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Somatic sensory projections to the pretectum in the cat
Brain Research, 158 (1978) 445-449 © Elsevier/North-Holland Biomedical Press
445
Short Communications
Somatic sensory projections to the pretectum in the cat
KAREN J. BERKLEY and DEBORAH C. MASH Department of Psychology, Florida State University, Tallahassee, Fla. 32306 (U.S.A.)
(Accepted August 17th, 1978)
It is well known that part of the pretectum receives direct input from the retina6,19 and projects to diencephalic structures which have visual functions6,14,15. Very little is known, however, about pretectal regions which do not appear to be connected to the visual system. The present work demonstrates that, in the cat, some of these regions receive extensive input from the dorsal column nuclei and the somatic sensory portions of the cerebral cortex. Such projections have been mentioned briefly in the rat by other investigators22,31. The data are taken from 4 cats in which the inputs from the gracile and cuneate nuclei, the somatic sensory portions of the cerebral cortex and the retina were compared directly by using a differential labeling strategy in which one input was labeled using autoradiographic tracing methods while another input was labeled using degeneration tracing methods in the same cat. This strategy permitted direct comparisons of the input patterns of the two labeled sources. (See Methods section in ref. 5 for further discussion of this strategy.) Additional data were taken from 20 other cats in which these inputs had been compared with inputs from other sources. The results illustrated in Figs. 1 and 2 compare the regions of pretectum receiving input from retina with the regions receiving input from the gracile and cuneate nuclei and the somatic sensory areas of the cerebral cortex. Similar to the observations of several other investigators, the present re suits show that the retina projects to the nucleus of the optic tract and the olivary nucleus6,19 as well as to a small portion of the posterior pretectal nucleus 19. On the other hand, the gracile and cuneate nuclei and the first and second somatic sensory areas of the cerebral cortex project to overlapping portions of the anterior pretectal n., pars compacta and to small parts of the posterior pretectal n., all regions that appear to lack retinal projections. These results demonstrate that there are major inputs to the pretectum from selected somatic sensory as well as visual sources and that the two regions receiving these inputs are spatially separated within the pretectum. Other authors have shown that, although neither of these pretectal regions appears to project to the primary visual or somatic sensory thalamic relay nuclei (e.g. lateral geniculate n., and ventro-
0 0
A ~
?
a
MGNMV -B. .
Fig. ]. Projectionsto the pretectumfromtheretina,the dorsalcolumnnucleiandthesomatosensory cortex. The charts on the left in A show the location of pre-terminal and terminal labeling in coronal sections at 1 mm intervals through the pretectum of a cat in which the contralateral retinal input (× ×××) was labeled autoradiographically and the input from the contralateral gracile and cuneate nuclei (:. :.) were labeled by ablating the two nuclei. Each chart combines the results from two adjacent sections, one treated autoradiographically, the other treated using silver impregnation methods for degenerating elements. Similar results were observed with the reverse procedure (inject the gracilecuneate n. and remove one eye). In addition, injections or ablations of either the gracile or the cuneate n. in other cats produced similar results. The charts on the right in B are similar to those shown on the left but they are taken from a case in which the inputs from the contralateral gracile n. (:. :.) were labeled autoradiographically and those from both the primary and secondary ipsilateral somatic sensory portions of the cerebral cortex ( _% ) were labeled by ablating those regions. Regions where the two inputs overlap are shown in solid black. Similar results were obtained with the reverse procedure. In addition, injections or ablations of either the primary or the secondary somatic sensory cortical regions in other cats produced labeling in the same portions of the pretectum. Abbreviations: B, brachium of the inferior colliculus; D, n. of Darkschewitsch; LGN, lateral geniculate n. ; LP, lateral posterior complex; MGN, medial geniculate n.; MGNm, magnocellular part of MGN; MGNm-VB, border between ventrobasal complex and M G N m ; ML, medial lemniscus; MML, medial medullary lamina; NIM, medial interlaminar n. of LGN; NPA, anterior pretectal n.; NPAc, pars compacta of NPA; NPAr, pars reticulata of NPA; N PC, n. of the posterior commissure; NPM, medial pretectal n. ; NPO, olivary pretectal n.; NPP, posterior pretectal n.; NTO, n. of the optic tract; P, pulvinar n.; PC, posterior commissure; POI, lateral part of thalamic posterior complex; POm, medial part of thalamic posterior complex; VGL, ventral n. of LGN.
