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Thalamocortical interconnections of the visual system of the mink
Brain Research, 70 (1974) 139-143
139
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Short Communications
Thalamocortical interconnections of the visual system of the mink
K. J. S A N D E R S O N
AND
J. H. KAAS
Department of Anatomy, University of Wisconsin, Madison, Wisc. 53706 and Department of Psychology, Vanderbilt University, Nashville, Tenn. 37240 (U.S.A.) (Accepted January 3rd, 1974)
Recent investigations of the dorsal lateral geniculate nucleus of the mink, Mustela vison, have shown that there is a curious duplication of laminae A and A1 with the two A layers receiving contralateral input and the two A1 layers receiving ipsilateral input 11. Because of the duplication of layers A and A1, the mink has 4 well defined interlaminar zones in the lateral geniculate nucleus, two more than the cat has. In the cat both the A-A~ and A~-C interlaminar zones separate a contralateral layer from an ipsilateral layer, and both interlaminar zones receive a major input from corticogeniculate fibers 4, most of which are likely to carry binocular activity5. In the mink, the two extra interlaminar zones, A - A and A1-A1, lie between layers which receive input from the same eye. It thus seems possible that these 'monocular' interlaminar zones might receive a different input than the interlaminar zones which separate ipsilateral and contralateral layers and which appear to be particularly well placed to distribute the activity carried by the binocular corticogeniculate axons. The present report deals with interconnections between the lateral geniculate nucleus and the visual cortex in the mink. We aimed (1) to see whether the A - A and A1-A1 interlaminar zones in the lateral geniculate nucleus of the mink receive a different cortical projection than the A-A1 and A1-C interlaminar zones do and (2) to see if there was any difference between the two A layers (or the two A1 layers) with respect to their connections with the visual cortex. The experiments were carried out on fully pigmented mink, since previous investigations revealed abnormal retinogeniculate projections in mink with reduced eye pigmentation 12. The projections from the lateral geniculate nucleus to the cortex were traced using the retrograde cell degeneration method in 5 mink which had lesions placed by suction in one or both visual cortices. Following a postoperative survival of 48-54 days the mink were perfused with formol-saline. The brains were embedded in celloidin and serial 30/~m sections were stained with thionin. The thalamus was cut in the horizontal plane and the cortex was sectioned separately in either the frontal or horizontal plane. One additional mink received an injection of horseradish perox-
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72-166
73-74
Fig. 1. Line drawing of a mink brain, dorsal view, showing the locations of two cortical lesions.
idase (HRP) in one visual cortex and the geniculocortical projections were traced using the method of retrograde axonal transport of H R P as described by LaVail et al.S. Projections from the cortex to the thalamus were traced in 4 mink in which cortical lesions were placed and these were allowed to survive 4-7 days. The visual cortex was embedded in celloidin and serial 30 # m frontal sections were stained with thionin to show the lesion. The thalamus was cut frozen at 40 #m in the horizontal plane and a 1 in 5 series was stained with cresyl violet. Adjacent 1 in 5 series were stained according to the Nauta-Gygax 9 and Fink-Heimer 1 methods. Fig. 1 shows the cortical lesions in two o f the mink, 72-166 which had a 50 day survival time and 73-74 which survived 5 days postoperatively. Both of the lesions were in area 17 with some involvement o f area 18. In addition, there was some damage to the white matter. Placement of the lesions was aided by previous microelectrode recordings in two mink in which the border between the primary and secondary visual areas was determined from the pattern of visuotopic organization. The recording methods were similar to those used for cats 6. In Fig. 1 the dotted line in each hemisphere is an estimate of the 17/18 border derived both from the mapping and from an examination of the cytoarchitectonic structure of the cortex. Figs. 2 and 3 show the typical pattern of retrograde degeneration seen in the lateral geniculate nucleus after a cortical lesion with a long term survival (mink 72-166). The zone o f degeneration forms a wedge extending through the medial part of the duplicated A and A1 layers. The degeneration is most severe in the paired A laminae where there is marked cell shrinkage (compare Fig. 2 with Fig. 4). Degeneration in the paired A1 laminae is less marked and the degeneration in the C laminae, if any, is very mild. The paired A layers show equal amounts of degeneration, indicating, as expected, that the retinotopic organization of the two layers is the same (see Kaas et al.7). Similarly the degeneration is approximately the same in the paired A1 layers. There did not appear to be any cell shrinkage in the perigeniculate nucleus. The results obtained with H R P were in agreement with the retrograde degeneration studies. Following an injection of H R P into the striate cortex a column of
Fig. 2. Retrograde degeneration in the lateral geniculate nucleus after a lesion of the visual cortex in mink 72-166. Horizontal section; Nissl stain; x 37. Fig. 3. Line drawing of the section shown in Fig. 2. NPG, perigeniculate nucleus; MIN, medial interlaminar nucleus. Fig. 4. Horizontal section through the lateral geniculate nucleus of mink 72-166 on the non-lesioned side. Nissl stain; x 37. Compare this section with Fig. 2 which shows retrograde degeneration. Fig. 5. Anterograde degeneration in the lateral geniculate nucleus after a lesion of the visual cortex in mink 73-74. Horizontal section; Fink-Heimer; x 55. Note the dense degeneration in the interlaminar zones. Medial is to the left. Fig. 6. Higher power magnification of Fig. 5. The arrows in Figs. 5 and 6 indicate the same blood vessel, x 180.
