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Demonstration of ocular dominance columns in Nissl-stained sections of monkey visual cortex following enucleation
Brain Research, 176 (1979) 153-158 © Elsevier/North-Holland Biomedical Press
153
Demonstration of ocular dominance columns in Nissl-stained sections of monkey visual cortex following enucleation
E. C. HASELTINE, E. J. DeBRUYN, and V. A. CASAGRANDE Departments of ,4natomy and Psychology, I/anderbilt University, Nashville, Tenn. 37232 (U.S.A.)
(Accepted July 5th, 1979)
It is well known that eye removal in mammals can cause marked anterograde transneuronal changes, even in adults (for review see3,9). The best documented change of this type has been reported for the lateral geniculate nucleus (LGN) of primates where deprived cells consistently show marked shrinkage and pallor 6,16,17,19. More subtle secondary transneuronal effects of enucleation have also been reported for visual cortex 4,5,7,8,18. These include cell loss, loss of dendritic spines and changes in cell pacl~ing density and size. Unfortunately, no systematic effort has been made to relate secondary transneuronal consequences of enucleation to the primary changes that occur in the LGN. Moreover, the effects of enucleation upon visual cortex have not yet been quantified. We chose to study the macaque monkey in order to understand the relationship between the geniculate and cortical effects of enucleation because changes that occur in the L G N following eye removal are more dramatic in primates than in other species. Furthermore, in macaques, there is a well defined relationship between the segregation of ocular inputs in the L G N and the visual cortex, so that correlations can be made between changes in different ocular dominance columns and changes in the geniculate laminae projecting to these columns13-15, 20. Finally, there exists only one study of the effects of eye removal on the visual cortex of adult primates 4. In our study, we addressed 3 questions concerning the cortical effects of enucleation: (1) do neurons in enucleated LGN laminae lose their cortical connections? (2) can perikaryal changes of the type found in the L G N be demonstrated in striate cortex ? and (3) if such perikaryal changes are present, what is their relationship to the pattern of geniculostriate connections (i.e. ocular dominance columns)? Two adult cynomolgus monkeys were used in this study. One served as a normal control, while the other animal had its right eye removed. Following a period of 29 months, 2 #1 of 30 ~o horseradish peroxidase (HRP, Sigma type IX) in saline was injected into the posterior poles of both striate cortices of the enucleated animal, and 500 #Ci of [3H]proline (spec. act. 22.1 Ci/mmol) was injected into the remaining eye. Two days later, the monkey was perfused with saline followed by 2 ~ buffered paraformaldehyde and the brain was cut frozen at 30/zm. Appropriate sections were
154
Fig. 1. A: frontal section of the LGN ipsilateral to the enucleation. Cells in layers 2, 3 and 5 display pronounced atrophy. B: L G N contralateral to the enucleation. In this section, layers 1, 4 and 6 are deprived. C: L G N contralateral to the enucleation : label from the cortical HRP injection is evident in layers 2, 3, 4 and 5. D : higher power photomicrograph of C. Layers are indicated by numerals; layer 4 is deprived. See text for details.
