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Extrastriate projections from thalamus to posterior occipital-temporal cortex in rat
Brain Research, 194 (1980) 205-209 © Elsevier/North-Holland Biomedical Press
205
Short Communications
Extrastriate projections from thalamus to posterior occipital-temporal cortex in rat
J. COLEMAN and W. J. CLERICI Departments of Psychology and Physiology, University of South Carolina, Columbia, S.C. 29208 (U.S.A.)
(Accepted March 20th, 1980) Key words: extrastriate -- thalamus -- occipito-temporal-- cortex
The general mammalian plan for the classical visual pathway involves a projection from the dorsal lateral geniculate nucleus (GL) which is confined to cortical area 17 (striate cortex). This restricted target for G L has been demonstrated in such mammals as hedgehog 9, opossum 4, tree shrew 11, bush baby s and rhesus monkey 12. The most clearly demonstrated exception to this plan is the cat in which GL projects to cortical areas 18, 19 and beyondV,ls,23. According to Lashley the projection field of GL in rat is restricted to striate cortex. His results were based upon observations of retrograde degeneration 16,17. More recently, the use of retrograde and anterograde transport techniques has produced conflicting observations concerning a GL projection to Krieg's area 18a 13,19,24,26. According to Krieg 14,15 area 18a is a cytoarchitectonically homogeneous region lateral to striate cortex and is anatomically interposed between part of area 17 and the caudal margin of cortex. Electrical recordings in rat have revealed an organization somewhat unusual among mammals. In contrast to the single representation of visual field observed in area 18 of many mammals, the portion of 18a adjacent to area 17 of rat is reported to contain multiple representations21, 22. We investigated the thalamic projections to posterior neocortex in rat using the retrograde transport marker horseradish peroxidase (HRP). We chose to make small injections of HRP (Sigma; type VI) by iontophoretic application (1.9/~A direct; 10 ~o HRP) through micropipettes (15-20 #m tips) concentrating our injections caudally within occipital-temporal cortex to avoid injection of geniculostriate axons of passage. Microscopic inspection of cortex later also confirmed absence of damage. Following 24 survival animals were perfused with a saline/sodium nitrite solution followed by 2.5 ~ glutaraldehyde in phosphate buffer (pH 7.4), then a 5 ~ polyethylene glycol solution. Frozen sections cut at 40 #m were immersed in buffer overnight and then processed for HRP histochemistry using either diaminobenzine 1° or tetramethyl benzidene zo.
206
18a
C D
36b
45 ° A
B
D
125
~.
134
~
145
"~.
Fig. 1. Distribution of labeled thalamic neurons resulting from HRP injected caudally into cortical areas 18a and 36a of rat. A standard 45 ° view shows the loocation of injections in 4 different cases. The position of each labeled neuron is depicted by a dot. Thalamic section numbers represent 40/~m. A and B : two 18a injections near the caudal border of area 17 result in the appearance of labeled neurons in LP and GL. C: a more lateral injection of 18a (photomicrograph of injection center at upper right inset) restricted to the caudal pole of cortex produces labeled neurons in GL, LP, L. and MD. D : labeled cells in the caudal sector of LP result from a 36a injection. Abbreviations are as follows: CL, central lateral nucleus; HI, lateral habenula nucleus; Hm, medial habenula nucleus; GL, dorsal lateral geniculate nucleus; GM, medial geniculate nucleus; L, lateral thalamic nucleus; LP, lateral posterior nucleus; MD, medial dorsal nucleus; Pc, paracentral nucleus; Po, posterior nucleus; Pom, medial division of the posterior nucleus; Pt, pretectum; R, reticular nucleus; VGL, ventral lateral geniculate nucleus; VP, ventral posterior nucleus; 17 and 18a, areas of occipital cortex; 36a and 36b, areas of temporal cortex.
