Exp. Brain Res. 24, 523--529 (1976)
Experimental Brain Research 9 by Springer-Verlag 1976
Retinogeniculate Projections in Hooded and Albino Rats:
An Autoradiographic Study* T. L. Itiekey and P. D. Spear School of Optometry, University of Alabama in Birmingham, Birmingham (USA) and Department of Psychology, Kansas State University, Manhattan (USA)
Introduction The projection of the retina onto the lateral genieulate nucleus of the rat has been demonstrated in a number of previous studies (Cunningham and Land, 1971; Giolli and Creel, 1974; Guillery et al., 1971; Hayhow et al., 1962; Lashley, 1934a; Lurid, 1965; L a n d and Cunningham, 1972; Lund et al., 1975; ?r and Guillery, 1968 ; Swanson et al., 1975). Most of these studies were concerned with the retinal projections to the dorsal lateral genieulate nucleus (DGL), and comparisons between albino and pigmented strains of rats have been confined almost exclusively to the DGL. The retinal projections to the ventral lateral geniculate nucleus (VGL) has not been as well studied in either strain. Questions still exist concerning whether the retinal projection to VGL is totally confined to the external division of the nucleus and whether there is any ipsilateral retinal projection to VGL in albino rats. As a part of a study of collateral sprouting in the rat VGL we undertook an autoradiographie investigation of normal retinogeniculate projections in both pigmented and albino rats. The autoradiographie teehnique has allowed us to demonstrate quite dearly the differences between retinal projections to both DGL and VGL in these animals. I n addition, it has revealed a previously undescribed projection to a leaflet of cells lying between these two nuclei.
Methods Six rats, three albino (Sprague Dawley) and three hooded (Long Evans), were used in the present study. The histologic and autoradiographic procedures used were similar to those described elsewhere (Hiekey and Guillery, 1974). Twentyfour hours following an intraocular injection of (I-I)a-Leucine, each animal was anesthetized and then sacrificed and the brain routinely prepared for paraffin embedding. The brains were cut in the coronal plane since this plane of section best demonstrates the retinal projection to VGL. Following all autoradiographic l?roeedures, the sections were stained with Thionin. * Supported by Medical Center Faculty Research Grants ~82-6120 and ~82-6203 from the Graduate School, University of Alabama in Birmingham and USPHS grant 5 I~01 Eu to P.D.S. and N.S.F. grant BMS 74-23658to T.L.tI.
524
T.L. Hickey and P. D. Spear
Results
Dorsal Lateral Geniculate Nucleus I n both the albino and hooded rats, the contralateral DGL receives an extensive retinal projection. The retinal projections to the ipsilateral DGL appear to be more extensive in the hooded rats. While there are several patches of ipsilateral input in the more anterior parts of the nucleus in both albino and hooded rats, further caudally in the nucleus the hooded rats exhibit a single region of ipsilateral input. Albino rats continue to show multiple regions of ipsilateral input throughout most of the nucleus. These results using autoradiographic techniques confirm previous studies using degeneration techniques (Cnnningham and Lund, 1971; Giolli and Creel, 1974; Guillery et al., 1971; Lund, 1965; Lund et al., 1975) which showed a larger and more continuous ipsilateral retinal projection to DGL in hooded rats t h a n in albino rats (see Fig. 1).