155
Fig. 2. Photomicrographs of Nissl-stained frontal sections of striate cortex in our normal monkey (A,C), and ipsilateral (B,D,F,) and contralateral (E) to the enucleation in our deprived monkey. Adjacent photographs show comparable cortical regions. Note the marked banding in layer IV (with hints of banding in IIIB and VI). Also note that the banding stops abruptly at the 17/18 border (D). Our own investigations into cortical lamination in primates have led us to adopt the scheme of Hassler and Wagner 1~. For comparison, we have included Brodmann's 1 scheme which is indicated in parentheses. I (I); I[ (I1); IrlA (III); IIIB OVA); IIIC (IVB); IV (IVCa, [VC/3), V (V); VI (VI). processed for a u t o r a d i o g r a p h y , r e a c t e d with d i a m i n o b e n z i d i n e o r t e t r a m e t h y l b e n z i dine, o r s t a i n e d with cresyl violet. Cell m e a s u r e m e n t s in t h e L G N o f the enucleated m o n k e y were m a d e by d r a w i n g
156 the outlines of all perikarya within a 10,000 sq. ktm area at 1000 × with the aid of a Zeiss camera lucida attachment; cell areas were determined using an electronic planimeter. Measurements were taken within corresponding points of all geniculate laminae in both hemispheres according to previously described methods TM. The percentage of L G N cells labelled following the cortical injections was determined by assessing the number of cells containing reaction product within a 10,000 sq./~m area in the zone of densest label in each layer. Cell measurements in striate cortex were made as described for the LGN, and packing density was determined by counting the number of neurons within a 10,000 sq. #m area in adjacent deprived and non-deprived regions of layer IV. Examination of the L G N in the enucleated monkey revealed a marked shrinkage of cells in the deprived laminae (Fig. 1A and B); differences in mean perikaryal sizes between denervated and normally innervated laminae ranged from 39 To to 53 ~ (see Table I). The magnitude of the effect was the same for magnocellular and parvocellular laminae and for laminae innervated by opposite eyes. Despite the dramatic changes in cell size, the percentage of HRP-labelled cells within the areas of most dense label was 90-95 ~ in both deprived and non-deprived layers, although the total area of label was considerably larger in the non-deprived laminae (Fig. 1C and D). Since our autoradiographic results showed no evidence of redistribution ofretinogeniculate axons from the remaining eye, these results suggest that denervated adult L G N cells can maintain connections with cortex despite long-term absence of retinal input. Our most striking finding was seen in Nissl-stained sections of striate cortex of the enucleated monkey. Unlike the homogeneous appearance of layer IV in striate cortex in the normal monkey (Fig. 2A, C), layer IV of the enucleated monkey was comprised of alternating light and dark bands of equal width (Fig. 2B, D, E, F). We believe this banding pattern represents ocular dominance columns because it is most pronounced in layer IV of striate cortex, and because the widths of the light and dark bands (300-500 /~m) are approximately the same as those of ocular dominance columns described by other investigators la,2°. Cell measurements at the base of layer IV in adjacent light and dark bands demonstrated that cells in the dark bands were 20 ~-30 ~ more tightly packed and 7 14 ~ smaller in area (mean 31.4/,2 i 0.61) than their counterparts in the lighter bands (mean 34.8/z2 ± 0.89; P < 0.01, one-tailed t-test). Because the cells overlapped more in the dark bands, it was not possible to determine if individual cells in the dark bands were also more heavily stained. We believe that dark bands represent the enucleated eye because: (1) the shrinkage in the dark columns was consistant with the other secondary transneuronal changes reported following enucleation, such as reduction in the number of dendritesT; (2) Cragg 5 has shown in cats that bilateral optic nerve crush leads to results identical to ours, namely cell shrinkage and an increase in cell packing density; (3) the increase in packing density has also been found following lid suture in both squirrels and catsS,10; and (4) inspection of the monocular segments of visual cortex of the enucleated monkey revealed that the deprived segment was darker than its normally
157 TABLE I Perikaryal sizes in the dorsal lateral geniculate nucleus of macaque 79-2 (29 month enucleation)
Measurements taken from deprived layers are indicated by an asterisk. All laminar differences are significant (P < 0.01, one-tailed t-test for related samples). In all layers, n = 25 except 1 (n = 24 ±psi); 3 (n = 23 contra); 5 (n = 27 ±psi, 26 contra). Values are means in sq./~m + S.E. Layer
Contralateral to suture
Ipsilateral to suture
~ Difference
1 2 3 4 5 6
148.9 + 280.7 4166.1 490.4 4, 162.6 480.6 q-
314.6 ± 154.3 ± 89.2 4. 147.1 4. 84.2 4, 131.6 4.
52.6 45.0 46.2 38.5 48.2 38.7
6.1" 17.1 9.0 4.7* 7.9 4.2*
15.6 10.2" 4.4* 6.5 3.5* 8.6
i n n e r v a t e d counterpart. N o such assymetry was noticed in the n o r m a l monkey. I n s u m m a r y , we have presented evidence i n an adult m a c a q u e that L G N n e u r o n s in deprived l a m i n a e m a i n t a i n at least some of their cortical connections, b u t that these c o n n e c t i o n s are i n a d e q u a t e to sustain n o r m a l perikaryal size of layer IV cells. The cell shrinkage a n d increased packing density of layer IV neurons, like changes observed in the L G N , a p p e a r to be restricted to regions subserved by the enucleated eye. This work was supported by G r a n t s EY-07007 (E.C.H.), I T 3 2 - M H 1 5 4 5 2 (E.J.D.), a n d EY-01778 a n d I K07 EY-00061 (V.A.C.). We t h a n k the following individuals for their assistance i n various phases of this project: Dr. V a u g h n Allen, Mr. G a r y Novack, Ms. Elizabeth Birecree, Ms. R u t h Lennek, a n d Dr. J o n Kaas.