207 Results of injections caudal and lateral to striate cortex are illustrated in Fig. 1. The largest HRP injection illustrated (Fig. 1A) shows the position of labeled neurons in two thalamic structures: the lateral posterior nucleus (LP) and GL. Observation of a projection from LP to belt cortex adjacent to striate cortex confirms findings of similar connections in other mammalian speciesS,9,27. The labeled cells which were observed in GL underscore a more unique mammalian phenomenon. GL cells with reaction product were not distributed in one cluster, but were found in different sectors of GL. A more medial injection of area 18a (Fig. 1B) also produces labeled cells in both GL and LP. These injections appear to coincide with the physiologically defined posterior visual area of ratZl, 22. The possibility that labeling in GL resulted from diffusion into striate cortex or from transected axons of passage was not supported. First, labeled GL cells were sometimes widely separated and often in locations remote from cells believed to project to the border of striate cortex near the site of injection. Further evidence for a geniculoextrastriate pathway in rat was provided by an HRP injection in the caudal pole of area 18a distant from area 17 (Fig. 1C and inset). The result was labeling of GL, as well as LP, and the lateral and mediodorsal nuclei. In addition, the superficial position of this injection along the curvature of cortex suggests that GL fibers terminate superior to the lamina V of area 18a. This injection seems to correspond with the previously described posterolateral area of rat21, 22. GL labeling was observed in all cases involving caudal 18a regardless of the chromagen used. The percentage of GL neurons labeled from caudal 18a injections relative to the total number of labeled neurons in the lateral thalamus ranged from 2.3 ~ to 13.3 ~. For example, the case illustrated in Fig. 1B labeled 54 LP cells and 7 GL cells (13.0~). To determine how far laterally in cortex the GL projection extended we made further injections in an area which Krieg included as part of area 36, but which we have identified as cytoarchitectonically distinct. From Nissl- and myelin-stained rat preparations Krieg's area 36 was further subdivided into areas 36a and 36b. Relative to area 36b, area 36a has thicker layers 1 and 2, and has clearer lamination patterns below layer 2. Area 36a has greater overall thickness and appears fiber-rich in myelin stains. Injections into area 36a produced labeled neurons in the caudal portion of LP (Fig. 1D). Area 36a was the only region of caudal occipital-temporal cortex in which afferent input from this sector of LP was observed. A second injection involving only layers 4 and 5 of area 36a labeled many caudal LP neurons. It is interesting to compare this finding to observations of a projection from the caudal sector of LP or the pulvinar nucleus to posterior temporal cortex in squirrel 27, opossum (personal observation), or to middle temporal areas of primates2, s. The evidence suggests that, like the primary sensory projection centers of neocortex, this temporal area may be a generalized and ancient mammalian cortical center 1. This finding in rat also conforms to the idea of specific projection patterns of zones of the LP-pulvinar complex (which receive visual input from midbrain and cortex) to particular areas of occipital-temporal cortex3, 27. A projection of the lateral thalamic nucleus only to the region between medial 18a and 36a also supports this (Fig. 1C).
208 Studies in rat involving electrophysiological mapping o f extrastriate cortical structures demonstrate multiple representations o f the visual field21, 22. In particular, the rat, unlike most other mammals investigated, shows interrupted and separate visual representations in the region adjacent to striate cortex, although these representations do show mirror-image field reversals at the striate-extrastriate borders. The cat is the only other m a m m a l in which G L has been shown convincingly to project to extrastriate cortex 7,18,28. Such reports in the cat indicate that the major laminae of G L all send afferents to various parts o f extrastriate cortex including areas 18 and 19. LeVay and Gilbert TM observed that the widest projection in cat was from the C laminae which innervate areas 18, 19 and other regions of the suprasylvian gyrus. Our results indicate the presence o f two G L projection zones in caudal occipital cortex which show a rough topography. H R P injections approaching the caudolateral striate border label G L cells close to the zero vertical meridian representation. Whether the G L extrastriate fibers are expressions o f collaterals from G L neurons projecting to striate cortex m a y be determined by employing a double label transport technique. It is not k n o w n what physiological properties rat G L cells possess, but in cat area 18 receives input from the large, fast-conducting G L Y cells, while area 17 receives input from both X and Y cells 2s. O f special interest is the role extrastriate thalamic projections play in visual function. Rats with bilateral lesions of striate cortex can perform successive pattern discriminations, but there is a more severe deficit if lesions of the lateral posterior nucleus are made in additionlL Lesions o f area 18a in rats seriously impair visual conditional discrimination and reversal learning tasks 6. Further, large ablations of area 17 in rats have no effect on the location and size o f receptive fields o f cells in area 18a and their general topography 2s. All these results point to the role of direct projections by the lateral, lateral posterior and lateral geniculate nuclei to area 18a in rat, and their importance in structural and functional organization.