Ventral Lateral Geniculate Nucleus There is a heavy contralateral retinal projection to the VGL in both hooded and albino rats (Figs. 1 and 2). This projection is confined primarily to the external division of the nucleus. However, contralateral retinogeniculate fibers can be seen terminating within the internal division in both strains of rats, especially in the more caudal parts of the nucleus. This is shown for both an albino and hooded rat in the photomicrographs in Figs. lb and ld, respectively. The projection to the internal division of the VGL is comparatively sparse. Nevertheless, in some more caudal sections levels of labeling which are higher than background clearly extend to the most medial edge of the VGL. I n both hooded and albino rats, there are regions in the external division of the contralateral VGL which show a reduced contralateral projection. Such areas are always much easier to demonstrate in the hooded rats. An ipsilateral projection to the external division of the VGL was found in both hooded and albino rats. This is shown for an albino rat in the photomicrograph in Fig. I f and for a hooded rat in Fig. lh. The overall extent of the ipsilateral projection appears to be similar for both albino and hooded rats although it is always much more interrupted in the albino animals (see Figs. 1 and 2). Previous investigators have reported a sparse contralatera] retinal projection to the internal division of the VGL in the golden hamster (Schneider, 1968), d utchbelted rabbit (Mathers and Mascetti, 1975), and albino rat (Swanson et al., 1975). Our results confirm the existence of this projection in the albino rat and show t h a t it also is present in the pigmented hooded rat. In contrast to a previous report (Lund, 1965), we also have found t h a t an ipsilateral retinal projection is present in the VGL in the albino rat, as well as in the hooded rat.
Intergeniculate Leaflet We have identified a separate retinal projection to a group of cells lying between DGL and VGL rostrally and extending medial to VGL caudally. These ceils are small and oval shaped, and are similar to those in the internal division of the VGL.
..$
Fig. 1. Drawings and corresponding darkfield photomicrographs showing the eontralateral (a, b, c, d) a n d ipsilateral (e, f, g, h) retinal projections to the DGL, VGL and intergenieulate leaflet in a n albino (a, b, e, f) a n d hooded (c, d, g, h) rat. The parts of the nuclei t h a t contained retinal axon terminuls, as determined by the distribution of silver grains, are represented b y the dots in the drawings. Regions in the eontralateral nuclei t h a t received a reduced projection are represented as 'holes' in the field of dots. Such areas were never totally devoid of label in the albino rats b u t were usually quite clearly defined in the hooded rats. I n b o t h cases the left eye was injected with (H)*-Leueine. • 6
526
T.L. Hiekey and P. D. Spear
IPS!
ALBINO .~
,..,
.,.-,,
CONTRA
Astral
:2::.
.::'.'"
IPSI
HOODED
Fig. 2. Drawings made from coronal sections taken at three points along the rostral-caudal extent of the VGL in an albino (top) and hooded (bottom) rat. While both animals receive an ipsilateral projection, the position of the projection varies considerably between albino rats but is primarily confined to the dorsal border of the VGL in hooded rats. The projection shown outside the boundary of the VGL is discussed in Fig. 3