1 Brodmann, K., I/ergleichende Lokalisations lehre der Grosshirnrinde in ihren Prinzipiel dargestellt aufGrund des Zellen baues, Verlag J. A. Barth, Leipzig, 1909 pp. 1-324. 2 Casagrande, V. A., Guillery, R. W., and Harting, J. K., Differential effects of monocular deprivation seen in different layers of the lateral geniculate nucleus, J. comp. Neurol., 179 (1978) 469-486. 3 Cowan, W. M., Anterograde and retrograde transneuronal degeneration in the central and peripheral nervous system. In W. J. Nauta and S. O. E. Ebbesson (Eds.), Contemporary Research Methods in Neuroanatomy, Springer-Verlag, New York, 1970 pp. 217-251. 4 Cragg, B. G., The fate of axon terminals in visual cortex during transsynaptic atrophy of the lateral geniculate nucleus, Brain Research, 34 (1971) 53-60. 5 Cragg, B. G., The development of synapses in kitten visual cortex during visual deprivation, Exp. Neurol., 46 (1975) 445--451. 6 Glees, P. and LeGros Clark, W. E., The termination of optic fibers in the lateral geniculate body of the monkey. J. Anat. (Lond.), 75 (1941) 295-308. 7 Globus, A. and Scheibel, A. B., Loss of dendritic spines as an index of presynaptic terminal patterns: an experimental application of the Golgi method, Nature (Lond.), 212 (1966) 463-465. 8 Globus, A. and Scheibel, A. B., The effect of visual deprivation on cortical neurons: a Golgi study, Exp. NeuroL, 19 (1967) 331-345. 9 Guillery, R. W., On structural changes that can be produced experimentally in the mammalian visual pathways. In R. Bellairs and E. G. Gray (Eds.), Essays on the Nervous System, A Festschrift for Professor J. Z. Young, Clarendon Press, Oxford, 1974 pp. 299-326. 10 Guillery, R. W. and Kaas, J., The effects of monocular lid suture on the development of the visual
158 cortex in squirrels (Sciureus carolinensis), J. comp. Neurol., 154 (1974) 443-452. 11 Guillery, R. W. and Stelzner, D. J., The differential effects of unilateral lid closure upon the binocular and monocular segments of the dorsal lateral geniculate nucleus in the cat, J. comp. Neurol., 139 (1970) 413-422. 12 Hassler, R. and Wagner, A., Experimentelle und morphologische befunde uber die vierfachecorticale projektion des visuellen systems, Proc. 8th int. Congr. NeuroL ( Wein), vol. III, 1965, pp. 77-96. 13 Hubel, D. H. and Wiesel, T. N., Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey, J. romp. Neurol., 146 (1972) 421-450. 14 Hubel, D. H., Wiesel, T. N. and LeVay, S., Functional architecture of area 17 in normal and monocularly deprived macaque monkeys, Cold Spr. Harb. Syrup. quant. Biol., 40 (1976) 581-589. 15 Hubel, D. H., Wiesel, T. N. and LeVay, S., Plasticity of ocular dominance columns in monkey striate cortex, Phil. Trans. B, 278 (1977) 377-411. 16 Kupfer, C., The distribution of cell size in the lateral geniculate nucleus of man following transneuronal cell atrophy, J. Neuropath. exp. NeuroL 24 (1965) 653-661. 17 Kupfer, C. and Downer, J. L., Ribonucleic acid content and metabolic activity of lateral geniculate nucleus in monkey following afferent denervation, J. Neurochem., 14 (1967) 257-263. 18 Lindner, 1. and Umrath, K., Veranderungen der sehspare 1 und II in ihrem monocularen und binocularen teil nach extirlzation eines augen beim kaninchen, D. Z. Nervheik, 172 (1955) 495-525. 19 Mathews, M. R., Cowen, W. M. and Powell, T. P. S., Transneuronal cell degeneration in the lateral geniculate nucleus of tile macaque monkey, J. Anat. (Land.), 94 (1960) 145 169. 20 Wiesel, T. N., Hubel, D. H. and Lam, D. N. K., Autoradiographic demonstration of ocular dominance columns in monkey striate cortex by means of transneuronal transport, Brain Research, 79 (1974) 273-279.