1 Allman, J. M., Evaluation of the visual system in the early primates. In J. M. Sprague and A. N. Epstein (Eds.), Progress in Psychology and Physiological Psychology, Iioi. 18, Academic Press, New York, 1977, pp. 1-53. 2 Allman, J. M. and Kaas, J. H., Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus), Brain Research, 35 (1971) 89-106. 3 Berson, D. M. and Graybiel, A. M., Parallel thalamic zones in the LP-pulvinar complex of the cat identified by their afferent and efferent connections, Brain Research, 147 (1978) 139-148. 4 Coleman, J., Diamond, I. T. and Winer, J. A., The visual cortex of the opossum: the retrograde transport of horseradish peroxidase to the lateral geniculate and lateral posterior nuclei, Brain Research, 137 (1977) 233-252. 5 Diirsteler, M. R., Blakemore, C. and Garey, L. J., Projections to the visual cortex in the golden hamster, J. comp. NeuroL, 183 (1979) 185-204. 6 Gallardo, L., Mottles, M., Vera, L., Carrasco, M., Torrealba, F., Montero, V. M. and PintoHamuy, T., Failure by rats to learn a visual conditional discrimination after lateral peristriate cortical lesions, PhysioL Psychol., 7 (1979) 173-177. 7 Garey, L. J. and Powell, T. P. S., An experimental study of the lateral geniculate cortical pathway in the cat and monkey, Proc. roy. Soc. B, 119 (1971) 41-63. 8 Glendenning, K. K., Kofron, E. A. and Diamond, I. T., Laminar organization of the projections of the lateral geniculate nucleus to the striate cortex in Galago, Brain Research, 105 (1976) 538546.
209 9 Gould, H. J., III. Hall, W. C. and Ebner, F. F., Connections of the visual cortex in the hedgehog (Paraechinus hypomelas). I. Thalamocortical projections, J. comp. Neurol., 177 (1978) 445-472. 10 Graham, R. C., Jr. and Karnovsky, M. J., The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique, J. Histochem. Cytochem., 14 (1966) 291-302. I 1 Harting, J. K., Diamond, I. T. and Hall, W. C., Anterograde degeneration study of the cortical projections of the lateral geniculate and pulvinar nuclei in the tree shrew, J. comp. Neurol., 150 (1973) 393-440. 12 Hubel, D. H. and Wiesel, T. N., Laminar and columnar distribution of the geniculocortical fibers in the macaque monkey, J. comp. Neurol., 146 (1972) 421-450. 13 Hughes, H. C., Anatomical and neurobehavioral investigations concerning the thalamo-cortical organization of the rat's visual system, J. comp. Neurol., 175 (1977) 311-336. 14 Krieg, W. J. S., Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas, J. comp. Neurol., 84 (1946) 221-276. 15 Krieg, W. J. S., Connections of the cerebral cortex. II. The albino rat. B. Structure of the cortical areas, J. comp. neurol., 84 (1946) 277-323. 16 Lashley, K. S., The mechanism of vision. VIII. The projection of the retina upon the cerebral cortex of the rat, J. comp. neurol., 60 (1934) 57-80. 17 Lashley, K. S., Thalamo-cortical connections of the rat's brain, J. comp. Neurol., 75 (1941) 67-121. 18 LeVay, S. and Gilbert, C. D., Laminar patterns of geniculo-cortical projection in the cat, Brain Research, 113 (1976) 1-19. 19 McDaniel, W. F., McDaniel, S. E. and Thomas, R. K., Thalamocortical projections to the temporal and parietal association cortices in the rat, Neurosci. Lett., 7 (1978) 121-125. 20 Mesulam, M. M., Tetramethyl benzidine for horseradish peroxidase neuro-histochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents, J. Histochem. Cytochem., 26 (1978) 106-117. 21 Montero, V. M., Bravo, H. and Fernandez, V., Striate-peristriate corticocortical connections in the albino and gray rat, Brain Research, 53 (1973) 202-207. 