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Cortical neurons in and around the Clare-Bishop area related with lens accommodation in the cat
Brain Research, 225 (1981) 195-199 Elsevier/North-Holland Biomedical Press
195
Cortical neurons in and around the Clare-Bishop area related with lens accommodation in the cat
TAKEHIKO BANDO, KENJI TSUKUDA, NOBUHIKO YAMAMOTO, JUN MAEDA and NAKAAKIRA TSUKAHARA Department of Physiology, Yamanashi Medtcal School, Tamaho, Nakakoma, Yamanashi 409-38, Department of Biophysical Engineering, Faculty of Engineering Science, Osaka University, Toyonaka, Osaka 560 and The National Institute for Physiological Sciences, Okazaki 444, Aichi (Japan)
(Accepted August 6th, 1981) Key words: lens accommodation - - spontaneous accommodation - - Clare-Bishop area - - lateral
suprasylvian visual area - - cat
Single-unit discharges in the cat Clare-Bishop area were correlated with spontaneous accommodation responses. No appreciable change was found in accommodation responses evoked by stimulating the Clare-Bishop area, when cerebellar outflow was blocked reversibly by cooling the superior cerebellar peduncle. It is suggested, therefore, that the Clare-Bishop area plays an important role in the lens accommodation system through a pathway independent from that of the cerebellum. Dynamic properties of the lens accommodation system have been studied in earlier work on humans using high-speed infrared optometry1,11,16. The peripheral mechanisms of lens accommodation, including the innervation of ciliary muscles, are established1; and recently the physiological properties of oculomotor parasympathetic neurons controlling lens accommodation have been described a. Less is known about the central neuronal mechanisms involved in lens accommodation. However, recently, it was found that the cerebellum participates in the control of this process 2,7,9. In the present study, single units are recorded in the Clare-Bishop area of cat visual association cortex in an attempt to investigate the possibility of cerebral participation in lens accommodation. It will be shown that some units discharge in temporal correlation with spontaneously occurring lens accommodation. Furthermore, based on cerebellar cooling during stimulation of the Clare-Bishop area, it will be suggested that the cerebral influence on lens accommodation is mediated by a pathway different from the previously reported cerebellar pathway2,7, 9. Thirteen cats were anesthetized with a-chloralose and were immobilized by pancuronium bromide (Mioblock, Organon). Lens accommodation of the left eye was monitored continuously by a high-speed infrared optometer in a dark roomS, 7. The left pupil was paralyzed with L-phenylephrine chloride. Tungsten electrodes were used for recording single unit activities and for microstimulation. Electrodes were driven by 0006-8993/81/0000-0000/$02.50 © Elsevier/North-Holland Biomedical Press
196 0.5D
A
B
ACCOM. N=23
C sP,Kes 5~MSEC OPTOMETER"
~,~-Z~CG
~
~
SCN
I
I
I
I
J
I
A30 20 10 0 1'10 D
HISTOGRAM ~
I h
20use
. !
Fig. 1. A: a schematic diagram of the experimental arrangement. CHAMBER, a chamber for hydraulic micromanipulation; CG, ciliary ganglion; CM, ciliary muscle; LS, lateral sulcus; SCN, short ciliary nerve; SSS, medial and posterior suprasylvian sulci; III, the oculomotor nerve. Numbers below show stereotaxic coordinates. B: spontaneous accommodation responses superimposed 23 times with reference to the onset time of each response. C: times of occurrence of spike potentials recorded simultaneously with the accommodation response shown in B. Each single bar shows the occurrence of a spike potential in 2 ms, and bars with double length show two spike potentials in 2 ms. D: the histogram of spike potentials. Bin width is 20 ms. Vertical dotted lines in B and D show the onset time of the accommodation response. a hydraulic manipulator (Narishige, MO-95) in a closed chamber filled with liquid paraffin. Accommodation responses and extracellularly recorded spike potentials were stored in a data-recorder for off-line computer data-processing 3. In several experiments, a cooling probe 17 was inserted into the superior cerebellar peduncle to block cerebellar outflow, reversibly, by cooling. The location of single units was confirmed in Nissl-stained histological sections (Fig. 2B). The experimental arrangement is shown in Fig. 1A. Units were sought in the medial and lateral bank of the middle suprasylvian sulcus and in the crown of the suprasylvian gyru s. Spontaneously occurring accommodation responses were recorded simultaneously with spike potentials of the suprasylvian cortical neurons. Twenty-one single units were found whose discharge was correlated with accommodation responses. In Fig. 1B, 23 spontaneous accommodation responses are superimposed, with reference to the onset time of each response. The times of occurrence of spike potentials simultaneously recorded with accommodation responses are shown in C, and the histogram of spike potentials is shown in D. The number of spike potentials in the histogram increased, on the average, 290 ms (S.D. 60 ms, n = 21) before the onset times of accommodation responses. The location of 20 out of 21 accommodation-correlated units was confirmed in histological sections. Most of them were found in the medial bank of the middle suprasylvian sulcus (the Clare-Bishop areaS), extending rostrocaudally between stereotaxic coordinates A7.0 and A2.0 (Fig. 2(]). A few of them were found in the crown of the suprasylvian gyrus.