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labeled cells was located in the lateral geniculate nucleus. Labeled cells were found in all layers o f the dorsal lateral geniculate nucleus. Fig. 5 shows the typical pattern o f anterograde degeneration seen in the lateral geniculate nucleus after a coltical lesion with a short term survival (mink 73-74). The degeneration forms a column extending through all layers of the nucleus with very dense degeneration in the interlaminar zones. The degeneration is composed of fine grains and was usually better demonstrated by the Fink-Heimer than the NautaGygax method. We interpret this as anterograde degeneration since (1) it is most dense in the interlaminar zones where there are no cells and (2) we did not see any retrograde cell degeneration in Nissl sections o f the lateral geniculate nucleus of mink 73-74. The degeneration is equally as dense in the A-A interlaminar zone as in the A-A1 interlaminar zone (see Fig. 6) indicating that there is no obvious difference between the cortical projections to these two kinds of interlaminar zones. The A-A interlaminar zone separates two contralateral layers and the A-A1 interlaminar zone separates a contralateral layer from an ipsilateral layer. As in the cat z,3,1°, anterograde degeneration is found in other brain stem structures after lesions of areas 17 and 18 o f the mink. Degeneration is found in the medial interlaminar nucleus, possibly as a result of extending the lesion from area 17 into area 18. There is a dense cortical projection to the perigeniculate nucleus, which is much better developed in the mink than in the catlL In addition, in the mink as in the cat2,3, ~0, there is a cortical projection to both the lateral posterior region of the thalamus and to the superior colliculus. While projections from the striate cortex to the ventral lateral geniculate nucleus have been described in the cat 1°, there was virtually no degeneration in the present anterograde cases in the mink. Since some of the lesions made for anterograde degeneration were similar to lesions made for retrograde degeneration (see Fig. 1), it could be seen that there are approximately reciprocal connections between the visual cortex and the lateral geniculate nucleus in the mink. Note that most o f our lesions involved area 18 as well as area 17. The results o f this study show no difference between the duplicated A layers (or A1 layers) with regard to their connections with the visual cortex. At the present therefore the significance o f the duplication of layers A and A~ in the mink must remain a mystery. More generally, the interlaminar zones, which show a particular concentration of corticogeniculate axon terminals in cat and mink, cannot be easily understood as zones that are primarily concerned with binocular interactions occurring between adjacent geniculate layers. We thank Dr. R. W. Guillery for comments on the manuscript. Some of the histological materials were prepared by Mrs. I. Lucey and Mrs. B. Yelk. Mrs. E. Langer provided valuable technical assistance. Supported by N.S.F. Grant, GB-36779 and by G~ants 5-R01-NS06662 and 5-R01-EY00962 from the NIH. Part of this work was completed while J. Kaas was at the Laboratory of Neurophysiology, University of Wisconsin and was supported by NINDS Grants NS-05326 and NS-06225.