Since t h e y receive a clear b i l a t e r a l p r o j e c t i o n which a p p e a r s t o be d i s t i n c t from t h e p r o j e c t i o n s to either t h e D G L or VGL, we h a v e given this g r o u p of cells a s e p a r a t e n a m e : t h e i n t e r g e n i c u l a t e leaflet (IGL). R o s t r a l l y , t h e p r o j e c t i o n to t h e I G L is e o n f i n e d t o t h e region b e t w e e n t h e D G L a n d t h e V G L (Figs. 1 a n d 2). I n t h e m i d - p o r t i o n of t h e nuclei, t h e I G L p r o j e c t i o n a p p e a r s to e x t e n d v e n t r a l l y a n d m e d i a l t o t h e i n t e r n a l division of t h e V G L (Figs. 2 a n d 3). A t t h i s point, it a p p e a r s to merge w i t h t h e zona i n e e r t a j u s t l a t e r a l to t h e mediM lemniscus. More c a u d a l l y in t h e D G L a n d V G L nuclei, t h e I G L p r o j e c t i o n d r o p s o u t completely. T h e c o n t r a l a t e r a l p r o j e c t i o n t o t h e I G L is s o m e w h a t larger t h a n t h e ipsilateral p r o j e c t i o n (Figs. 1--3). A l t h o u g h t h e r e is a g r e a t deal of v a r i a b i l i t y in t h e size
Fig. 3. Brightfield (a, d) and corresponding darkfield (b) photomicrographs showing the contrMateral projection to the DGL, VGL and intergenieulate leaflet in an albino rat. The arrows in Fig. 3a and d indicate corresponding points in the two photomicrographs. Figure 3c contains a darkfield photomicrograph showing the ipsilateral projection to the intergeniculate leaflet. The magnified view of the intergenieulate leaflet in l~ig. 3d shows the relationship between the heavily labeled external division of the VGL, the more lightly labeled internal
Fig. 3 division of the VGL and the intergeniculate leaflet (black arrow). The region shown in this figure represents the most extensive retina! projection to the intergenieulate leaflet. I n this p a r t of the leaflet the retinal projection appears to extend ventro-medially and merge with the zona incerta (Fig. 3a, b, c; • 6) (Fig. 3d; • 25) 36 :Exp. Braio Res. u
24
528
T.L. Hiekey and P. D. Spear
a n d location of t h e p r o j e c t i o n from one a n i m a l to a n o t h e r it a p p e a r s t h a t t h e c o n t r a l a t e r a l a n d i p s i l a t e r a l r e t i n a l p r o j e c t i o n s do overlap, especially in more c a u d a l p a r t s of t h e leaflet. A r e t i n a l p r o j e c t i o n to t h e i n t e r g e n i c u l a t e leaflet was p r e s e n t in all six a n i m a l s s t u d i e d and, a l t h o u g h it was difficult to d e t e r m i n e due t o t h e v a r i a b i l i t y b e t w e e n animals, it seems t o be g r e a t e r in t h e albino rats. T h e l a t t e r is especially t r u e for t h e t w o a n i m a l s shown in Fig. 2. A b i l a t e r a l r e t i n a l p r o j e c t i o n to t h e dorsal m o s t p a r t of t h e t r e e shrew V G L h a s been described b y L a e m l e (1968). I t seems possible t h a t L a e m l e ' s V G L dorsal s e g m e n t corresponds t o t h e i n t e r g e n i c u l a t e leaflet described here for t h e rat. I f so, it would suggest t h a t this region m a y be p r e s e n t in o t h e r species as well. Along these lines we h a v e r e c e n t l y d e m o n s t r a t e d , using a u t o r a d i o g r a p h i c techniques, a v e r y similar r e t i n a l p r o j e c t i o n in d u t c h b e l t e d r a b b i t s (Takahashi, t t i c k e y a n d Oyster, m a n u s c r i p t in p r e p a r a t i o n ) . W h e t h e r or n o t t h e p r o j e c t i o n t o this a r e a is r e t i n o t o p i c a ] l y organized a n d t h e fate of efferent p r o j e c t i o n s of t h e cells in this region r e m a i n to be w o r k e d out.
AcIcnowledgements. We thank Ms. Sharon Landrum, Ms. Gloria Avery and Ms. Patrice Smith for their patient help in preparing this material and Mr. J. Marbourg for his assistance with the photography and illustrations. Mr. Marbourg was supported in part by a grant from The Skeffington Memorial :Fund made available through the Virginia Optometric Association. We also wish to thank Ms. Hazel Davis for secretarial help.
