral suprasylvian area does not completely block the transfer of visual informa- tion coming from the intact side. We feel that these differences in results can best be explained in terms of lesion extent. In the present experiment, a deliberate attempt was made to limit the lesions as much as possible to the medial bank of the suprasylvian sulcus. As indicated in the histological results, the lesion did invade to various extents the crown of the gyrus, the lateral bank of the sulcus and parts of the primary visual areas. However, they were generally less extensive than many of those presented in the Berlucchi et al., [6] paper. Cat C 45 from the latter study, which most closely appears to resemble our cats in terms of lesion extent, also most closely resembles our cats in terms of its learning and transfer behavior.
Our results, on the other hand, resemble quite closely those obtained in a different study by Berlucchi et al. [4], where the lesions were limited to the primary visual areas 17, 18 and 19 and where transfer, though affected to about the same extent as in the present experiment, was neither completely blocked nor importantly retarded. It would appear, therefore, that a certain amount of equipotentiality exists between the primary visual areas and the lateral suprasylvian area in their ability to mediate interhemispheric transfer.
If the lateral suprasylvian area were the only region involved in mediating interhemispheric transfer, then its bilateral removal should block transfer in either direction. Transfer is, in fact, poorer in these animals when compared to animals having one intact hemisphere. Moreover, the statistical analyses of the bilaterally lesioned animals showed some differences in the transfer behavior of the animals in relation to the direction of transfer, namely, whether transfer proceeded from the hemisphere lesioned second to the one lesioned first or the reverse. Transfer was immediate in the former condition. When, on the other hand, the hemisphere lesioned first was used for learning, the animals showed both poor initial performance and increased number of errors to attain final criterion during transfer testing. Although this finding is difficult to explain, the significant results remain that interhemispheric transfer was at worst retarded but certainly not abolished by the bilateral removal of the lateral suprasylvian area.
In conclusion, therefore, these results would tend to indicate that the lateral suprasylvian area, although probably involved in mediating interhemispheric transfer, shares this function with caUosally innervated regions of the primary
226
visual cortex. We feel that this conclusion is the most parsimonious and congruent
in specifying the importance played by the two major visual subsystems. Various
neurobehavioral studies have shown that ablation of either visual subsystem is not
sufficient to completely abolish in cats their ability to discriminate patterns [ 1, 2,
6, 9, 13, 27]. Each is therefore capable of supporting this function. The anatomical
and electrophysiological studies cited at the beginning of this article [3, 14, 15, 24 ],
among others, have shown that these structures in each hemisphere are extensively
interconnected via the corpus callosum. Although it is possible that the callosal
interconnection of each system subserves different visual functions, it is more
probable, as our results would tend to indicate, that each is a sufficient structure
for mediating interhemispheric transfer of pattern discriminations.
ACKNOWLEDGEMENTS
This research was supported in part by grants from the Conseil de
Recherches en Sciences Naturelles et en G6nie du Canada, the Minist6re de
l 'Educat ion du Qu6bec and NATO. Thanks are also extended to M. Turcot te for
his help in the testing of the animals and to Dr. J.P. Descoteaux of the Institut
Armand Frappier for his kindness in allowing the technicians to prepare the
histological material.
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