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Fig. 2. Darkfield photomicrographs of the boxed-in area shown in the bottom right of Fig. lB. A: a photomicrograph of an autoradiogram illustrating an above-background grain density in NPAc subsequent to an injection of the contralateral gracile n. with tritiated leucine and proline. B is a photomicrograph of a Fink-Heimer-stained section adjacent to the one shown in A. B: degenerating terminals and pre-terminal fibers subsequent to an ablation of the first and second somatic sensory portions of the cerebral cortex. This degeneration is located within and extends beyond the same portion of NPAc that contains above-background grain densities. Note the blood vessels (numbered 1, 2 and 3) that run through both sections. Calibration shown in A for both A and B is 50/,m. basal complex, respectively), they do project separately to other regions 8,14,1z that appear to be involved in some aspect of visual or somatic sensorimotor function. For example, some of the regions that receive input from the retinal-recipient portions of the pretectum are the ventral lateral geniculate n. (VGL) and the pulvinar complex. These regions not only receive input from and project to other visual structuresT,S, 11, 14,28, but they also contain units which have been shown to process visual stimuli. For VGL, such processing appears to be related to visuomotor 28 and vestibular 23 functions, whereas for the pulvinar complex both visual and somatic sensory processes appear to be involved2, 24. A similar arrangement exists for the somatic sensory portions of the pretectum. For example, some of the regions which receive input from the somatic sensory portions of the pretectum are the zona incerta (ZI), the thalamic reticular n., the thalamic central lateral n. (CL) and the perirubral areaS,14,15. These regions in turn not only receive input from and project to other somatic sensory or motor structures ~,4,1°,13,17,18, but they also contain units which process somatic stimuli. For ZI and the perirubral area, such processing appears to be related to somatomotor integrative functions 12,16, 25,3°,whereas for the thalamic reticular n., such functions are unclear (see review in ref. 17), but may be related to vestibular functions 23. For CL, both visual and somatic sensory processes are involved 1,27. Thus, for both the visual and the somatic sensory systems, a portion of the pretectum appears to form part of a circuit which connects peripheral sensory input with several non-primary, but visual, vestibular or somatic diencephalic and mesencephalic regions. In addition, each of these separate visual and somatic pretectal territories receives descending input from appropriate visual 2° or somatic sensory (Fig. 1) cerebral cortical areas. Such an arrangement, when coupled with other information derived from behavioral and electrophysiological experiments 8,29 and with the fact that large portions of the pretectum receive input from the cerebellum 9, strongly suggests that
448 the functions o f these partially separated, pretectally-centered circuits involve sensorim o t o r i n te g r a ti o n in b o t h somatic and visual sensory realms. This w o r k was s u p p o r t e d by G r a n t s K04-NS-00118 and R01-NS-11892 f r o m the N a t i o n a l Institutes o f Health. W e t h a n k Ms. D. Hellings for technical assistance an d Drs. M. A. Berkley, N. Berman, P. J. H a n d , E. G. Jones a n d H. J. Ralston, III, for constructive c o m m e n t s on earlier versions o f this paper.
1 Albe-Fessard, D. and Kruger, L., Duality of unit discharges from cat centrum medianum in re-
sponse to natural and electrical stimuli, J. Neurophysiol., 25 (1962) 1-20. 2 Avanzini, G., Spreafico, R., Broggi, G., Giovannini, P. and Franceschetti, S., Topographic distribution of visual and somesthesic unitary responses in the Pul-LP complex of the cat, Neurosci. Lett., 4 (1977) 135-143. 3 Berk•ey•K.J.•Pr•jecti•nst•theintra•aminargr•upc•mp•ex•fnuc•eiinthecattha•amus•Neur•sci. Abstr., 2 (1976) 903. 4 Berkley, K. J. and Hand, P. J., Efferent projections of the gracile nucleus in the cat, Brain Research, in press. 5 Berkley, K. J. and Worden, I. G., Projections to the inferior olive of the cat. 1. Comparisons of input from the dorsal nuclei, the lateral cervical nucleus, the spino-olivary pathways, the cerebral cortex and the cerebellum, J. comp. NeuroL, 180 (1978) 237-251. 