References Cunningham, T.J., Land, 1%.D.: Laminar Patterns in the dorsal division of the lateral geniculate nucleus of the rat. Brain 1%es.34, 394--398 (1971) Giolli, R.A., Creel, D.J.: The primary optic projections in pigmented and albino guineae pigs: an experimental degeneration study. Brain Res. 55, 25--39 (1973) Giolli, 1%.A., Creel, D. J. : Inheritance and variability of the organization of the retinogeniculate projections in pigmented and albino rats. Brain Res. 78, 335--339 (1974) Guillery, 1%.W., Sitthi-Amorn, C., Eighmy, B.B. : Mutants with abnormal visual pathways: an explanation of anomalous geniculate laminae. Science 174, 831--832 (1971) Itayhow, W. 1%., Sefton, A., Webb, G. : Primary optic centers of the rat in relation to the terminal distribution of the crossed and uncrossed optic nerve fibers. J. comp. Neurol. 118, 295--322 (1962) Hickey, T.L., Guillery, 1%.W.: An autoradiographic study of retinogeniculate pathways in the cat and the fox. J. comp. Neurol. 156,239 --254 (1974) Laemle, L.K.: 1%etinal projections of Tupaia Glis. Brain Behav. Evol. 1, 473---499 (1968) Lashley, K. S. : The mechanism cf vision. VII. The projection of the retina upon the primary optic centers in the rat. J. comp. Neurol. 59, 341--373 (1934a) Lund, 1%.D. : Uncrossed visual pathways of hooded and albino rats. Science 149, 1506--1507 (1965) Lund, 1%.D., Cunningham, T.J. : Aspects of synaptic and laminar organization of the mammalian lateral geniculate body. Invest. Ophthal. 11,291--302 (1972) Lurid, 1%.D., Lund, J.S., Wise, R.P. : The Organization of the retinal projection to the dorsal lateral geniculate nucleus in pigmented and albino rats. J. temp. 1Neurol. 158, 383~404 (1975) Mathers, L. It., Masc~tti, G.G. : Electrophysiological and morphological properties of neurons in the ventral lateral geniculate nucleus of the rabbit. Exp. Neurol. 46, 506--520 (1975)
Retinogeniculate Projections in the Rat
529
Montero, V.M., Guillery, R.W. : Degeneration in the dorsal lateral geniculate nucleus of the rat following interruption of the retinal or cortical connections. J. eomp. Neurol. 134, 211--242 (1968) Schneider, G. E. : Retinal projections characterized by differential rate of degeneration revealed by silver impregnation. Anat. Rec. 16@,423 (1968) Swanson, L.W., Cowan, W.M., Jones, E.G.: An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. J. comp. Neurol. 156, 143--164 (1975)
.Received August 4, 1975 Dr. T. L. Hickey School of Optometry/The Medical Center University of Alabama in Birmingham Birmingham, Alabama 35294 USA
36*
Experimental Brain Research 9 by Springer-Verlag 1976
Retinogeniculate Projections in Hooded and Albino Rats:
An Autoradiographic Study* T. L. Itiekey and P. D. Spear School of Optometry, University of Alabama in Birmingham, Birmingham (USA) and Department of Psychology, Kansas State University, Manhattan (USA)
Introduction The projection of the retina onto the lateral genieulate nucleus of the rat has been demonstrated in a number of previous studies (Cunningham and Land, 1971; Giolli and Creel, 1974; Guillery et al., 1971; Hayhow et al., 1962; Lashley, 1934a; Lurid, 1965; L a n d and Cunningham, 1972; Lund et al., 1975; ?r and Guillery, 1968 ; Swanson et al., 1975). Most of these studies were concerned with the retinal projections to the dorsal lateral genieulate nucleus (DGL), and comparisons between albino and pigmented strains of rats have been confined almost exclusively to the DGL. The retinal projections to the ventral lateral geniculate nucleus (VGL) has not been as well studied in either strain. Questions still exist concerning whether the retinal projection to VGL is totally confined to the external division of the nucleus and whether there is any ipsilateral retinal projection to VGL in albino rats. As a part of a study of collateral sprouting in the rat VGL we undertook an autoradiographie investigation of normal retinogeniculate projections in both pigmented and albino rats. The autoradiographie teehnique has allowed us to demonstrate quite dearly the differences between retinal projections to both DGL and VGL in these animals. I n addition, it has revealed a previously undescribed projection to a leaflet of cells lying between these two nuclei.
