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The hemispheric dominance of cortical cells in the absence of direct visual pathways
Brain Research, 232 (1982) 187-190 Elsevier Biomedical Press
187
The hemispheric dominance of cortical cells in the absence of direct visual pathways
URI YINON, ABRAHAM HAMMER and MICHAEL PODELL Physiological Laboratory, Maurice and Gabriela Goldschleger Eye Institute, Tel-/lviv University Medical School, Sheba Medical Center, Tel-Hashomer 52621 (Israel)
(Accepted October 15th, 1981) Key words: split chiasm - - optic tract section - - visual cortex cells - - receptive fields - - corpus callosum
Unit recording was carried out in the visual cortex of split chiasm and optic tract-sectioned adult cats. From the proportions of the visually responsive and unresponsive cells found in each hemisphere of the operated cats it was concluded that the indirect pathway via the corpus callosum becomes visually inactive under these conditions. However, the direct geniculocortical pathway remains visually active. Thus, it was assumed that unilateral or bilateral elimination of the decussating palhway has a crucial effect on the amount of interhemispheric callosal transfer of basic visual functions. It has already been found that callosal fibers in the posterior part of the corpus eallosum (splenium) have visual properties similar to that of cells in the visual cortex, as revealed by their receptive field organization and binocularity 2,7,1z. It has further been discovered that the great majority of the eallosal fibers have receptive fields which overlap the midline and thus connect with the vertical meridian of the retina. On the basis of these findings it was suggested that the corpus callosum takes part in binocular depth perception for the center of the visual field, and in the preservation of continuity between the two halves of the visual field. That such an interhemispheric transfer of visual information exists in the corpus callosum has been further confirmed electrophysiologicaUy by several investigators 3-5, 15; they found, in the visual cortex of split chiasm and optic tract-sectioned cats, a visual input which is mediated through the indirect callosal pathways. In view of the above-mentioned studies, there is a need to show the effectiveness of the input from the direct geniculocortical route versus the indirect pathway via the corpus callosum. This bears on the hemispheric dominance in the absence of the direct route which is the main subject of the present study. In 6 adult street cats, the optic chiasm was surgically split along the sagittal line 9. Additional details concerning the surgical techniques have been described previously in detail 16. Thus, it was possible to test electrophysiologicaUy, in each hemisphere of these cats, the effectiveness of the indirect callosal visual input following visual 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
188 stimulation of the contralateral eye. Furthermore, using a similar surgical approach, the optic tract was unilaterally sectioned in 3 other adult cats. In the latter group of cats, electlophysiological studies in the hemisphere isolated from direct visual input could indicate the amount of indirect callosal input. Five normal adult cats served as controls. Unit recording was made in one acute, and 5 chronic (1-4 months) split chiasm, and in two acute and one chronic (3 months) optic tract-sectioned cats. For the recording session the cat was anesthetized with thiopentone sodium, paralyzed, a~tiffcially respired and placed in a stereotaxic apparatus. Infusion solution of precalculated amounts of Flaxedil, dextrose and saline was given constantly. The ECG, EEG, rectal temperature and expiratory CO2 weze continuously monitored. The eyes were optically refracted and corrected and the retinal landmarks projected onto a screen on which receptive fields were mapped for each cell and eye. Tungsten microelectrodes wele inserted into the cortex following craniotomy. The visual cortex was recorded mainly from the 17-18 boundary where the callosal fibers terminate 1,13,14. Light slits driven by hand or by an automatic remote control system were used for stimulation. Action potentials were identified and electronically counted. Each recolding session lasted for 2-4 days. The sectioned chiasm and tract and the penetration sites in the cortex were studied histologically using cresyl violet staining techniques. Other details concerning anesthesia, smgery, stimulation and recording were described