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1 FINK, R.P., AND HEIMER, L., Two methods for selective silver impregnation of degenerating axons and their synaptic ends in the central nervous system, Brain Research, 4 (1968) 369-374. 2 GAREY,L. J., Interrelations of the visual cortex and superior colliculus in the cat, Nature (Lond.), 207 (1965) 1410-1411. 3 GUILLERY,R. W., Patterns of fiber degeneration in the dorsal lateral geniculate nucleus of the cat following lesions in visual cortex, J. comp. Neurol., 130 (1967) 197-222. 4 GUILLERY, R. W., Patterns of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat and monkey: a brief review, Vision Res., Suppl., 3 (1971) 211-227. 5 HUBEL, D. H., AND WIESEL, T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, J. PhysioL (Lond.), 160 (1962) 106-154. 6 KAAS, J. H., AND GUILLERY, R. W., The transfer of abnormal visual field representations from the dorsal lateral geniculate nucleus to the visual cortex in Siamese cats, Brain Research, 59 (1973) 61-95. 7 KAAS, J. H., GU1LLERY,R. W., AND ALLMAN,J. M., Some principles of organization in the dorsal lateral geniculate nucleus, Brain Behav. EvoL, 6 (1972) 253-299. 8 LAVAIL,J. H., WINSTON, K. R., AND TISH, A., A method based on retrograde intraaxonal transport of protein for identification of cell bodies of origin of axons terminating within the CNS, Brain Research, 58 (1973)470-477. 9 NAUTA, W. J. H., AND GYGAX, P. A., Silver impregnation of degenerating axons in the central nervous system. A modified technic, Stain Technol., 29 (1954) 91-93. 10 NIIM1, K., KAWAMURA,S., AND |SHIMARU,S., Projections of the visual cortex to the lateral geniculate and posterior thalamic nuclei in the cat, J. eomp. Neurol., 143 (1971) 279-312. 11 SANDERSON,K. J., Lamination of the dorsal lateral geniculate nucleus in carnivores of the weasel (Mustelidae), raccoon (Procyonidae) and fox (Canidae) families, J. comp. Neurol., (1974) in press. 12 SANDERSON,K.J., GUILLERY, R. W., AND SHACKELFORD,R. i . , Congenitally abnormal visual pathways in mink with reduced retinal pigment, J. comp. NeuroL, (1974) in press.
139
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Short Communications
Thalamocortical interconnections of the visual system of the mink
K. J. S A N D E R S O N
AND
J. H. KAAS
Department of Anatomy, University of Wisconsin, Madison, Wisc. 53706 and Department of Psychology, Vanderbilt University, Nashville, Tenn. 37240 (U.S.A.) (Accepted January 3rd, 1974)
Recent investigations of the dorsal lateral geniculate nucleus of the mink, Mustela vison, have shown that there is a curious duplication of laminae A and A1 with the two A layers receiving contralateral input and the two A1 layers receiving ipsilateral input 11. Because of the duplication of layers A and A1, the mink has 4 well defined interlaminar zones in the lateral geniculate nucleus, two more than the cat has. In the cat both the A-A~ and A~-C interlaminar zones separate a contralateral layer from an ipsilateral layer, and both interlaminar zones receive a major input from corticogeniculate fibers 4, most of which are likely to carry binocular activity5. In the mink, the two extra interlaminar zones, A - A and A1-A1, lie between layers which receive input from the same eye. It thus seems possible that these 'monocular' interlaminar zones might receive a different input than the interlaminar zones which separate ipsilateral and contralateral layers and which appear to be particularly well placed to distribute the activity carried by the binocular corticogeniculate axons. The present report deals with interconnections between the lateral geniculate nucleus and the visual cortex in the mink. We aimed (1) to see whether the A - A and A1-A1 interlaminar zones in the lateral geniculate nucleus of the mink receive a different cortical projection than the A-A1 and A1-C interlaminar zones do and (2) to see if there was any difference between the two A layers (or the two A1 layers) with respect to their connections with the visual cortex. The experiments were carried out on fully pigmented mink, since previous investigations revealed abnormal retinogeniculate projections in mink with reduced eye pigmentation 12. The projections from the lateral geniculate nucleus to the cortex were traced using the retrograde cell degeneration method in 5 mink which had lesions placed by suction in one or both visual cortices. Following a postoperative survival of 48-54 days the mink were perfused with formol-saline. The brains were embedded in celloidin and serial 30/~m sections were stained with thionin. The thalamus was cut in the horizontal plane and the cortex was sectioned separately in either the frontal or horizontal plane. One additional mink received an injection of horseradish perox-
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72-166
73-74
Fig. 1. Line drawing of a mink brain, dorsal view, showing the locations of two cortical lesions.