22 Montero, V. M., Rojas, A. and Torrealba, F., Retinal organization of striate and peristriate visual cortex in the albino rat, Brain Research, 53 (1973) 197-201. 23 Niimi, K. and Sprague, J. M., Thalamo-cortical organization of the visual system in the cat, J. comp. Neurol., 138 (1970) 219-250. 24 Olavarria, J., A horseradish peroxidase study of the projections from the latero-posterior nucleus to three lateral peristriate areas in the rat, Brain Research, 173 (1979) 137-141. 25 Olavarria, J. and Torrealba, F., The effects of acute lesions of the striate cortex on the retinotopic organization of the lateral peristriate cortex in the rat, Brain Research, 151 (1978) 386-391. 26 Ribak, C. E. and Peters, A., An autoradiographic study of the projections from the lateral geniculate body of the rat, Brain Research, 92 (1975) 341-368. 27 Robson, J. A. and Hall, W. C., The organization of the pulvinar in the grey squirrel (Sciurus carolinensis). II. Synaptic organization and comparisons with the dorsal lateral geniculate nucleus, J. comp. Neurok, 173 (1977) 389-416. 28 Stone, J. and Dreher, B., Projection of the X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of the visual cortex, J. NeurophysioL, 36 (1973) 551-567.
205
Short Communications
Extrastriate projections from thalamus to posterior occipital-temporal cortex in rat
J. COLEMAN and W. J. CLERICI Departments of Psychology and Physiology, University of South Carolina, Columbia, S.C. 29208 (U.S.A.)
(Accepted March 20th, 1980) Key words: extrastriate -- thalamus -- occipito-temporal-- cortex
The general mammalian plan for the classical visual pathway involves a projection from the dorsal lateral geniculate nucleus (GL) which is confined to cortical area 17 (striate cortex). This restricted target for G L has been demonstrated in such mammals as hedgehog 9, opossum 4, tree shrew 11, bush baby s and rhesus monkey 12. The most clearly demonstrated exception to this plan is the cat in which GL projects to cortical areas 18, 19 and beyondV,ls,23. According to Lashley the projection field of GL in rat is restricted to striate cortex. His results were based upon observations of retrograde degeneration 16,17. More recently, the use of retrograde and anterograde transport techniques has produced conflicting observations concerning a GL projection to Krieg's area 18a 13,19,24,26. According to Krieg 14,15 area 18a is a cytoarchitectonically homogeneous region lateral to striate cortex and is anatomically interposed between part of area 17 and the caudal margin of cortex. Electrical recordings in rat have revealed an organization somewhat unusual among mammals. In contrast to the single representation of visual field observed in area 18 of many mammals, the portion of 18a adjacent to area 17 of rat is reported to contain multiple representations21, 22. We investigated the thalamic projections to posterior neocortex in rat using the retrograde transport marker horseradish peroxidase (HRP). We chose to make small injections of HRP (Sigma; type VI) by iontophoretic application (1.9/~A direct; 10 ~o HRP) through micropipettes (15-20 #m tips) concentrating our injections caudally within occipital-temporal cortex to avoid injection of geniculostriate axons of passage. Microscopic inspection of cortex later also confirmed absence of damage. Following 24 survival animals were perfused with a saline/sodium nitrite solution followed by 2.5 ~ glutaraldehyde in phosphate buffer (pH 7.4), then a 5 ~ polyethylene glycol solution. Frozen sections cut at 40 #m were immersed in buffer overnight and then processed for HRP histochemistry using either diaminobenzine 1° or tetramethyl benzidene zo.