Methods Six rats, three albino (Sprague Dawley) and three hooded (Long Evans), were used in the present study. The histologic and autoradiographic procedures used were similar to those described elsewhere (Hiekey and Guillery, 1974). Twentyfour hours following an intraocular injection of (I-I)a-Leucine, each animal was anesthetized and then sacrificed and the brain routinely prepared for paraffin embedding. The brains were cut in the coronal plane since this plane of section best demonstrates the retinal projection to VGL. Following all autoradiographic l?roeedures, the sections were stained with Thionin. * Supported by Medical Center Faculty Research Grants ~82-6120 and ~82-6203 from the Graduate School, University of Alabama in Birmingham and USPHS grant 5 I~01 Eu to P.D.S. and N.S.F. grant BMS 74-23658to T.L.tI.
524
T.L. Hickey and P. D. Spear
Results
Dorsal Lateral Geniculate Nucleus I n both the albino and hooded rats, the contralateral DGL receives an extensive retinal projection. The retinal projections to the ipsilateral DGL appear to be more extensive in the hooded rats. While there are several patches of ipsilateral input in the more anterior parts of the nucleus in both albino and hooded rats, further caudally in the nucleus the hooded rats exhibit a single region of ipsilateral input. Albino rats continue to show multiple regions of ipsilateral input throughout most of the nucleus. These results using autoradiographic techniques confirm previous studies using degeneration techniques (Cnnningham and Lund, 1971; Giolli and Creel, 1974; Guillery et al., 1971; Lund, 1965; Lund et al., 1975) which showed a larger and more continuous ipsilateral retinal projection to DGL in hooded rats t h a n in albino rats (see Fig. 1).
Ventral Lateral Geniculate Nucleus There is a heavy contralateral retinal projection to the VGL in both hooded and albino rats (Figs. 1 and 2). This projection is confined primarily to the external division of the nucleus. However, contralateral retinogeniculate fibers can be seen terminating within the internal division in both strains of rats, especially in the more caudal parts of the nucleus. This is shown for both an albino and hooded rat in the photomicrographs in Figs. lb and ld, respectively. The projection to the internal division of the VGL is comparatively sparse. Nevertheless, in some more caudal sections levels of labeling which are higher than background clearly extend to the most medial edge of the VGL. I n both hooded and albino rats, there are regions in the external division of the contralateral VGL which show a reduced contralateral projection. Such areas are always much easier to demonstrate in the hooded rats. An ipsilateral projection to the external division of the VGL was found in both hooded and albino rats. This is shown for an albino rat in the photomicrograph in Fig. I f and for a hooded rat in Fig. lh. The overall extent of the ipsilateral projection appears to be similar for both albino and hooded rats although it is always much more interrupted in the albino animals (see Figs. 1 and 2). Previous investigators have reported a sparse contralatera] retinal projection to the internal division of the VGL in the golden hamster (Schneider, 1968), d utchbelted rabbit (Mathers and Mascetti, 1975), and albino rat (Swanson et al., 1975). Our results confirm the existence of this projection in the albino rat and show t h a t it also is present in the pigmented hooded rat. In contrast to a previous report (Lund, 1965), we also have found t h a t an ipsilateral retinal projection is present in the VGL in the albino rat, as well as in the hooded rat.
Intergeniculate Leaflet We have identified a separate retinal projection to a group of cells lying between DGL and VGL rostrally and extending medial to VGL caudally. These ceils are small and oval shaped, and are similar to those in the internal division of the VGL.
..$
Fig. 1. Drawings and corresponding darkfield photomicrographs showing the eontralateral (a, b, c, d) a n d ipsilateral (e, f, g, h) retinal projections to the DGL, VGL and intergenieulate leaflet in a n albino (a, b, e, f) a n d hooded (c, d, g, h) rat. The parts of the nuclei t h a t contained retinal axon terminuls, as determined by the distribution of silver grains, are represented b y the dots in the drawings. Regions in the eontralateral nuclei t h a t received a reduced projection are represented as 'holes' in the field of dots. Such areas were never totally devoid of label in the albino rats b u t were usually quite clearly defined in the hooded rats. I n b o t h cases the left eye was injected with (H)*-Leueine. • 6
526
T.L. Hiekey and P. D. Spear
IPS!
ALBINO .~
,..,
.,.-,,
CONTRA
Astral
:2::.