idase (HRP) in one visual cortex and the geniculocortical projections were traced using the method of retrograde axonal transport of H R P as described by LaVail et al.S. Projections from the cortex to the thalamus were traced in 4 mink in which cortical lesions were placed and these were allowed to survive 4-7 days. The visual cortex was embedded in celloidin and serial 30 # m frontal sections were stained with thionin to show the lesion. The thalamus was cut frozen at 40 #m in the horizontal plane and a 1 in 5 series was stained with cresyl violet. Adjacent 1 in 5 series were stained according to the Nauta-Gygax 9 and Fink-Heimer 1 methods. Fig. 1 shows the cortical lesions in two o f the mink, 72-166 which had a 50 day survival time and 73-74 which survived 5 days postoperatively. Both of the lesions were in area 17 with some involvement o f area 18. In addition, there was some damage to the white matter. Placement of the lesions was aided by previous microelectrode recordings in two mink in which the border between the primary and secondary visual areas was determined from the pattern of visuotopic organization. The recording methods were similar to those used for cats 6. In Fig. 1 the dotted line in each hemisphere is an estimate of the 17/18 border derived both from the mapping and from an examination of the cytoarchitectonic structure of the cortex. Figs. 2 and 3 show the typical pattern of retrograde degeneration seen in the lateral geniculate nucleus after a cortical lesion with a long term survival (mink 72-166). The zone o f degeneration forms a wedge extending through the medial part of the duplicated A and A1 layers. The degeneration is most severe in the paired A laminae where there is marked cell shrinkage (compare Fig. 2 with Fig. 4). Degeneration in the paired A1 laminae is less marked and the degeneration in the C laminae, if any, is very mild. The paired A layers show equal amounts of degeneration, indicating, as expected, that the retinotopic organization of the two layers is the same (see Kaas et al.7). Similarly the degeneration is approximately the same in the paired A1 layers. There did not appear to be any cell shrinkage in the perigeniculate nucleus. The results obtained with H R P were in agreement with the retrograde degeneration studies. Following an injection of H R P into the striate cortex a column of
Fig. 2. Retrograde degeneration in the lateral geniculate nucleus after a lesion of the visual cortex in mink 72-166. Horizontal section; Nissl stain; x 37. Fig. 3. Line drawing of the section shown in Fig. 2. NPG, perigeniculate nucleus; MIN, medial interlaminar nucleus. Fig. 4. Horizontal section through the lateral geniculate nucleus of mink 72-166 on the non-lesioned side. Nissl stain; x 37. Compare this section with Fig. 2 which shows retrograde degeneration. Fig. 5. Anterograde degeneration in the lateral geniculate nucleus after a lesion of the visual cortex in mink 73-74. Horizontal section; Fink-Heimer; x 55. Note the dense degeneration in the interlaminar zones. Medial is to the left. Fig. 6. Higher power magnification of Fig. 5. The arrows in Figs. 5 and 6 indicate the same blood vessel, x 180.