6 Berman, N., Connections of the pretectum in the cat, J. comp. NeuroL, 174 (1977) 227-254. 7 Berman, N. and Jones E. G., A retino-pulvinar projection in the cat, Brain Research, 134 (1977) 237-248. 8 Chalupa, L. M., Anchel, H. and Lindsley, D. B., Visual input to the pulvinar via lateral geniculate, superior colliculus and visual cortex in the cat, Exp. Neurol., 36 (1972) 449-462. 9 Cohen, D., Chamber, W. and Sprague, J. M., Experimental study of the efferent projections from the cerebellar nuclei to the brainstem of the cat, J. comp. Neurol., 109 (1958) 233-259. 10 Edwards, S. B., The ascending and descending projections of the red nucleus in the cat: An experimental study using an autoradiographic tracing method, Brain Research, 48 (1972) 45-63. 11 Edwards, S. B., Rosenquist, A. C. and Palmer, L. A., An autoradiographic study of ventral lateral geniculate projections in the cat, Brain Research, 72 (1972) 282-287. 12 Frigyesi, T. L., Intracellular studies of neurons in zona incerta during corpus striatum stimulation. In Proc. Int. Union of Physiol. Sci., Vol. 7, 1968, p. 145. 13 Frigyesi, T. L. and Rabin, A., Basal ganglia-diencephalon synaptic relations in the cat. III. An intracellular study of ansa lenticularis, lenticular fasciculus and pallidosubthalamic projection activities, Brain Research, 35 (1971) 67-87. 14 Graybiel, A. M., Some extrageniculate visual pathways in the cat, Invest. Ophthal., 11 (1972) 322332. 15 Itoh, K., Efferent projections of the pretectum in the cat, Exp. Brain Res., 30 (1977) 89-106. 16 Jeneskog, T. and Johansson, H., The rubro-bulbospinal path. A descending system known to influence dynamic fusimotor neurones and its interaction with distal cutaneous afferents in the control of flexor reflex afferent pathways, Exp. Brain Res., 27 (1977) 161-179. 17 Jones, E. G., Some aspects of the organization of the thalamic reticular complex, J. comp. Neurol., 162 (1975) 285-308. 18 Jones, E. G. and Leavitt, R. Y., Retrograde axonal transport and the demonstration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat, and monkey, J. comp. Neurol., 154 (1974) 349-378. 19 Kanaseki, T. and Sprague, J. M., Anatomical organization of pretectal nuclei and tectal laminae in the cat, J. comp. Neurol., 158 (1974) 319-337. 20 Kawamura, S., Sprague, J. M. and Niimi, K., Cortifugal projections from the visual cortices to the thalamus, pretectum and superior colliculus in the cat, J. comp. Neurol., 158 (1974) 339-362. 21 Kruger, L. and Albe-Fessard, D., Distribution of responses to somatic afferent stimuli in the diencephalon of the cat under chlolalose anesthesia, Exp. Neurol., 2 (1960) 442-467.
449 22 Lund, R. D. and Webster, K.E.,Thalamicafferents from the dorsal column nuclei : an experimental study in the rat, J. comp. Neurol., 130 (1967) 301-312. 23 Magnin, M. and Putkonen, P. T. S., A new vestibular thalamic area: electrophysiological study of the thalamic reticular nucleus and of the ventral lateral geniculate complex of the cat, Exp. Brain Res., 32 (1978) 91-104. 24 Mathers, L. H. and Rapisardi, S., Visual and somatosensory receptive fields of neurons in the squirrel monkey pulvinar, Brain Research, 64 (1973) 65-83. 25 Nishioka, S. and Nakahama, H., Peripheral somatic activation of neurons in the cat red nucleus, J. Neurophysiol., 36 (1973) 296-307. 26 Sanides, D., The retinal projection to the ventral lateral geniculate nucleus of the cat, Brain Research, 85 (1975) 313-316. 27 Schlag, J., Lehtinen, I. and Schlag-Rey, M., Neuronal activity before and during eye movements in thalamic internal medullary lamina of the cat, J. NeurophysioL, 37 (1974) 982-995. 28 Spear, P. D., Smith, D. C. and Williams, L. L., Visual receptive-field properties of single neurons in cat's ventral lateral geniculate nucleus, J. Neurophysiol., 40 (1977) 390-409. 29 Sprague, J. M., Berlucchi, G. and Rizzolatti, G., The role of the superior colliculus and pretectum in vision and visually guided behavior. In R. Jung (Ed.), Handbook of Sensory Physiology, Vol. VII/3, Part B., Springer-Verlag, Berlin, 1973, pp. 27-102. 30 Tsubokawa, T. and Sutin, J., Subthalamic neurons: response to joint movement, Brain Research, 10 (1968) 463-466. 31 Wise, S. P. and Jones, E. G., Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex, J. eomp. NehroL, 175 (1977) 129-158.