.::'.'"
IPSI
HOODED
Fig. 2. Drawings made from coronal sections taken at three points along the rostral-caudal extent of the VGL in an albino (top) and hooded (bottom) rat. While both animals receive an ipsilateral projection, the position of the projection varies considerably between albino rats but is primarily confined to the dorsal border of the VGL in hooded rats. The projection shown outside the boundary of the VGL is discussed in Fig. 3
Since t h e y receive a clear b i l a t e r a l p r o j e c t i o n which a p p e a r s t o be d i s t i n c t from t h e p r o j e c t i o n s to either t h e D G L or VGL, we h a v e given this g r o u p of cells a s e p a r a t e n a m e : t h e i n t e r g e n i c u l a t e leaflet (IGL). R o s t r a l l y , t h e p r o j e c t i o n to t h e I G L is e o n f i n e d t o t h e region b e t w e e n t h e D G L a n d t h e V G L (Figs. 1 a n d 2). I n t h e m i d - p o r t i o n of t h e nuclei, t h e I G L p r o j e c t i o n a p p e a r s to e x t e n d v e n t r a l l y a n d m e d i a l t o t h e i n t e r n a l division of t h e V G L (Figs. 2 a n d 3). A t t h i s point, it a p p e a r s to merge w i t h t h e zona i n e e r t a j u s t l a t e r a l to t h e mediM lemniscus. More c a u d a l l y in t h e D G L a n d V G L nuclei, t h e I G L p r o j e c t i o n d r o p s o u t completely. T h e c o n t r a l a t e r a l p r o j e c t i o n t o t h e I G L is s o m e w h a t larger t h a n t h e ipsilateral p r o j e c t i o n (Figs. 1--3). A l t h o u g h t h e r e is a g r e a t deal of v a r i a b i l i t y in t h e size
Fig. 3. Brightfield (a, d) and corresponding darkfield (b) photomicrographs showing the contrMateral projection to the DGL, VGL and intergenieulate leaflet in an albino rat. The arrows in Fig. 3a and d indicate corresponding points in the two photomicrographs. Figure 3c contains a darkfield photomicrograph showing the ipsilateral projection to the intergeniculate leaflet. The magnified view of the intergenieulate leaflet in l~ig. 3d shows the relationship between the heavily labeled external division of the VGL, the more lightly labeled internal
Fig. 3 division of the VGL and the intergeniculate leaflet (black arrow). The region shown in this figure represents the most extensive retina! projection to the intergenieulate leaflet. I n this p a r t of the leaflet the retinal projection appears to extend ventro-medially and merge with the zona incerta (Fig. 3a, b, c; • 6) (Fig. 3d; • 25) 36 :Exp. Braio Res. u
24
528
T.L. Hiekey and P. D. Spear
a n d location of t h e p r o j e c t i o n from one a n i m a l to a n o t h e r it a p p e a r s t h a t t h e c o n t r a l a t e r a l a n d i p s i l a t e r a l r e t i n a l p r o j e c t i o n s do overlap, especially in more c a u d a l p a r t s of t h e leaflet. A r e t i n a l p r o j e c t i o n to t h e i n t e r g e n i c u l a t e leaflet was p r e s e n t in all six a n i m a l s s t u d i e d and, a l t h o u g h it was difficult to d e t e r m i n e due t o t h e v a r i a b i l i t y b e t w e e n animals, it seems t o be g r e a t e r in t h e albino rats. T h e l a t t e r is especially t r u e for t h e t w o a n i m a l s shown in Fig. 2. A b i l a t e r a l r e t i n a l p r o j e c t i o n to t h e dorsal m o s t p a r t of t h e t r e e shrew V G L h a s been described b y L a e m l e (1968). I t seems possible t h a t L a e m l e ' s V G L dorsal s e g m e n t corresponds t o t h e i n t e r g e n i c u l a t e leaflet described here for t h e rat. I f so, it would suggest t h a t this region m a y be p r e s e n t in o t h e r species as well. Along these lines we h a v e r e c e n t l y d e m o n s t r a t e d , using a u t o r a d i o g r a p h i c techniques, a v e r y similar r e t i n a l p r o j e c t i o n in d u t c h b e l t e d r a b b i t s (Takahashi, t t i c k e y a n d Oyster, m a n u s c r i p t in p r e p a r a t i o n ) . W h e t h e r or n o t t h e p r o j e c t i o n t o this a r e a is r e t i n o t o p i c a ] l y organized a n d t h e fate of efferent p r o j e c t i o n s of t h e cells in this region r e m a i n to be w o r k e d out.