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labeled cells was located in the lateral geniculate nucleus. Labeled cells were found in all layers o f the dorsal lateral geniculate nucleus. Fig. 5 shows the typical pattern o f anterograde degeneration seen in the lateral geniculate nucleus after a coltical lesion with a short term survival (mink 73-74). The degeneration forms a column extending through all layers of the nucleus with very dense degeneration in the interlaminar zones. The degeneration is composed of fine grains and was usually better demonstrated by the Fink-Heimer than the NautaGygax method. We interpret this as anterograde degeneration since (1) it is most dense in the interlaminar zones where there are no cells and (2) we did not see any retrograde cell degeneration in Nissl sections o f the lateral geniculate nucleus of mink 73-74. The degeneration is equally as dense in the A-A interlaminar zone as in the A-A1 interlaminar zone (see Fig. 6) indicating that there is no obvious difference between the cortical projections to these two kinds of interlaminar zones. The A-A interlaminar zone separates two contralateral layers and the A-A1 interlaminar zone separates a contralateral layer from an ipsilateral layer. As in the cat z,3,1°, anterograde degeneration is found in other brain stem structures after lesions of areas 17 and 18 o f the mink. Degeneration is found in the medial interlaminar nucleus, possibly as a result of extending the lesion from area 17 into area 18. There is a dense cortical projection to the perigeniculate nucleus, which is much better developed in the mink than in the catlL In addition, in the mink as in the cat2,3, ~0, there is a cortical projection to both the lateral posterior region of the thalamus and to the superior colliculus. While projections from the striate cortex to the ventral lateral geniculate nucleus have been described in the cat 1°, there was virtually no degeneration in the present anterograde cases in the mink. Since some of the lesions made for anterograde degeneration were similar to lesions made for retrograde degeneration (see Fig. 1), it could be seen that there are approximately reciprocal connections between the visual cortex and the lateral geniculate nucleus in the mink. Note that most o f our lesions involved area 18 as well as area 17. The results o f this study show no difference between the duplicated A layers (or A1 layers) with regard to their connections with the visual cortex. At the present therefore the significance o f the duplication of layers A and A~ in the mink must remain a mystery. More generally, the interlaminar zones, which show a particular concentration of corticogeniculate axon terminals in cat and mink, cannot be easily understood as zones that are primarily concerned with binocular interactions occurring between adjacent geniculate layers. We thank Dr. R. W. Guillery for comments on the manuscript. Some of the histological materials were prepared by Mrs. I. Lucey and Mrs. B. Yelk. Mrs. E. Langer provided valuable technical assistance. Supported by N.S.F. Grant, GB-36779 and by G~ants 5-R01-NS06662 and 5-R01-EY00962 from the NIH. Part of this work was completed while J. Kaas was at the Laboratory of Neurophysiology, University of Wisconsin and was supported by NINDS Grants NS-05326 and NS-06225.
SHORT COMMUNICATIONS
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1 FINK, R.P., AND HEIMER, L., Two methods for selective silver impregnation of degenerating axons and their synaptic ends in the central nervous system, Brain Research, 4 (1968) 369-374. 2 GAREY,L. J., Interrelations of the visual cortex and superior colliculus in the cat, Nature (Lond.), 207 (1965) 1410-1411. 3 GUILLERY,R. W., Patterns of fiber degeneration in the dorsal lateral geniculate nucleus of the cat following lesions in visual cortex, J. comp. Neurol., 130 (1967) 197-222. 4 GUILLERY, R. W., Patterns of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat and monkey: a brief review, Vision Res., Suppl., 3 (1971) 211-227. 5 HUBEL, D. H., AND WIESEL, T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, J. PhysioL (Lond.), 160 (1962) 106-154. 6 KAAS, J. H., AND GUILLERY, R. W., The transfer of abnormal visual field representations from the dorsal lateral geniculate nucleus to the visual cortex in Siamese cats, Brain Research, 59 (1973) 61-95. 7 KAAS, J. H., GU1LLERY,R. W., AND ALLMAN,J. M., Some principles of organization in the dorsal lateral geniculate nucleus, Brain Behav. EvoL, 6 (1972) 253-299. 8 LAVAIL,J. H., WINSTON, K. R., AND TISH, A., A method based on retrograde intraaxonal transport of protein for identification of cell bodies of origin of axons terminating within the CNS, Brain Research, 58 (1973)470-477. 9 NAUTA, W. J. H., AND GYGAX, P. A., Silver impregnation of degenerating axons in the central nervous system. A modified technic, Stain Technol., 29 (1954) 91-93. 10 NIIM1, K., KAWAMURA,S., AND |SHIMARU,S., Projections of the visual cortex to the lateral geniculate and posterior thalamic nuclei in the cat, J. eomp. Neurol., 143 (1971) 279-312. 11 SANDERSON,K. J., Lamination of the dorsal lateral geniculate nucleus in carnivores of the weasel (Mustelidae), raccoon (Procyonidae) and fox (Canidae) families, J. comp. Neurol., (1974) in press. 12 SANDERSON,K.J., GUILLERY, R. W., AND SHACKELFORD,R. i . , Congenitally abnormal visual pathways in mink with reduced retinal pigment, J. comp. NeuroL, (1974) in press.