445
Short Communications
Somatic sensory projections to the pretectum in the cat
KAREN J. BERKLEY and DEBORAH C. MASH Department of Psychology, Florida State University, Tallahassee, Fla. 32306 (U.S.A.)
(Accepted August 17th, 1978)
It is well known that part of the pretectum receives direct input from the retina6,19 and projects to diencephalic structures which have visual functions6,14,15. Very little is known, however, about pretectal regions which do not appear to be connected to the visual system. The present work demonstrates that, in the cat, some of these regions receive extensive input from the dorsal column nuclei and the somatic sensory portions of the cerebral cortex. Such projections have been mentioned briefly in the rat by other investigators22,31. The data are taken from 4 cats in which the inputs from the gracile and cuneate nuclei, the somatic sensory portions of the cerebral cortex and the retina were compared directly by using a differential labeling strategy in which one input was labeled using autoradiographic tracing methods while another input was labeled using degeneration tracing methods in the same cat. This strategy permitted direct comparisons of the input patterns of the two labeled sources. (See Methods section in ref. 5 for further discussion of this strategy.) Additional data were taken from 20 other cats in which these inputs had been compared with inputs from other sources. The results illustrated in Figs. 1 and 2 compare the regions of pretectum receiving input from retina with the regions receiving input from the gracile and cuneate nuclei and the somatic sensory areas of the cerebral cortex. Similar to the observations of several other investigators, the present re suits show that the retina projects to the nucleus of the optic tract and the olivary nucleus6,19 as well as to a small portion of the posterior pretectal nucleus 19. On the other hand, the gracile and cuneate nuclei and the first and second somatic sensory areas of the cerebral cortex project to overlapping portions of the anterior pretectal n., pars compacta and to small parts of the posterior pretectal n., all regions that appear to lack retinal projections. These results demonstrate that there are major inputs to the pretectum from selected somatic sensory as well as visual sources and that the two regions receiving these inputs are spatially separated within the pretectum. Other authors have shown that, although neither of these pretectal regions appears to project to the primary visual or somatic sensory thalamic relay nuclei (e.g. lateral geniculate n., and ventro-
0 0
A ~
?
a
MGNMV -B. .
Fig. ]. Projectionsto the pretectumfromtheretina,the dorsalcolumnnucleiandthesomatosensory cortex. The charts on the left in A show the location of pre-terminal and terminal labeling in coronal sections at 1 mm intervals through the pretectum of a cat in which the contralateral retinal input (× ×××) was labeled autoradiographically and the input from the contralateral gracile and cuneate nuclei (:. :.) were labeled by ablating the two nuclei. Each chart combines the results from two adjacent sections, one treated autoradiographically, the other treated using silver impregnation methods for degenerating elements. Similar results were observed with the reverse procedure (inject the gracilecuneate n. and remove one eye). In addition, injections or ablations of either the gracile or the cuneate n. in other cats produced similar results. The charts on the right in B are similar to those shown on the left but they are taken from a case in which the inputs from the contralateral gracile n. (:. :.) were labeled autoradiographically and those from both the primary and secondary ipsilateral somatic sensory portions of the cerebral cortex ( _% ) were labeled by ablating those regions. Regions where the two inputs overlap are shown in solid black. Similar results were obtained with the reverse procedure. In addition, injections or ablations of either the primary or the secondary somatic sensory cortical regions in other cats produced labeling in the same portions of the pretectum. Abbreviations: B, brachium of the inferior colliculus; D, n. of Darkschewitsch; LGN, lateral geniculate n. ; LP, lateral posterior complex; MGN, medial geniculate n.; MGNm, magnocellular part of MGN; MGNm-VB, border between ventrobasal complex and M G N m ; ML, medial lemniscus; MML, medial medullary lamina; NIM, medial interlaminar n. of LGN; NPA, anterior pretectal n.; NPAc, pars compacta of NPA; NPAr, pars reticulata of NPA; N PC, n. of the posterior commissure; NPM, medial pretectal n. ; NPO, olivary pretectal n.; NPP, posterior pretectal n.; NTO, n. of the optic tract; P, pulvinar n.; PC, posterior commissure; POI, lateral part of thalamic posterior complex; POm, medial part of thalamic posterior complex; VGL, ventral n. of LGN.
447 ,
..... /.