previously in detail t6. All the cells recorded in the split chiasm cats reacted exclusively to stimulation of the ipsilateral eye (Table I). Only few cells in these cats (10) were initially suspected as binocularly driven; however, they could not be clearly proved as visually responsive using most physiological criteria and especially receptive field mapping. The ipsilaterally driven cells could not, by any means, be driven through the indirect callosal pathway in the chronic (n =: 5), as well as in the acute (n = l) cats. Thus, the visual activity transferred through the corpus eallosum in these cats was not efficient enough to activate cells deprived of their direct visual input. In the left hemisphere of the split chiasm cats 45.4 ~/o of the identified cells were visually responsive and in the right TABLE I
Properties of visual cortex cells recorded from split chiasm and optic tract sectioned cats Operation
No. of No. of Hemisphere cats cells recorded
Split chiasm 6 Optictract 3 section Normal controls 5
374 201
145
% Identified cells Driven by ipsilateral eye
Driven by Binocularly contralateral driven eye
Visually unresponsive
Both Ipsilateralto sectionedtract Contralateral to sectioned tract
41.0
--
--
59.0
--
--
--
100.0
3.3
2.2
44.4
50.0
Left
13.0
10.9
63.8
12.3
189 hemisphere this value was 34.1 ~o. The high proportion of visually unresponsive cells (total: 59.0 ~ , Table I) resulted from the loss of 70 ~ optic nerve fibers naturally decussating in the optic chiasm of cats 11. The results in the cats with the unilaterally sectioned optic tract showed that not one cell was visually responsive in the hemisphere ipsilateral to the operated side (Table I). In one cat two cells were suspected as visually responsive in this hemisphere but this could not be clearly verified. However, half of the cells were visually driven in the hemisphere ipsilateral to the intact tract. It is worth mentioning here that the distribution of cortical cells according to their ocular dominance is far different in the responsive hemisphere of these cats (5.5 ~ monocularly and 44.4 ~ binocularly driven cells) in comparison to the normal conUols (23.9 ~ monocularly and 63.8 ~ binocularly driven cells). As in the previous group of cats, many visually unresponsive cells (50.0 ~o in comparison to 12.3 ~ in our control cats) with clear action potentials and with typical spontaneous discharge were found in the visually active hemisphere - - a fact which is not yet explainable. The results were similar for the chronic (n = 1) and the acute (n = 2) cats of this group concerning the hemispheric dominance of cortical cells. The absence of visual input mediated through the indirect callosal pathway in the operated cats of both groups is not due to a traumatic surgical procedure, since the same results were obtained when recording was performed in the fully recovered chronic (up to 4 months) and acute cats. Furthermore, the disappearance of contralateral visual input is not due to damage to the non-decussating fibers concerned with the vertical meridian, as verified histologically in the two groups of cats. In addition, these fibers are intact in the unoperated side of the unilaterally optic tract-sectioned cats and still have no visual contribution to the hemisphere ipsilateral to the sectioned tract. The results from the split chiasm cats might lead to the conclusion that only optic nerve fibers decussating in the chiasm are represented in the corpus callosum; following the disappearance of these fibers the callosum becomes inactive. Although this condition is not impossible, it is not supported by the findings in the tract-sectioned cats. In these animals, despite the fact that one set of decussating fibers remains intact, we have not obtained any visual callosal input. Thus, the two experimental paradigms are in keeping with each other regarding the inactivation of the corpus callosum. Our results disagree with those of previous authors who found in one case 12.9 ~o3, and in another case 81.1 ~5, binocularly driven cells in the visual cortex of split chiasm adult cats. In addition, we could not confirm previous positive results4,15 in the visual cortex of unilaterally optic tract-sectioned cats. This contradiction might be explained by technical reasons. Unlike the previous studies, in our study the main criterion for responsiveness was the organization and spatial properties of the receptive field ~6. Differences in the surgical procedures might also explain the difference in the results. Our results suggest that the visual activity projected normally to the visual cortex via the corpus callosum and concerned with basic visual functions, is limited. This conclusion is suppoIted by the fact that in the visual corpus callosum only small