206
18a
C D
36b
45 ° A
B
D
125
~.
134
~
145
"~.
Fig. 1. Distribution of labeled thalamic neurons resulting from HRP injected caudally into cortical areas 18a and 36a of rat. A standard 45 ° view shows the loocation of injections in 4 different cases. The position of each labeled neuron is depicted by a dot. Thalamic section numbers represent 40/~m. A and B : two 18a injections near the caudal border of area 17 result in the appearance of labeled neurons in LP and GL. C: a more lateral injection of 18a (photomicrograph of injection center at upper right inset) restricted to the caudal pole of cortex produces labeled neurons in GL, LP, L. and MD. D : labeled cells in the caudal sector of LP result from a 36a injection. Abbreviations are as follows: CL, central lateral nucleus; HI, lateral habenula nucleus; Hm, medial habenula nucleus; GL, dorsal lateral geniculate nucleus; GM, medial geniculate nucleus; L, lateral thalamic nucleus; LP, lateral posterior nucleus; MD, medial dorsal nucleus; Pc, paracentral nucleus; Po, posterior nucleus; Pom, medial division of the posterior nucleus; Pt, pretectum; R, reticular nucleus; VGL, ventral lateral geniculate nucleus; VP, ventral posterior nucleus; 17 and 18a, areas of occipital cortex; 36a and 36b, areas of temporal cortex.
207 Results of injections caudal and lateral to striate cortex are illustrated in Fig. 1. The largest HRP injection illustrated (Fig. 1A) shows the position of labeled neurons in two thalamic structures: the lateral posterior nucleus (LP) and GL. Observation of a projection from LP to belt cortex adjacent to striate cortex confirms findings of similar connections in other mammalian speciesS,9,27. The labeled cells which were observed in GL underscore a more unique mammalian phenomenon. GL cells with reaction product were not distributed in one cluster, but were found in different sectors of GL. A more medial injection of area 18a (Fig. 1B) also produces labeled cells in both GL and LP. These injections appear to coincide with the physiologically defined posterior visual area of ratZl, 22. The possibility that labeling in GL resulted from diffusion into striate cortex or from transected axons of passage was not supported. First, labeled GL cells were sometimes widely separated and often in locations remote from cells believed to project to the border of striate cortex near the site of injection. Further evidence for a geniculoextrastriate pathway in rat was provided by an HRP injection in the caudal pole of area 18a distant from area 17 (Fig. 1C and inset). The result was labeling of GL, as well as LP, and the lateral and mediodorsal nuclei. In addition, the superficial position of this injection along the curvature of cortex suggests that GL fibers terminate superior to the lamina V of area 18a. This injection seems to correspond with the previously described posterolateral area of rat21, 22. GL labeling was observed in all cases involving caudal 18a regardless of the chromagen used. The percentage of GL neurons labeled from caudal 18a injections relative to the total number of labeled neurons in the lateral thalamus ranged from 2.3 ~ to 13.3 ~. For example, the case illustrated in Fig. 1B labeled 54 LP cells and 7 GL cells (13.0~). To determine how far laterally in cortex the GL projection extended we made further injections in an area which Krieg included as part of area 36, but which we have identified as cytoarchitectonically distinct. From Nissl- and myelin-stained rat preparations Krieg's area 36 was further subdivided into areas 36a and 36b. Relative to area 36b, area 36a has thicker layers 1 and 2, and has clearer lamination patterns below layer 2. Area 36a has greater overall thickness and appears fiber-rich in myelin stains. Injections into area 36a produced labeled neurons in the caudal portion of LP (Fig. 1D). Area 36a was the only region of caudal occipital-temporal cortex in which afferent input from this sector of LP was observed. A second injection involving only layers 4 and 5 of area 36a labeled many caudal LP neurons. It is interesting to compare this finding to observations of a projection from the caudal sector of LP or the pulvinar nucleus to posterior temporal cortex in squirrel 27, opossum (personal observation), or to middle temporal areas of primates2, s. The evidence suggests that, like the primary sensory projection centers of neocortex, this temporal area may be a generalized and ancient mammalian cortical center 1. This finding in rat also conforms to the idea of specific projection patterns of zones of the LP-pulvinar complex (which receive visual input from midbrain and cortex) to particular areas of occipital-temporal cortex3, 27. A projection of the lateral thalamic nucleus only to the region between medial 18a and 36a also supports this (Fig. 1C).