197
A
C
/'/'
AT.0
A50
A5.0
~ss
~
B A3.0
5 mm m
Fig. 2. A: a top view of the cerebrum. Three dotted lines correspond to the levels of the 3 frontal planes shown in C. LS, lateral sulcus, MSS, medial suprasylvian sulcus. B: photomicrograph of a Nissl-stained histological section. The oblique arrow points to the marking made by injecting DC current through the recording microelectrode. Bar 1.0 ram. C: the location of units whose discharge was correlated with accommodation responses. They are pooled in 3 frontal planes at the levels of stereotaxic coordinates, A7.0, A5.0 and A3.0. Accommodation responses were evoked by microstimulation at the points marked by filled circles and were not evoked at the points marked by open circles. By microstimulation with current pulses of less than 100/~A through the recording microelectrode, accommodation responses were evoked at the recording sites of 10 out of 12 units, which were found between A5.0 and A2.0 (filled circles in Fig. 2C). On the other hand, in the anterior part of this area (A7.0 and A6.0), accommodation responses were elicited at only 2 out of 8 recording sites (open circles in Fig. 2C). There is a tendenoy for accommodation-correlated neurons in the middle and posterior parts of the Clare-Bishop area to be found in superficial positions. Since cerebellar participation has already been reported in the lens accommodation system 2,7,9, the possibility was tested that neurons in the Clare-Bishop area play a role in lens accommodation through the cerebellum. The superior cerebellar peduncle was reversibly cooled by a cooling probe 17 inserted into it. The accommodation responses evoked by bipolar stimulation of the interpositus nucleus of the cerebellum disappeared several minutes after the onset of cooling, and they recovered completely
198 about 10 min after the cessation of cooling. Accommodation responses evoked by cortical stimulation were sampled for 8 min before, during and after cooling, and compared using off-line computer data-processing8. No appreciable change was induced by cerebellar cooling in the accommodation response evoked by stimulating the Clare-Bishop area, whereas the cerebellarly induced accommodation response was completely abolished (Fig. 3). It is suggested, based on these results, that neurons in the Clare-Bishop area participate in the lens accommodation system through a pathway independent from that of the cerebellum. Only a few studies are known on the activities of the cerebral cortex correlated with lens accommodation. JampeP 0 reported increased lens accommodation, using retinoscopy, when he stimulated the surface of areas 19 and 22 around the superior temporal sulcus in monkey cerebral cortex. Elul and Marchiafava6 studied the correlation between changes in the EEGs of alert cats and dynamic responses of lens accommodation, observed using a high-speed infrared optometer. However, no systematic study on the activity of cerebral cortical neurons controlling lens accommodation is known. The lateral suprasylvian visual area, or the Clare-Bishop area, has been the target of many physiological and morphological studiesis. The retinotopic organization has been well documented13. Responses of single neurons to visual stimuli were studied4,S,14,15 and most of them respond best to a target moving at high-speed, have large receptive fields, and show direction selectivity. Because of these properties, it is suggested that these neurons in the lateral suprasylvian visual area play a role in analyzing moving targets in the visual space, rather than in the perception of shape of visual targets 4,14. Other neurons have been reported in and around the Clare-Bishop
BEFORE COOL I NG
DURING COOLI NG
AFTER COOL I NG
CEREBELLUM /~ =
0.2D
~
500 msec
CEREBRUM N= 29
Fig. 3. The effect of cooling the superior cerebellar peduncle on the evoked accommodation response. Accommodation responses were evoked by stimulating the interpositus nucleus of the cerebellum (the upper row) or the Clare-Bishop area (the lower row). A specially designed computer program was used to superimpose accommodation responses. The number of superimpositions is shown at the left(N). In the left, middle and right column, accommodation responses sampled before, during and after cooling are shown, respectively. An arrow in each trace shows the timing of the stimulus.
