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Representation of the complete retina in the contralateral superior colliculus of some mammals
Brain Research, 65 (1974) 343-346 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
343
Representation of the complete retina in the contralateral superior colliculus of some mammals
J. H. KAAS*, J. K. HARTING AND R. W. GUILLERY
Laboratory of Neurophysiology and Department of Anatomy, University of Wisconsin, Madison, Wisc. 53706 (U.S.A.) (Accepted October 4th, 1973)
'Our data on the rat include one case, number 2, with a lesion restricted to the extreme temporal retina, entirely on the temporal side of the fixation point. In this case the great majority of the degenerated fibers are uncrossed. None of the crossed fibers can be seen to terminate in the lateral geniculate nucleus and certainly most of them pass over the nucleus and terminate in the lateral margin of the superior colliculus. The uncrossed fibers, on the other hand, all enter the lateral geniculate nucleus and terminate within its caudal third.' K. S. Lashley, 1934 (ref. 7), For many years investigators interested in the mammalian visual system have accepted the theory that both the lateral geniculate nucleus and the superior colliculus receive retinal input from only the contralateral hemifield (see refs. 3 and 5 for reviews). With the exception of a few degrees of visual field close to the vertical meridian 8, there is no reason to question this theory regarding the lateral geniculate nucleus. However, the organization of retinal input to the superior colliculus may need to be re-evaluated in the light of recent electrophysiological evidence. Such data indicate that part of the ipsilateral hemifield is represented in the superior colliculus of the squirrel 4, the tree shrew 4 and the domestic cat 1,6 (see ref. 5 for review). Thus, each colliculus represents the entire contralateral retina, including the temporal retinal expanse that is devoted to the hemifield ipsilateral to that colliculus. Two possible pathways may account for this representation of the temporal retina within the contralateral superior colliculus ~. The first is a direct pathway to the superior colliculus from the temporal retina of the contralateral eye. The second is a route from the temporal retina to the ipsilateral colliculus and then after a relay through the intertectal commissure to the contralateral colliculus. The latter, indirect pathway is unlikely in the squirrel and tree shrew since retinal input to the ipsilateral colliculus is quite sparse in both forms (unpublished data). Furthermore, the long neglected observation of Lashley 7 (see above) indicates the likelihood - - at least in some species - - of a direct pathway from the temporal retina to the contralateral superior colliculus. In order to test this latter possibility, small lesions were made along the temporal margin of the retina in 6 tree shrews (Tupaia glis) and 6 grey squirrels (Sciureus * Present address: Department of Psychology,Vanderbilt University, Nashville, Tenn. 37240, U.S.A.
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SHORT COMMUNICATIONS
carolinensis). Following survival periods of 5-8 days the animals were killed, the brains removed, and frozen sections were stained for degenerating axons and their endings 2. The location of each lesion was recorded by direct observation of the flattened retina, and the normal eye was also examined for retinal damage. In 4 squirrels and 3 tree shrews the lesions appeared upon examination of the retina to involve only' the most temporal margin of the retina. In all 7 cases, degeneration was observed within the contralateral superior colliculus. Such degeneration was restricted to the superficial layers of the rostral and lateral regions of the colliculus (see Fig. 1). Thus, the degeneration occurred precisely where electrophysiological recordings have shown cells receiving inputs from the temporal retina 4. In addition, there were no other zones of tectal degeneration which might have suggested that the nasal retina had been damaged. Degeneration was also observed within the ipsilateral dorsal lateral geniculate of all 7 animals. In the tree shrews such degeneration was restricted to layers 1 and 5, with layer 5 receiving by far the densest input. The primary zone of degeneration within the squirrel's ipsilateral lateral geniculate was confined to layer 2. There was, however, one case in which degeneration was also observed within a portion of layer 3.
DORSAL
C A U D A L
Fig. 1. A parasagittal section of the superior colliculus. Degeneration is obvious within the rostral portion and has resulted from a large lesion involving the temporal retina of the contralateral eye. The boxed in area including the degeneration is shown at a higher magnification in the insert, l, -stratum griseum superficialis; 2, stratum opticum; 3, stratum griseum intermediates.
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345
Tempo~iNasal ~ Nucleus
/
Fig. 2. Schema of retinal projections to the dorsal lateral geniculate nucleus and the superior colliculus in tree shrews and squirrels. A pathway from the temporal retina to the ipsilateral superior colliculus was apparent only in one squirrel. Thus, for some mammals the primary projection from the temporal retina is to the contra-, not the ipsilateral superior colliculus. This is exactly the conclusion that Lashley, working on the rat, arrived at some 40 years ago 7. However, it was largely neglected since it did not fit current knowledge concerning the organization of the mammalian visual system. While we feel secure that our lesions did not cross the vertical meridian in any of our 7 critical animals, only two squirrels showed no degeneration at all in the contralateral lateral geniculate nucleus. In the remaining 2 squirrels and 3 tree shrews, there was a small fOCUS of degeneration within a small segment of the contralateral nucleus. These foci of degeneration were located in geniculate areas which do not receive retinal input from the region of the vertical meridian. Therefore, such degeneration could not have been produced by lesions that extended across the vertical meridian. In fact, several cases contained contralateral geniculate degeneration which was located within the monocular segment of the nucleus. We can only suggest that these foci of degeneration may (1) have resulted from our pulling on the optic nerve during surgerS,, (2) be the result of interruption of 'looping', retinofugal fibers, or (3) they may actually be terminals of axons arising within the temporal retina. None of these 5 animals showed a tectal focus of degeneration that would, oll the basis of known maps, correspond to a lesion of the nasal retina. The problem raised by these contralateral geniculate projections remains to be studied in detail. This investigation was supported by N I N D s Grants NS-06225, NS-06662, NS-05326, N S F Grant GB-36779 and Grant 135-4424 from the Graduate School, University of Wisconsin.