AcIcnowledgements. We thank Ms. Sharon Landrum, Ms. Gloria Avery and Ms. Patrice Smith for their patient help in preparing this material and Mr. J. Marbourg for his assistance with the photography and illustrations. Mr. Marbourg was supported in part by a grant from The Skeffington Memorial :Fund made available through the Virginia Optometric Association. We also wish to thank Ms. Hazel Davis for secretarial help.
References Cunningham, T.J., Land, 1%.D.: Laminar Patterns in the dorsal division of the lateral geniculate nucleus of the rat. Brain 1%es.34, 394--398 (1971) Giolli, R.A., Creel, D.J.: The primary optic projections in pigmented and albino guineae pigs: an experimental degeneration study. Brain Res. 55, 25--39 (1973) Giolli, 1%.A., Creel, D. J. : Inheritance and variability of the organization of the retinogeniculate projections in pigmented and albino rats. Brain Res. 78, 335--339 (1974) Guillery, 1%.W., Sitthi-Amorn, C., Eighmy, B.B. : Mutants with abnormal visual pathways: an explanation of anomalous geniculate laminae. Science 174, 831--832 (1971) Itayhow, W. 1%., Sefton, A., Webb, G. : Primary optic centers of the rat in relation to the terminal distribution of the crossed and uncrossed optic nerve fibers. J. comp. Neurol. 118, 295--322 (1962) Hickey, T.L., Guillery, 1%.W.: An autoradiographic study of retinogeniculate pathways in the cat and the fox. J. comp. Neurol. 156,239 --254 (1974) Laemle, L.K.: 1%etinal projections of Tupaia Glis. Brain Behav. Evol. 1, 473---499 (1968) Lashley, K. S. : The mechanism cf vision. VII. The projection of the retina upon the primary optic centers in the rat. J. comp. Neurol. 59, 341--373 (1934a) Lund, 1%.D. : Uncrossed visual pathways of hooded and albino rats. Science 149, 1506--1507 (1965) Lund, 1%.D., Cunningham, T.J. : Aspects of synaptic and laminar organization of the mammalian lateral geniculate body. Invest. Ophthal. 11,291--302 (1972) Lurid, 1%.D., Lund, J.S., Wise, R.P. : The Organization of the retinal projection to the dorsal lateral geniculate nucleus in pigmented and albino rats. J. temp. 1Neurol. 158, 383~404 (1975) Mathers, L. It., Masc~tti, G.G. : Electrophysiological and morphological properties of neurons in the ventral lateral geniculate nucleus of the rabbit. Exp. Neurol. 46, 506--520 (1975)
Retinogeniculate Projections in the Rat
529
Montero, V.M., Guillery, R.W. : Degeneration in the dorsal lateral geniculate nucleus of the rat following interruption of the retinal or cortical connections. J. eomp. Neurol. 134, 211--242 (1968) Schneider, G. E. : Retinal projections characterized by differential rate of degeneration revealed by silver impregnation. Anat. Rec. 16@,423 (1968) Swanson, L.W., Cowan, W.M., Jones, E.G.: An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. J. comp. Neurol. 156, 143--164 (1975)
.Received August 4, 1975 Dr. T. L. Hickey School of Optometry/The Medical Center University of Alabama in Birmingham Birmingham, Alabama 35294 USA
36*