199 a r e a which discharge in c o r r e l a t i o n with saccadic eye m o v e m e n t in the d a r k 12. S o m e o f t h e m d i d n o t r e s p o n d with p h o t i c stimuli, a n d it is suggested t h a t they d e t e r m i n e eye p o s i t i o n 12. T h e present r e p o r t suggests t h a t p r e - p r o g r a m m e d n e u r o n a l activities o f the lens a c c o m m o d a t i o n system are also present in the C l a r e - B i s h o p area. T h e y are possibly related to fixation following saccadic eye m o v e m e n t . H o w e v e r , it is also possible t h a t they c o o p e r a t e with slow p u r s u i t eye m o v e m e n t , o r p l a y a role in the center o f the n e a r response 1, c o o r d i n a t i n g lens a c c o m m o d a t i o n , convergent eye m o v e m e n t a n d constrict i o n o f the pupil. W e t h a n k Miss K. K a t a y a m a for technical assistance in p r e p a r i n g histological material. This w o r k was s u p p o r t e d by grants f r o m the J a p a n e s e M i n i s t r y o f E d u c a t i o n , Science a n d Culture. 1 Alpern, M., Accommodation. In H. Davson (Ed.), The Eye, Vol. 3, Muscular Mechanisms. Academic Press, New York, 1969, pp. 217-249. 2 Bando, T., Ishihara, A. and Tsukahara, N., Interpositus neurons controlling lens accomodation, Proc. Jap. Acad., 55 (1979) 153-156. 3 Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. and Tsukahara, N., Mesencephalic neurons controlling lens accommodation in the cat, Brain Research, 213 (1981) 201-204. 4 Camarda, R. and Rizzolatti, G., Visual receptive fields in the lateral suprasylvian area (ClareBishop area) of the cat, Brain Research, 101 (1976) 427-443. 5 Campbell, F. W. and Robson, J. G., High-speed infrared optometer, J. Opt. Soc. Amer., 49 (1959) 268-272. 6 Elul, R. and Marchiafava, P. L., Accommodation of the eye as related to behavior in the cat, Arch. ital. Biol., 102 (1964) 616-644. 7 Hosoba, M., Bando, T. and Tsukahara, N., The cerebellar control of accommodation of the eye in the cat, Brain Research, 153 (1978) 495-505. 8 Hubel, D. H. and Wiesel, T. N., Visual area of the lateral suprasylvian gyrus (Clare-Bishop area) of the cat, J. Physiol. (Lond.), 202 (1969) 251-260. 9 Hultborn, H., Mori, K. and Tsukahara, N., Cerebellar influence of parasympathetic neurons innervating intraocular muscles, Brain Research, 159 (1978) 269-278. 10 Jampel, R. S., Convergence, divergence, pupillary reactions and accommodation of the eyes from faradic stimulation of the macaque brain, J. comp. Neurol., 115 (1960) 371-400. 11 Kasai, T., Unno, M., Fujii, K., Sekiguchi, M. and Shinohara, K., Dynamic characteristics of human eye accommodation system, Technol. Rep. Osaka Univ., 21 (1971) 569-586. 12 Komatsu, Y., Shibuki, K. and Toyama, K., Responses of neurons in and around the ClareBishop area during photic stimulation and eye movements of the cat, Neurosci. Lett., Suppl. 4 (1980) $69. 13 Palmer, L. A., Rosenquist, A. C. and Tusa, R. J., The retinotopic organization of lateral suprasylvian visual areas in the cat, J. comp. Neurol., 177 (1978) 237-256. 14 Toyama, K. and Kozasa, T., Responses of cat's Clare-Bishop cells to three-demensional visual stimuli, NeuroscL Lett. Suppl. 6 (1981) Sl16. 15 Spear, P. D. and Baumann, T. P., Receptive-field characteristics of single neurons in the lateral suprasylvian visual area of the cat, J. NeurophysioL, 38 (1975) 1403-1420. 16 Stark, L., Neurological Control Systems--Studies in Bioengineering, Plenum Press, New York, 1968, pp. 185-230. 17 Tsukahara, N., Bando, T., Murakami, F. and Ozawa, N., Control of the cerebellar reverberatory activities by local cooling of the cerebellar peduncles. In M. Ito, N. Tsukahara, K. Kubota and K. Yagi (Eds.), Integrative Control Functions of the Brain, VoL 1, Kodansha, Tokyo Elsevier/North-Holland, Amsterdam 1978, pp. 439--440. 18 Van Essen, D. C., Visual areas of the mammalian cerebral cortex, Ann. Rev. Neurosci., 2 (1979) 227-263.