153
Demonstration of ocular dominance columns in Nissl-stained sections of monkey visual cortex following enucleation
E. C. HASELTINE, E. J. DeBRUYN, and V. A. CASAGRANDE Departments of ,4natomy and Psychology, I/anderbilt University, Nashville, Tenn. 37232 (U.S.A.)
(Accepted July 5th, 1979)
It is well known that eye removal in mammals can cause marked anterograde transneuronal changes, even in adults (for review see3,9). The best documented change of this type has been reported for the lateral geniculate nucleus (LGN) of primates where deprived cells consistently show marked shrinkage and pallor 6,16,17,19. More subtle secondary transneuronal effects of enucleation have also been reported for visual cortex 4,5,7,8,18. These include cell loss, loss of dendritic spines and changes in cell pacl~ing density and size. Unfortunately, no systematic effort has been made to relate secondary transneuronal consequences of enucleation to the primary changes that occur in the LGN. Moreover, the effects of enucleation upon visual cortex have not yet been quantified. We chose to study the macaque monkey in order to understand the relationship between the geniculate and cortical effects of enucleation because changes that occur in the L G N following eye removal are more dramatic in primates than in other species. Furthermore, in macaques, there is a well defined relationship between the segregation of ocular inputs in the L G N and the visual cortex, so that correlations can be made between changes in different ocular dominance columns and changes in the geniculate laminae projecting to these columns13-15, 20. Finally, there exists only one study of the effects of eye removal on the visual cortex of adult primates 4. In our study, we addressed 3 questions concerning the cortical effects of enucleation: (1) do neurons in enucleated LGN laminae lose their cortical connections? (2) can perikaryal changes of the type found in the L G N be demonstrated in striate cortex ? and (3) if such perikaryal changes are present, what is their relationship to the pattern of geniculostriate connections (i.e. ocular dominance columns)? Two adult cynomolgus monkeys were used in this study. One served as a normal control, while the other animal had its right eye removed. Following a period of 29 months, 2 #1 of 30 ~o horseradish peroxidase (HRP, Sigma type IX) in saline was injected into the posterior poles of both striate cortices of the enucleated animal, and 500 #Ci of [3H]proline (spec. act. 22.1 Ci/mmol) was injected into the remaining eye. Two days later, the monkey was perfused with saline followed by 2 ~ buffered paraformaldehyde and the brain was cut frozen at 30/zm. Appropriate sections were
154
Fig. 1. A: frontal section of the LGN ipsilateral to the enucleation. Cells in layers 2, 3 and 5 display pronounced atrophy. B: L G N contralateral to the enucleation. In this section, layers 1, 4 and 6 are deprived. C: L G N contralateral to the enucleation : label from the cortical HRP injection is evident in layers 2, 3, 4 and 5. D : higher power photomicrograph of C. Layers are indicated by numerals; layer 4 is deprived. See text for details.
155
Fig. 2. Photomicrographs of Nissl-stained frontal sections of striate cortex in our normal monkey (A,C), and ipsilateral (B,D,F,) and contralateral (E) to the enucleation in our deprived monkey. Adjacent photographs show comparable cortical regions. Note the marked banding in layer IV (with hints of banding in IIIB and VI). Also note that the banding stops abruptly at the 17/18 border (D). Our own investigations into cortical lamination in primates have led us to adopt the scheme of Hassler and Wagner 1~. For comparison, we have included Brodmann's 1 scheme which is indicated in parentheses. I (I); I[ (I1); IrlA (III); IIIB OVA); IIIC (IVB); IV (IVCa, [VC/3), V (V); VI (VI). processed for a u t o r a d i o g r a p h y , r e a c t e d with d i a m i n o b e n z i d i n e o r t e t r a m e t h y l b e n z i dine, o r s t a i n e d with cresyl violet. Cell m e a s u r e m e n t s in t h e L G N o f the enucleated m o n k e y were m a d e by d r a w i n g