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SHORT COMMUNICATIONS Fig. 2 was d r a w n by Ms. D . U r b a n . H i s t o l o g i c a l m a t e r i a l s w e r e p r e p a r e d by
Ms. J o a n E k l e b e r r y a n d Ms. B o n n i e Bade.
1 FELDON,S., FELDON, P., AND KRUGER, L., Topography of the retinal projection upon the superior colliculus of the cat, Vision Res., 10 (1970) 135-193. 2 FINK, R. P., AND HEIMER, L., TWO methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374. 3 KAAS, J. H., GUILEERY, R. W., AND AELMAN,J. M., Some principles of organization in the dorsal lateral geniculate nucleus, Brain Behav. Evol., 6 (1972) 253-299. 4 LANE, R. H., ALLMAN, J. M., AND KAAS, J. H., Representation of the visual field in the superior colliculus of the grey squirrel (Sciurus carolinensis) and the tree shrew (Tupaia glis), Brain Research, 26 (1971) 277-292. 5 LANE, R. H., ALLMAN,J. M., KAAS, J. H., AND MIEZIN, F. M., The visuotopic organization of the superior colliculus of the owl monkey (Aotus trivirgatus) and the bushbaby (Galago senegalensis), Brain Research, 60 (1973) 335-349. 6 LANE, R. H., KAAS, J. H. AND ALLMAN,J. M., Visuotopic organization of the superior colliculus in normal and Siamese cats, Brain Research, in press. 7 LASHLEY,K. S., The mechanism of vision : VII. The projection of the retina upon the primary optic centers in the rat, J. comp. Neurok, 59 (1934) 341-373. 8 SANDERSON,K. J., AND SHERMAN,S. M., Nasotemporal overlap in visual field projected to lateral geniculate nucleus in the cat, J. Neurophysiol., 34 (1971) 453-466.
343
Representation of the complete retina in the contralateral superior colliculus of some mammals
J. H. KAAS*, J. K. HARTING AND R. W. GUILLERY
Laboratory of Neurophysiology and Department of Anatomy, University of Wisconsin, Madison, Wisc. 53706 (U.S.A.) (Accepted October 4th, 1973)
'Our data on the rat include one case, number 2, with a lesion restricted to the extreme temporal retina, entirely on the temporal side of the fixation point. In this case the great majority of the degenerated fibers are uncrossed. None of the crossed fibers can be seen to terminate in the lateral geniculate nucleus and certainly most of them pass over the nucleus and terminate in the lateral margin of the superior colliculus. The uncrossed fibers, on the other hand, all enter the lateral geniculate nucleus and terminate within its caudal third.' K. S. Lashley, 1934 (ref. 7), For many years investigators interested in the mammalian visual system have accepted the theory that both the lateral geniculate nucleus and the superior colliculus receive retinal input from only the contralateral hemifield (see refs. 3 and 5 for reviews). With the exception of a few degrees of visual field close to the vertical meridian 8, there is no reason to question this theory regarding the lateral geniculate nucleus. However, the organization of retinal input to the superior colliculus may need to be re-evaluated in the light of recent electrophysiological evidence. Such data indicate that part of the ipsilateral hemifield is represented in the superior colliculus of the squirrel 4, the tree shrew 4 and the domestic cat 1,6 (see ref. 5 for review). Thus, each colliculus represents the entire contralateral retina, including the temporal retinal expanse that is devoted to the hemifield ipsilateral to that colliculus. Two possible pathways may account for this representation of the temporal retina within the contralateral superior colliculus ~. The first is a direct pathway to the superior colliculus from the temporal retina of the contralateral eye. The second is a route from the temporal retina to the ipsilateral colliculus and then after a relay through the intertectal commissure to the contralateral colliculus. The latter, indirect pathway is unlikely in the squirrel and tree shrew since retinal input to the ipsilateral colliculus is quite sparse in both forms (unpublished data). Furthermore, the long neglected observation of Lashley 7 (see above) indicates the likelihood - - at least in some species - - of a direct pathway from the temporal retina to the contralateral superior colliculus. In order to test this latter possibility, small lesions were made along the temporal margin of the retina in 6 tree shrews (Tupaia glis) and 6 grey squirrels (Sciureus * Present address: Department of Psychology,Vanderbilt University, Nashville, Tenn. 37240, U.S.A.