190 p r o p o r t i o n s o f visually active cells c o u l d be f o u n d z,7. As m e n t i o n e d above, the nondecussating tibet s are either very p o o r l y represented in the corpus c a l l o s u m o f not real cats, or n o t at all. Thus, following e l i m i n a t i o n o f the decussating fibers - - even unilaterally - - the t h r e s h o l d excitation o f the callosal fibers is elevated. This hypothesis is especially conceivable if callosal activity is reciprocally a n d instantaneously d e p e n d e n t on the two hemispheres. The conclusion d r a w n in the present study f r o m the tract-sectioned cats, is in keeping with o u r previous one 16 based on studies with split chiasm cats; namely, visual callosal fibers take p a r t in high o r d e r interhemispheric c o m m u n i c a t i v e tasks and, thus, scarcely reflect simple visual functions. Evidence for this comes from several studies on c a l l o s u m - s e c t i o n e d cats. W h e n the cortical receptive fields were studied in these cats it was c o n c l u d e d that no change in the cortical r e p r e s e n t a t i o n o f the region o f the vertical m e r i d i a n h a d been f o u n d 8. F u r t h e r s u p p o r t for this was given by a visual field p e r i m e t r y study in split c a l l o s u m a d u l t cats, where no effect was f o u n d following the surgery 6. However, a r e d u c t i o n o f b i n o c u l a r l y driven cortical cells was f o u n d following sectioning o f the corpus c a l l o s u m 1°. F o l l o w i n g the a b o v e - m e n t i o n e d studies a n d o u r present study, it seems necessary to find a way for studying the efficiency o f the direct geniculocortical, versus the indirect callosal p a t h w a y s in the intact visual system. 1 Berlucchi, G., Anatomical and physiological aspects of visual functions of corpus callosum, Brain Res., 37 (1972) 371-392. 2 Berlucchi, G., Gazzaniga, M. S. and Rizzolatti, G., Microelectrode analysis of visual information by the corpus callosum, Arch. ital. Biol., 105 (1967) 583-596. 3 Berlucchi, G. and Rizzolatti, G., Binocularly driven neurons in visual cortex of split-chiasm cats, Science, 159 (1968) 308-310. 4 Choudhurry, B. P., Whitteridge, D. and Wilson, M. E., The function of the callosal connections of the visual cortex, Quart. J. exp. Physiol., 50 (1965) 214~219. 5 Cynader, M., Lepor6, F. and Guillemot, J., Inter-hemispheric competition during postnatal development, Nature (Lond.), 290 (1981) 139-140. 6 Elberger, A. J., The role of the corpus callosum in the development of interocular eye alignment and the organization of the visual field in the cat, Exp. Brain Res., 36 (1979) 71-88. 7 Hubel, D. H. and Wiesel, T. N., Cortical and callosal connections concerned with the vertical meridian of visual fields in the cat, J. Neurophysiol., 30 (1967) 1561-1573. 8 Leicester, J., Projection of the visual vertical meridian to cerebral cortex of the cat, J. Neurophysiol., 31 (1968) 371-382. 9 Myers, R. E., lnterocular transfer of pattern discrimination in cats following section of crossed optic fibers, J. comp. physioL PsychoL, 48 (1955) 470-473. 10 Payne, B. R., Elberger, A. J., Berman, N. and Murphy, E. H., Binoculatiry in the cat visual cortex is reduced by sectioning the corpus callosum, Science, 207 (1980) 1097-1099. 11 Polyak, S., The Vertebrate Visual System (Ed. H. Kl/iver), University of Chicago Press, Chicago, 1968, 788 pp. 12 Shatz, C. J., Abnormal interhemispheric connections in the visual system of Boston Siamese cats: a physiological study, J. comp. Neurol,, 171 (1977) 229-246. 13 Shatz, C. J., Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats, J. comp. NeuroL, 173 (t977) 497-518. 14 Tusa, R. J., Palmer, L. A. and Rosenquist, A. C., The retinotopic organization of area 17 (striate cortex) in the cat, J. comp. Neurol., 177 (1978) 213-236. 15 Vesbayeva, C., Whitteridge, D. and Wilson, M. E., Callosal connexions of the cortex representing the area centralis, J. Physiol. (Lond.), 191 (1967) 79P-80P. 16 Yinon, U. and Hammer, A., Physiological mechanisms underlying responsiveness of visual cortex neurons following optic chiasm split in cats. In H. Flohr and W. Preeht (Eds.), Lesion-Induced Neuronal Plasticity in Sensorimotor Systems, Springer-Verlag, Berlin, 1981, pp. 360-368.