156 the outlines of all perikarya within a 10,000 sq. ktm area at 1000 × with the aid of a Zeiss camera lucida attachment; cell areas were determined using an electronic planimeter. Measurements were taken within corresponding points of all geniculate laminae in both hemispheres according to previously described methods TM. The percentage of L G N cells labelled following the cortical injections was determined by assessing the number of cells containing reaction product within a 10,000 sq./~m area in the zone of densest label in each layer. Cell measurements in striate cortex were made as described for the LGN, and packing density was determined by counting the number of neurons within a 10,000 sq. #m area in adjacent deprived and non-deprived regions of layer IV. Examination of the L G N in the enucleated monkey revealed a marked shrinkage of cells in the deprived laminae (Fig. 1A and B); differences in mean perikaryal sizes between denervated and normally innervated laminae ranged from 39 To to 53 ~ (see Table I). The magnitude of the effect was the same for magnocellular and parvocellular laminae and for laminae innervated by opposite eyes. Despite the dramatic changes in cell size, the percentage of HRP-labelled cells within the areas of most dense label was 90-95 ~ in both deprived and non-deprived layers, although the total area of label was considerably larger in the non-deprived laminae (Fig. 1C and D). Since our autoradiographic results showed no evidence of redistribution ofretinogeniculate axons from the remaining eye, these results suggest that denervated adult L G N cells can maintain connections with cortex despite long-term absence of retinal input. Our most striking finding was seen in Nissl-stained sections of striate cortex of the enucleated monkey. Unlike the homogeneous appearance of layer IV in striate cortex in the normal monkey (Fig. 2A, C), layer IV of the enucleated monkey was comprised of alternating light and dark bands of equal width (Fig. 2B, D, E, F). We believe this banding pattern represents ocular dominance columns because it is most pronounced in layer IV of striate cortex, and because the widths of the light and dark bands (300-500 /~m) are approximately the same as those of ocular dominance columns described by other investigators la,2°. Cell measurements at the base of layer IV in adjacent light and dark bands demonstrated that cells in the dark bands were 20 ~-30 ~ more tightly packed and 7 14 ~ smaller in area (mean 31.4/,2 i 0.61) than their counterparts in the lighter bands (mean 34.8/z2 ± 0.89; P < 0.01, one-tailed t-test). Because the cells overlapped more in the dark bands, it was not possible to determine if individual cells in the dark bands were also more heavily stained. We believe that dark bands represent the enucleated eye because: (1) the shrinkage in the dark columns was consistant with the other secondary transneuronal changes reported following enucleation, such as reduction in the number of dendritesT; (2) Cragg 5 has shown in cats that bilateral optic nerve crush leads to results identical to ours, namely cell shrinkage and an increase in cell packing density; (3) the increase in packing density has also been found following lid suture in both squirrels and catsS,10; and (4) inspection of the monocular segments of visual cortex of the enucleated monkey revealed that the deprived segment was darker than its normally
157 TABLE I Perikaryal sizes in the dorsal lateral geniculate nucleus of macaque 79-2 (29 month enucleation)
Measurements taken from deprived layers are indicated by an asterisk. All laminar differences are significant (P < 0.01, one-tailed t-test for related samples). In all layers, n = 25 except 1 (n = 24 ±psi); 3 (n = 23 contra); 5 (n = 27 ±psi, 26 contra). Values are means in sq./~m + S.E. Layer
Contralateral to suture
Ipsilateral to suture
~ Difference
1 2 3 4 5 6
148.9 + 280.7 4166.1 490.4 4, 162.6 480.6 q-
314.6 ± 154.3 ± 89.2 4. 147.1 4. 84.2 4, 131.6 4.
52.6 45.0 46.2 38.5 48.2 38.7
6.1" 17.1 9.0 4.7* 7.9 4.2*
15.6 10.2" 4.4* 6.5 3.5* 8.6
i n n e r v a t e d counterpart. N o such assymetry was noticed in the n o r m a l monkey. I n s u m m a r y , we have presented evidence i n an adult m a c a q u e that L G N n e u r o n s in deprived l a m i n a e m a i n t a i n at least some of their cortical connections, b u t that these c o n n e c t i o n s are i n a d e q u a t e to sustain n o r m a l perikaryal size of layer IV cells. The cell shrinkage a n d increased packing density of layer IV neurons, like changes observed in the L G N , a p p e a r to be restricted to regions subserved by the enucleated eye. This work was supported by G r a n t s EY-07007 (E.C.H.), I T 3 2 - M H 1 5 4 5 2 (E.J.D.), a n d EY-01778 a n d I K07 EY-00061 (V.A.C.). We t h a n k the following individuals for their assistance i n various phases of this project: Dr. V a u g h n Allen, Mr. G a r y Novack, Ms. Elizabeth Birecree, Ms. R u t h Lennek, a n d Dr. J o n Kaas.