208 Studies in rat involving electrophysiological mapping o f extrastriate cortical structures demonstrate multiple representations o f the visual field21, 22. In particular, the rat, unlike most other mammals investigated, shows interrupted and separate visual representations in the region adjacent to striate cortex, although these representations do show mirror-image field reversals at the striate-extrastriate borders. The cat is the only other m a m m a l in which G L has been shown convincingly to project to extrastriate cortex 7,18,28. Such reports in the cat indicate that the major laminae of G L all send afferents to various parts o f extrastriate cortex including areas 18 and 19. LeVay and Gilbert TM observed that the widest projection in cat was from the C laminae which innervate areas 18, 19 and other regions of the suprasylvian gyrus. Our results indicate the presence o f two G L projection zones in caudal occipital cortex which show a rough topography. H R P injections approaching the caudolateral striate border label G L cells close to the zero vertical meridian representation. Whether the G L extrastriate fibers are expressions o f collaterals from G L neurons projecting to striate cortex m a y be determined by employing a double label transport technique. It is not k n o w n what physiological properties rat G L cells possess, but in cat area 18 receives input from the large, fast-conducting G L Y cells, while area 17 receives input from both X and Y cells 2s. O f special interest is the role extrastriate thalamic projections play in visual function. Rats with bilateral lesions of striate cortex can perform successive pattern discriminations, but there is a more severe deficit if lesions of the lateral posterior nucleus are made in additionlL Lesions o f area 18a in rats seriously impair visual conditional discrimination and reversal learning tasks 6. Further, large ablations of area 17 in rats have no effect on the location and size o f receptive fields o f cells in area 18a and their general topography 2s. All these results point to the role of direct projections by the lateral, lateral posterior and lateral geniculate nuclei to area 18a in rat, and their importance in structural and functional organization.
1 Allman, J. M., Evaluation of the visual system in the early primates. In J. M. Sprague and A. N. Epstein (Eds.), Progress in Psychology and Physiological Psychology, Iioi. 18, Academic Press, New York, 1977, pp. 1-53. 2 Allman, J. M. and Kaas, J. H., Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus), Brain Research, 35 (1971) 89-106. 3 Berson, D. M. and Graybiel, A. M., Parallel thalamic zones in the LP-pulvinar complex of the cat identified by their afferent and efferent connections, Brain Research, 147 (1978) 139-148. 4 Coleman, J., Diamond, I. T. and Winer, J. A., The visual cortex of the opossum: the retrograde transport of horseradish peroxidase to the lateral geniculate and lateral posterior nuclei, Brain Research, 137 (1977) 233-252. 5 Diirsteler, M. R., Blakemore, C. and Garey, L. J., Projections to the visual cortex in the golden hamster, J. comp. NeuroL, 183 (1979) 185-204. 6 Gallardo, L., Mottles, M., Vera, L., Carrasco, M., Torrealba, F., Montero, V. M. and PintoHamuy, T., Failure by rats to learn a visual conditional discrimination after lateral peristriate cortical lesions, PhysioL Psychol., 7 (1979) 173-177. 7 Garey, L. J. and Powell, T. P. S., An experimental study of the lateral geniculate cortical pathway in the cat and monkey, Proc. roy. Soc. B, 119 (1971) 41-63. 8 Glendenning, K. K., Kofron, E. A. and Diamond, I. T., Laminar organization of the projections of the lateral geniculate nucleus to the striate cortex in Galago, Brain Research, 105 (1976) 538546.