187
The hemispheric dominance of cortical cells in the absence of direct visual pathways
URI YINON, ABRAHAM HAMMER and MICHAEL PODELL Physiological Laboratory, Maurice and Gabriela Goldschleger Eye Institute, Tel-/lviv University Medical School, Sheba Medical Center, Tel-Hashomer 52621 (Israel)
(Accepted October 15th, 1981) Key words: split chiasm - - optic tract section - - visual cortex cells - - receptive fields - - corpus callosum
Unit recording was carried out in the visual cortex of split chiasm and optic tract-sectioned adult cats. From the proportions of the visually responsive and unresponsive cells found in each hemisphere of the operated cats it was concluded that the indirect pathway via the corpus callosum becomes visually inactive under these conditions. However, the direct geniculocortical pathway remains visually active. Thus, it was assumed that unilateral or bilateral elimination of the decussating palhway has a crucial effect on the amount of interhemispheric callosal transfer of basic visual functions. It has already been found that callosal fibers in the posterior part of the corpus eallosum (splenium) have visual properties similar to that of cells in the visual cortex, as revealed by their receptive field organization and binocularity 2,7,1z. It has further been discovered that the great majority of the eallosal fibers have receptive fields which overlap the midline and thus connect with the vertical meridian of the retina. On the basis of these findings it was suggested that the corpus callosum takes part in binocular depth perception for the center of the visual field, and in the preservation of continuity between the two halves of the visual field. That such an interhemispheric transfer of visual information exists in the corpus callosum has been further confirmed electrophysiologicaUy by several investigators 3-5, 15; they found, in the visual cortex of split chiasm and optic tract-sectioned cats, a visual input which is mediated through the indirect callosal pathways. In view of the above-mentioned studies, there is a need to show the effectiveness of the input from the direct geniculocortical route versus the indirect pathway via the corpus callosum. This bears on the hemispheric dominance in the absence of the direct route which is the main subject of the present study. In 6 adult street cats, the optic chiasm was surgically split along the sagittal line 9. Additional details concerning the surgical techniques have been described previously in detail 16. Thus, it was possible to test electrophysiologicaUy, in each hemisphere of these cats, the effectiveness of the indirect callosal visual input following visual 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
188 stimulation of the contralateral eye. Furthermore, using a similar surgical approach, the optic tract was unilaterally sectioned in 3 other adult cats. In the latter group of cats, electlophysiological studies in the hemisphere isolated from direct visual input could indicate the amount of indirect callosal input. Five normal adult cats served as controls. Unit recording was made in one acute, and 5 chronic (1-4 months) split chiasm, and in two acute and one chronic (3 months) optic tract-sectioned cats. For the recording session the cat was anesthetized with thiopentone sodium, paralyzed, a~tiffcially respired and placed in a stereotaxic apparatus. Infusion solution of precalculated amounts of Flaxedil, dextrose and saline was given constantly. The ECG, EEG, rectal temperature and expiratory CO2 weze continuously monitored. The eyes were optically refracted and corrected and the retinal landmarks projected onto a screen on which receptive fields were mapped for each cell and eye. Tungsten microelectrodes wele inserted into the cortex following craniotomy. The visual cortex was recorded mainly from the 17-18 boundary where the callosal fibers terminate 1,13,14. Light slits driven by hand or by an automatic remote control system were used for stimulation. Action potentials were identified and electronically counted. Each recolding session lasted for 2-4 days. The sectioned chiasm and tract and the penetration sites in the cortex were studied histologically using cresyl violet staining techniques. Other details concerning anesthesia, smgery, stimulation and recording were described previously in detail t6. All the cells recorded in the split chiasm cats reacted exclusively to stimulation of the ipsilateral eye (Table I). Only few cells in these cats (10) were initially suspected as binocularly driven; however, they could not be clearly proved as visually responsive using most physiological criteria and especially receptive field mapping. The ipsilaterally driven cells could not, by any means, be driven through the indirect callosal pathway in the chronic (n =: 5), as well as in the acute (n = l) cats. Thus, the visual activity transferred through the corpus eallosum in these cats was not efficient enough to activate cells deprived of their direct visual input. In the left hemisphere of the split chiasm cats 45.4 ~/o of the identified cells were visually responsive and in the right TABLE I
Properties of visual cortex cells recorded from split chiasm and optic tract sectioned cats Operation
No. of No. of Hemisphere cats cells recorded
Split chiasm 6 Optictract 3 section Normal controls 5
374 201
145
% Identified cells Driven by ipsilateral eye
Driven by Binocularly contralateral driven eye
Visually unresponsive
Both Ipsilateralto sectionedtract Contralateral to sectioned tract
41.0
--
--
59.0
--
--
--
100.0
3.3
2.2
44.4
50.0
Left
13.0
10.9
63.8
12.3
189 hemisphere this value was 34.1 ~o. The high proportion of visually unresponsive cells (total: 59.0 ~ , Table I) resulted from the loss of 70 ~ optic nerve fibers naturally decussating in the optic chiasm of cats 11. The results in the cats with the unilaterally sectioned optic tract showed that not one cell was visually responsive in the hemisphere ipsilateral to the operated side (Table I). In one cat two cells were suspected as visually responsive in this hemisphere but this could not be clearly verified. However, half of the cells were visually driven in the hemisphere ipsilateral to the intact tract. It is worth mentioning here that the distribution of cortical cells according to their ocular dominance is far different in the responsive hemisphere of these cats (5.5 ~ monocularly and 44.4 ~ binocularly driven cells) in comparison to the normal conUols (23.9 ~ monocularly and 63.8 ~ binocularly driven cells). As in the previous group of cats, many visually unresponsive cells (50.0 ~o in comparison to 12.3 ~ in our control cats) with clear action potentials and with typical spontaneous discharge were found in the visually active hemisphere - - a fact which is not yet explainable. The results were similar for the chronic (n = 1) and the acute (n = 2) cats of this group concerning the hemispheric dominance of cortical cells. The absence of visual input mediated through the indirect callosal pathway in the operated cats of both groups is not due to a traumatic surgical procedure, since the same results were obtained when recording was performed in the fully recovered chronic (up to 4 months) and acute cats. Furthermore, the disappearance of contralateral visual input is not due to damage to the non-decussating fibers concerned with the vertical meridian, as verified histologically in the two groups of cats. In addition, these fibers are intact in the unoperated side of the unilaterally optic tract-sectioned cats and still have no visual contribution to the hemisphere ipsilateral to the sectioned tract. The results from the split chiasm cats might lead to the conclusion that only optic nerve fibers decussating in the chiasm are represented in the corpus callosum; following the disappearance of these fibers the callosum becomes inactive. Although this condition is not impossible, it is not supported by the findings in the tract-sectioned cats. In these animals, despite the fact that one set of decussating fibers remains intact, we have not obtained any visual callosal input. Thus, the two experimental paradigms are in keeping with each other regarding the inactivation of the corpus callosum. Our results disagree with those of previous authors who found in one case 12.9 ~o3, and in another case 81.1 ~5, binocularly driven cells in the visual cortex of split chiasm adult cats. In addition, we could not confirm previous positive results4,15 in the visual cortex of unilaterally optic tract-sectioned cats. This contradiction might be explained by technical reasons. Unlike the previous studies, in our study the main criterion for responsiveness was the organization and spatial properties of the receptive field ~6. Differences in the surgical procedures might also explain the difference in the results. Our results suggest that the visual activity projected normally to the visual cortex via the corpus callosum and concerned with basic visual functions, is limited. This conclusion is suppoIted by the fact that in the visual corpus callosum only small