1 Brodmann, K., I/ergleichende Lokalisations lehre der Grosshirnrinde in ihren Prinzipiel dargestellt aufGrund des Zellen baues, Verlag J. A. Barth, Leipzig, 1909 pp. 1-324. 2 Casagrande, V. A., Guillery, R. W., and Harting, J. K., Differential effects of monocular deprivation seen in different layers of the lateral geniculate nucleus, J. comp. Neurol., 179 (1978) 469-486. 3 Cowan, W. M., Anterograde and retrograde transneuronal degeneration in the central and peripheral nervous system. In W. J. Nauta and S. O. E. Ebbesson (Eds.), Contemporary Research Methods in Neuroanatomy, Springer-Verlag, New York, 1970 pp. 217-251. 4 Cragg, B. G., The fate of axon terminals in visual cortex during transsynaptic atrophy of the lateral geniculate nucleus, Brain Research, 34 (1971) 53-60. 5 Cragg, B. G., The development of synapses in kitten visual cortex during visual deprivation, Exp. Neurol., 46 (1975) 445--451. 6 Glees, P. and LeGros Clark, W. E., The termination of optic fibers in the lateral geniculate body of the monkey. J. Anat. (Lond.), 75 (1941) 295-308. 7 Globus, A. and Scheibel, A. B., Loss of dendritic spines as an index of presynaptic terminal patterns: an experimental application of the Golgi method, Nature (Lond.), 212 (1966) 463-465. 8 Globus, A. and Scheibel, A. B., The effect of visual deprivation on cortical neurons: a Golgi study, Exp. NeuroL, 19 (1967) 331-345. 9 Guillery, R. W., On structural changes that can be produced experimentally in the mammalian visual pathways. In R. Bellairs and E. G. Gray (Eds.), Essays on the Nervous System, A Festschrift for Professor J. Z. Young, Clarendon Press, Oxford, 1974 pp. 299-326. 10 Guillery, R. W. and Kaas, J., The effects of monocular lid suture on the development of the visual
158 cortex in squirrels (Sciureus carolinensis), J. comp. Neurol., 154 (1974) 443-452. 11 Guillery, R. W. and Stelzner, D. J., The differential effects of unilateral lid closure upon the binocular and monocular segments of the dorsal lateral geniculate nucleus in the cat, J. comp. Neurol., 139 (1970) 413-422. 12 Hassler, R. and Wagner, A., Experimentelle und morphologische befunde uber die vierfachecorticale projektion des visuellen systems, Proc. 8th int. Congr. NeuroL ( Wein), vol. III, 1965, pp. 77-96. 13 Hubel, D. H. and Wiesel, T. N., Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey, J. romp. Neurol., 146 (1972) 421-450. 14 Hubel, D. H., Wiesel, T. N. and LeVay, S., Functional architecture of area 17 in normal and monocularly deprived macaque monkeys, Cold Spr. Harb. Syrup. quant. Biol., 40 (1976) 581-589. 15 Hubel, D. H., Wiesel, T. N. and LeVay, S., Plasticity of ocular dominance columns in monkey striate cortex, Phil. Trans. B, 278 (1977) 377-411. 16 Kupfer, C., The distribution of cell size in the lateral geniculate nucleus of man following transneuronal cell atrophy, J. Neuropath. exp. NeuroL 24 (1965) 653-661. 17 Kupfer, C. and Downer, J. L., Ribonucleic acid content and metabolic activity of lateral geniculate nucleus in monkey following afferent denervation, J. Neurochem., 14 (1967) 257-263. 18 Lindner, 1. and Umrath, K., Veranderungen der sehspare 1 und II in ihrem monocularen und binocularen teil nach extirlzation eines augen beim kaninchen, D. Z. Nervheik, 172 (1955) 495-525. 19 Mathews, M. R., Cowen, W. M. and Powell, T. P. S., Transneuronal cell degeneration in the lateral geniculate nucleus of tile macaque monkey, J. Anat. (Land.), 94 (1960) 145 169. 20 Wiesel, T. N., Hubel, D. H. and Lam, D. N. K., Autoradiographic demonstration of ocular dominance columns in monkey striate cortex by means of transneuronal transport, Brain Research, 79 (1974) 273-279.