209 9 Gould, H. J., III. Hall, W. C. and Ebner, F. F., Connections of the visual cortex in the hedgehog (Paraechinus hypomelas). I. Thalamocortical projections, J. comp. Neurol., 177 (1978) 445-472. 10 Graham, R. C., Jr. and Karnovsky, M. J., The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique, J. Histochem. Cytochem., 14 (1966) 291-302. I 1 Harting, J. K., Diamond, I. T. and Hall, W. C., Anterograde degeneration study of the cortical projections of the lateral geniculate and pulvinar nuclei in the tree shrew, J. comp. Neurol., 150 (1973) 393-440. 12 Hubel, D. H. and Wiesel, T. N., Laminar and columnar distribution of the geniculocortical fibers in the macaque monkey, J. comp. Neurol., 146 (1972) 421-450. 13 Hughes, H. C., Anatomical and neurobehavioral investigations concerning the thalamo-cortical organization of the rat's visual system, J. comp. Neurol., 175 (1977) 311-336. 14 Krieg, W. J. S., Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas, J. comp. Neurol., 84 (1946) 221-276. 15 Krieg, W. J. S., Connections of the cerebral cortex. II. The albino rat. B. Structure of the cortical areas, J. comp. neurol., 84 (1946) 277-323. 16 Lashley, K. S., The mechanism of vision. VIII. The projection of the retina upon the cerebral cortex of the rat, J. comp. neurol., 60 (1934) 57-80. 17 Lashley, K. S., Thalamo-cortical connections of the rat's brain, J. comp. Neurol., 75 (1941) 67-121. 18 LeVay, S. and Gilbert, C. D., Laminar patterns of geniculo-cortical projection in the cat, Brain Research, 113 (1976) 1-19. 19 McDaniel, W. F., McDaniel, S. E. and Thomas, R. K., Thalamocortical projections to the temporal and parietal association cortices in the rat, Neurosci. Lett., 7 (1978) 121-125. 20 Mesulam, M. M., Tetramethyl benzidine for horseradish peroxidase neuro-histochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents, J. Histochem. Cytochem., 26 (1978) 106-117. 21 Montero, V. M., Bravo, H. and Fernandez, V., Striate-peristriate corticocortical connections in the albino and gray rat, Brain Research, 53 (1973) 202-207. 22 Montero, V. M., Rojas, A. and Torrealba, F., Retinal organization of striate and peristriate visual cortex in the albino rat, Brain Research, 53 (1973) 197-201. 23 Niimi, K. and Sprague, J. M., Thalamo-cortical organization of the visual system in the cat, J. comp. Neurol., 138 (1970) 219-250. 24 Olavarria, J., A horseradish peroxidase study of the projections from the latero-posterior nucleus to three lateral peristriate areas in the rat, Brain Research, 173 (1979) 137-141. 25 Olavarria, J. and Torrealba, F., The effects of acute lesions of the striate cortex on the retinotopic organization of the lateral peristriate cortex in the rat, Brain Research, 151 (1978) 386-391. 26 Ribak, C. E. and Peters, A., An autoradiographic study of the projections from the lateral geniculate body of the rat, Brain Research, 92 (1975) 341-368. 27 Robson, J. A. and Hall, W. C., The organization of the pulvinar in the grey squirrel (Sciurus carolinensis). II. Synaptic organization and comparisons with the dorsal lateral geniculate nucleus, J. comp. Neurok, 173 (1977) 389-416. 28 Stone, J. and Dreher, B., Projection of the X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of the visual cortex, J. NeurophysioL, 36 (1973) 551-567.