344
SHORT COMMUNICATIONS
carolinensis). Following survival periods of 5-8 days the animals were killed, the brains removed, and frozen sections were stained for degenerating axons and their endings 2. The location of each lesion was recorded by direct observation of the flattened retina, and the normal eye was also examined for retinal damage. In 4 squirrels and 3 tree shrews the lesions appeared upon examination of the retina to involve only' the most temporal margin of the retina. In all 7 cases, degeneration was observed within the contralateral superior colliculus. Such degeneration was restricted to the superficial layers of the rostral and lateral regions of the colliculus (see Fig. 1). Thus, the degeneration occurred precisely where electrophysiological recordings have shown cells receiving inputs from the temporal retina 4. In addition, there were no other zones of tectal degeneration which might have suggested that the nasal retina had been damaged. Degeneration was also observed within the ipsilateral dorsal lateral geniculate of all 7 animals. In the tree shrews such degeneration was restricted to layers 1 and 5, with layer 5 receiving by far the densest input. The primary zone of degeneration within the squirrel's ipsilateral lateral geniculate was confined to layer 2. There was, however, one case in which degeneration was also observed within a portion of layer 3.
DORSAL
C A U D A L
Fig. 1. A parasagittal section of the superior colliculus. Degeneration is obvious within the rostral portion and has resulted from a large lesion involving the temporal retina of the contralateral eye. The boxed in area including the degeneration is shown at a higher magnification in the insert, l, -stratum griseum superficialis; 2, stratum opticum; 3, stratum griseum intermediates.
SHORT COMMUNICATIONS
345
Tempo~iNasal ~ Nucleus
/
Fig. 2. Schema of retinal projections to the dorsal lateral geniculate nucleus and the superior colliculus in tree shrews and squirrels. A pathway from the temporal retina to the ipsilateral superior colliculus was apparent only in one squirrel. Thus, for some mammals the primary projection from the temporal retina is to the contra-, not the ipsilateral superior colliculus. This is exactly the conclusion that Lashley, working on the rat, arrived at some 40 years ago 7. However, it was largely neglected since it did not fit current knowledge concerning the organization of the mammalian visual system. While we feel secure that our lesions did not cross the vertical meridian in any of our 7 critical animals, only two squirrels showed no degeneration at all in the contralateral lateral geniculate nucleus. In the remaining 2 squirrels and 3 tree shrews, there was a small fOCUS of degeneration within a small segment of the contralateral nucleus. These foci of degeneration were located in geniculate areas which do not receive retinal input from the region of the vertical meridian. Therefore, such degeneration could not have been produced by lesions that extended across the vertical meridian. In fact, several cases contained contralateral geniculate degeneration which was located within the monocular segment of the nucleus. We can only suggest that these foci of degeneration may (1) have resulted from our pulling on the optic nerve during surgerS,, (2) be the result of interruption of 'looping', retinofugal fibers, or (3) they may actually be terminals of axons arising within the temporal retina. None of these 5 animals showed a tectal focus of degeneration that would, oll the basis of known maps, correspond to a lesion of the nasal retina. The problem raised by these contralateral geniculate projections remains to be studied in detail. This investigation was supported by N I N D s Grants NS-06225, NS-06662, NS-05326, N S F Grant GB-36779 and Grant 135-4424 from the Graduate School, University of Wisconsin.
346
SHORT COMMUNICATIONS Fig. 2 was d r a w n by Ms. D . U r b a n . H i s t o l o g i c a l m a t e r i a l s w e r e p r e p a r e d by
Ms. J o a n E k l e b e r r y a n d Ms. B o n n i e Bade.
1 FELDON,S., FELDON, P., AND KRUGER, L., Topography of the retinal projection upon the superior colliculus of the cat, Vision Res., 10 (1970) 135-193. 2 FINK, R. P., AND HEIMER, L., TWO methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374. 3 KAAS, J. H., GUILEERY, R. W., AND AELMAN,J. M., Some principles of organization in the dorsal lateral geniculate nucleus, Brain Behav. Evol., 6 (1972) 253-299. 4 LANE, R. H., ALLMAN, J. M., AND KAAS, J. H., Representation of the visual field in the superior colliculus of the grey squirrel (Sciurus carolinensis) and the tree shrew (Tupaia glis), Brain Research, 26 (1971) 277-292. 5 LANE, R. H., ALLMAN,J. M., KAAS, J. H., AND MIEZIN, F. M., The visuotopic organization of the superior colliculus of the owl monkey (Aotus trivirgatus) and the bushbaby (Galago senegalensis), Brain Research, 60 (1973) 335-349. 6 LANE, R. H., KAAS, J. H. AND ALLMAN,J. M., Visuotopic organization of the superior colliculus in normal and Siamese cats, Brain Research, in press. 7 LASHLEY,K. S., The mechanism of vision : VII. The projection of the retina upon the primary optic centers in the rat, J. comp. Neurok, 59 (1934) 341-373. 8 SANDERSON,K. J., AND SHERMAN,S. M., Nasotemporal overlap in visual field projected to lateral geniculate nucleus in the cat, J. Neurophysiol., 34 (1971) 453-466.