190 p r o p o r t i o n s o f visually active cells c o u l d be f o u n d z,7. As m e n t i o n e d above, the nondecussating tibet s are either very p o o r l y represented in the corpus c a l l o s u m o f not real cats, or n o t at all. Thus, following e l i m i n a t i o n o f the decussating fibers - - even unilaterally - - the t h r e s h o l d excitation o f the callosal fibers is elevated. This hypothesis is especially conceivable if callosal activity is reciprocally a n d instantaneously d e p e n d e n t on the two hemispheres. The conclusion d r a w n in the present study f r o m the tract-sectioned cats, is in keeping with o u r previous one 16 based on studies with split chiasm cats; namely, visual callosal fibers take p a r t in high o r d e r interhemispheric c o m m u n i c a t i v e tasks and, thus, scarcely reflect simple visual functions. Evidence for this comes from several studies on c a l l o s u m - s e c t i o n e d cats. W h e n the cortical receptive fields were studied in these cats it was c o n c l u d e d that no change in the cortical r e p r e s e n t a t i o n o f the region o f the vertical m e r i d i a n h a d been f o u n d 8. F u r t h e r s u p p o r t for this was given by a visual field p e r i m e t r y study in split c a l l o s u m a d u l t cats, where no effect was f o u n d following the surgery 6. However, a r e d u c t i o n o f b i n o c u l a r l y driven cortical cells was f o u n d following sectioning o f the corpus c a l l o s u m 1°. F o l l o w i n g the a b o v e - m e n t i o n e d studies a n d o u r present study, it seems necessary to find a way for studying the efficiency o f the direct geniculocortical, versus the indirect callosal p a t h w a y s in the intact visual system. 1 Berlucchi, G., Anatomical and physiological aspects of visual functions of corpus callosum, Brain Res., 37 (1972) 371-392. 2 Berlucchi, G., Gazzaniga, M. S. and Rizzolatti, G., Microelectrode analysis of visual information by the corpus callosum, Arch. ital. Biol., 105 (1967) 583-596. 3 Berlucchi, G. and Rizzolatti, G., Binocularly driven neurons in visual cortex of split-chiasm cats, Science, 159 (1968) 308-310. 4 Choudhurry, B. P., Whitteridge, D. and Wilson, M. E., The function of the callosal connections of the visual cortex, Quart. J. exp. Physiol., 50 (1965) 214~219. 5 Cynader, M., Lepor6, F. and Guillemot, J., Inter-hemispheric competition during postnatal development, Nature (Lond.), 290 (1981) 139-140. 6 Elberger, A. J., The role of the corpus callosum in the development of interocular eye alignment and the organization of the visual field in the cat, Exp. Brain Res., 36 (1979) 71-88. 7 Hubel, D. H. and Wiesel, T. N., Cortical and callosal connections concerned with the vertical meridian of visual fields in the cat, J. Neurophysiol., 30 (1967) 1561-1573. 8 Leicester, J., Projection of the visual vertical meridian to cerebral cortex of the cat, J. Neurophysiol., 31 (1968) 371-382. 9 Myers, R. E., lnterocular transfer of pattern discrimination in cats following section of crossed optic fibers, J. comp. physioL PsychoL, 48 (1955) 470-473. 10 Payne, B. R., Elberger, A. J., Berman, N. and Murphy, E. H., Binoculatiry in the cat visual cortex is reduced by sectioning the corpus callosum, Science, 207 (1980) 1097-1099. 11 Polyak, S., The Vertebrate Visual System (Ed. H. Kl/iver), University of Chicago Press, Chicago, 1968, 788 pp. 12 Shatz, C. J., Abnormal interhemispheric connections in the visual system of Boston Siamese cats: a physiological study, J. comp. Neurol,, 171 (1977) 229-246. 13 Shatz, C. J., Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats, J. comp. NeuroL, 173 (t977) 497-518. 14 Tusa, R. J., Palmer, L. A. and Rosenquist, A. C., The retinotopic organization of area 17 (striate cortex) in the cat, J. comp. Neurol., 177 (1978) 213-236. 15 Vesbayeva, C., Whitteridge, D. and Wilson, M. E., Callosal connexions of the cortex representing the area centralis, J. Physiol. (Lond.), 191 (1967) 79P-80P. 16 Yinon, U. and Hammer, A., Physiological mechanisms underlying responsiveness of visual cortex neurons following optic chiasm split in cats. In H. Flohr and W. Preeht (Eds.), Lesion-Induced Neuronal Plasticity in Sensorimotor Systems, Springer-Verlag, Berlin, 1981, pp. 360-368.