• ~
/J
• /
Fig. 2. Darkfield photomicrographs of the boxed-in area shown in the bottom right of Fig. lB. A: a photomicrograph of an autoradiogram illustrating an above-background grain density in NPAc subsequent to an injection of the contralateral gracile n. with tritiated leucine and proline. B is a photomicrograph of a Fink-Heimer-stained section adjacent to the one shown in A. B: degenerating terminals and pre-terminal fibers subsequent to an ablation of the first and second somatic sensory portions of the cerebral cortex. This degeneration is located within and extends beyond the same portion of NPAc that contains above-background grain densities. Note the blood vessels (numbered 1, 2 and 3) that run through both sections. Calibration shown in A for both A and B is 50/,m. basal complex, respectively), they do project separately to other regions 8,14,1z that appear to be involved in some aspect of visual or somatic sensorimotor function. For example, some of the regions that receive input from the retinal-recipient portions of the pretectum are the ventral lateral geniculate n. (VGL) and the pulvinar complex. These regions not only receive input from and project to other visual structuresT,S, 11, 14,28, but they also contain units which have been shown to process visual stimuli. For VGL, such processing appears to be related to visuomotor 28 and vestibular 23 functions, whereas for the pulvinar complex both visual and somatic sensory processes appear to be involved2, 24. A similar arrangement exists for the somatic sensory portions of the pretectum. For example, some of the regions which receive input from the somatic sensory portions of the pretectum are the zona incerta (ZI), the thalamic reticular n., the thalamic central lateral n. (CL) and the perirubral areaS,14,15. These regions in turn not only receive input from and project to other somatic sensory or motor structures ~,4,1°,13,17,18, but they also contain units which process somatic stimuli. For ZI and the perirubral area, such processing appears to be related to somatomotor integrative functions 12,16, 25,3°,whereas for the thalamic reticular n., such functions are unclear (see review in ref. 17), but may be related to vestibular functions 23. For CL, both visual and somatic sensory processes are involved 1,27. Thus, for both the visual and the somatic sensory systems, a portion of the pretectum appears to form part of a circuit which connects peripheral sensory input with several non-primary, but visual, vestibular or somatic diencephalic and mesencephalic regions. In addition, each of these separate visual and somatic pretectal territories receives descending input from appropriate visual 2° or somatic sensory (Fig. 1) cerebral cortical areas. Such an arrangement, when coupled with other information derived from behavioral and electrophysiological experiments 8,29 and with the fact that large portions of the pretectum receive input from the cerebellum 9, strongly suggests that
448 the functions o f these partially separated, pretectally-centered circuits involve sensorim o t o r i n te g r a ti o n in b o t h somatic and visual sensory realms. This w o r k was s u p p o r t e d by G r a n t s K04-NS-00118 and R01-NS-11892 f r o m the N a t i o n a l Institutes o f Health. W e t h a n k Ms. D. Hellings for technical assistance an d Drs. M. A. Berkley, N. Berman, P. J. H a n d , E. G. Jones a n d H. J. Ralston, III, for constructive c o m m e n t s on earlier versions o f this paper.
1 Albe-Fessard, D. and Kruger, L., Duality of unit discharges from cat centrum medianum in re-
sponse to natural and electrical stimuli, J. Neurophysiol., 25 (1962) 1-20. 2 Avanzini, G., Spreafico, R., Broggi, G., Giovannini, P. and Franceschetti, S., Topographic distribution of visual and somesthesic unitary responses in the Pul-LP complex of the cat, Neurosci. Lett., 4 (1977) 135-143. 3 Berk•ey•K.J.•Pr•jecti•nst•theintra•aminargr•upc•mp•ex•fnuc•eiinthecattha•amus•Neur•sci. Abstr., 2 (1976) 903. 4 Berkley, K. J. and Hand, P. J., Efferent projections of the gracile nucleus in the cat, Brain Research, in press. 5 Berkley, K. J. and Worden, I. G., Projections to the inferior olive of the cat. 1. Comparisons of input from the dorsal nuclei, the lateral cervical nucleus, the spino-olivary pathways, the cerebral cortex and the cerebellum, J. comp. NeuroL, 180 (1978) 237-251. 6 Berman, N., Connections of the pretectum in the cat, J. comp. NeuroL, 174 (1977) 227-254. 7 Berman, N. and Jones E. G., A retino-pulvinar projection in the cat, Brain Research, 134 (1977) 237-248. 8 Chalupa, L. M., Anchel, H. and Lindsley, D. B., Visual input to the pulvinar via lateral geniculate, superior colliculus and visual cortex in the cat, Exp. Neurol., 36 (1972) 449-462. 9 Cohen, D., Chamber, W. and Sprague, J. M., Experimental study of the efferent projections from the cerebellar nuclei to the brainstem of the cat, J. comp. Neurol., 109 (1958) 233-259. 10 Edwards, S. B., The ascending and descending projections of the red nucleus in the cat: An experimental study using an autoradiographic tracing method, Brain Research, 48 (1972) 45-63. 11 Edwards, S. B., Rosenquist, A. C. and Palmer, L. A., An autoradiographic study of ventral lateral geniculate projections in the cat, Brain Research, 72 (1972) 282-287. 12 Frigyesi, T. L., Intracellular studies of neurons in zona incerta during corpus striatum stimulation. In Proc. Int. Union of Physiol. Sci., Vol. 7, 1968, p. 145. 13 Frigyesi, T. L. and Rabin, A., Basal ganglia-diencephalon synaptic relations in the cat. III. An intracellular study of ansa lenticularis, lenticular fasciculus and pallidosubthalamic projection activities, Brain Research, 35 (1971) 67-87. 14 Graybiel, A. M., Some extrageniculate visual pathways in the cat, Invest. Ophthal., 11 (1972) 322332. 15 Itoh, K., Efferent projections of the pretectum in the cat, Exp. Brain Res., 30 (1977) 89-106. 16 Jeneskog, T. and Johansson, H., The rubro-bulbospinal path. A descending system known to influence dynamic fusimotor neurones and its interaction with distal cutaneous afferents in the control of flexor reflex afferent pathways, Exp. Brain Res., 27 (1977) 161-179. 17 Jones, E. G., Some aspects of the organization of the thalamic reticular complex, J. comp. Neurol., 162 (1975) 285-308. 18 Jones, E. G. and Leavitt, R. Y., Retrograde axonal transport and the demonstration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat, and monkey, J. comp. Neurol., 154 (1974) 349-378. 19 Kanaseki, T. and Sprague, J. M., Anatomical organization of pretectal nuclei and tectal laminae in the cat, J. comp. Neurol., 158 (1974) 319-337. 20 Kawamura, S., Sprague, J. M. and Niimi, K., Cortifugal projections from the visual cortices to the thalamus, pretectum and superior colliculus in the cat, J. comp. Neurol., 158 (1974) 339-362. 21 Kruger, L. and Albe-Fessard, D., Distribution of responses to somatic afferent stimuli in the diencephalon of the cat under chlolalose anesthesia, Exp. Neurol., 2 (1960) 442-467.
449 22 Lund, R. D. and Webster, K.E.,Thalamicafferents from the dorsal column nuclei : an experimental study in the rat, J. comp. Neurol., 130 (1967) 301-312. 23 Magnin, M. and Putkonen, P. T. S., A new vestibular thalamic area: electrophysiological study of the thalamic reticular nucleus and of the ventral lateral geniculate complex of the cat, Exp. Brain Res., 32 (1978) 91-104. 24 Mathers, L. H. and Rapisardi, S., Visual and somatosensory receptive fields of neurons in the squirrel monkey pulvinar, Brain Research, 64 (1973) 65-83. 25 Nishioka, S. and Nakahama, H., Peripheral somatic activation of neurons in the cat red nucleus, J. Neurophysiol., 36 (1973) 296-307. 26 Sanides, D., The retinal projection to the ventral lateral geniculate nucleus of the cat, Brain Research, 85 (1975) 313-316. 27 Schlag, J., Lehtinen, I. and Schlag-Rey, M., Neuronal activity before and during eye movements in thalamic internal medullary lamina of the cat, J. NeurophysioL, 37 (1974) 982-995. 28 Spear, P. D., Smith, D. C. and Williams, L. L., Visual receptive-field properties of single neurons in cat's ventral lateral geniculate nucleus, J. Neurophysiol., 40 (1977) 390-409. 29 Sprague, J. M., Berlucchi, G. and Rizzolatti, G., The role of the superior colliculus and pretectum in vision and visually guided behavior. In R. Jung (Ed.), Handbook of Sensory Physiology, Vol. VII/3, Part B., Springer-Verlag, Berlin, 1973, pp. 27-102. 30 Tsubokawa, T. and Sutin, J., Subthalamic neurons: response to joint movement, Brain Research, 10 (1968) 463-466. 31 Wise, S. P. and Jones, E. G., Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex, J. eomp. NehroL, 175 (1977) 129-158.