195
Cortical neurons in and around the Clare-Bishop area related with lens accommodation in the cat
TAKEHIKO BANDO, KENJI TSUKUDA, NOBUHIKO YAMAMOTO, JUN MAEDA and NAKAAKIRA TSUKAHARA Department of Physiology, Yamanashi Medtcal School, Tamaho, Nakakoma, Yamanashi 409-38, Department of Biophysical Engineering, Faculty of Engineering Science, Osaka University, Toyonaka, Osaka 560 and The National Institute for Physiological Sciences, Okazaki 444, Aichi (Japan)
(Accepted August 6th, 1981) Key words: lens accommodation - - spontaneous accommodation - - Clare-Bishop area - - lateral
suprasylvian visual area - - cat
Single-unit discharges in the cat Clare-Bishop area were correlated with spontaneous accommodation responses. No appreciable change was found in accommodation responses evoked by stimulating the Clare-Bishop area, when cerebellar outflow was blocked reversibly by cooling the superior cerebellar peduncle. It is suggested, therefore, that the Clare-Bishop area plays an important role in the lens accommodation system through a pathway independent from that of the cerebellum. Dynamic properties of the lens accommodation system have been studied in earlier work on humans using high-speed infrared optometry1,11,16. The peripheral mechanisms of lens accommodation, including the innervation of ciliary muscles, are established1; and recently the physiological properties of oculomotor parasympathetic neurons controlling lens accommodation have been described a. Less is known about the central neuronal mechanisms involved in lens accommodation. However, recently, it was found that the cerebellum participates in the control of this process 2,7,9. In the present study, single units are recorded in the Clare-Bishop area of cat visual association cortex in an attempt to investigate the possibility of cerebral participation in lens accommodation. It will be shown that some units discharge in temporal correlation with spontaneously occurring lens accommodation. Furthermore, based on cerebellar cooling during stimulation of the Clare-Bishop area, it will be suggested that the cerebral influence on lens accommodation is mediated by a pathway different from the previously reported cerebellar pathway2,7, 9. Thirteen cats were anesthetized with a-chloralose and were immobilized by pancuronium bromide (Mioblock, Organon). Lens accommodation of the left eye was monitored continuously by a high-speed infrared optometer in a dark roomS, 7. The left pupil was paralyzed with L-phenylephrine chloride. Tungsten electrodes were used for recording single unit activities and for microstimulation. Electrodes were driven by 0006-8993/81/0000-0000/$02.50 © Elsevier/North-Holland Biomedical Press
196 0.5D
A
B
ACCOM. N=23
C sP,Kes 5~MSEC OPTOMETER"
~,~-Z~CG
~
~
SCN
I
I
I
I
J
I
A30 20 10 0 1'10 D
HISTOGRAM ~
I h
20use
. !
Fig. 1. A: a schematic diagram of the experimental arrangement. CHAMBER, a chamber for hydraulic micromanipulation; CG, ciliary ganglion; CM, ciliary muscle; LS, lateral sulcus; SCN, short ciliary nerve; SSS, medial and posterior suprasylvian sulci; III, the oculomotor nerve. Numbers below show stereotaxic coordinates. B: spontaneous accommodation responses superimposed 23 times with reference to the onset time of each response. C: times of occurrence of spike potentials recorded simultaneously with the accommodation response shown in B. Each single bar shows the occurrence of a spike potential in 2 ms, and bars with double length show two spike potentials in 2 ms. D: the histogram of spike potentials. Bin width is 20 ms. Vertical dotted lines in B and D show the onset time of the accommodation response. a hydraulic manipulator (Narishige, MO-95) in a closed chamber filled with liquid paraffin. Accommodation responses and extracellularly recorded spike potentials were stored in a data-recorder for off-line computer data-processing 3. In several experiments, a cooling probe 17 was inserted into the superior cerebellar peduncle to block cerebellar outflow, reversibly, by cooling. The location of single units was confirmed in Nissl-stained histological sections (Fig. 2B). The experimental arrangement is shown in Fig. 1A. Units were sought in the medial and lateral bank of the middle suprasylvian sulcus and in the crown of the suprasylvian gyru s. Spontaneously occurring accommodation responses were recorded simultaneously with spike potentials of the suprasylvian cortical neurons. Twenty-one single units were found whose discharge was correlated with accommodation responses. In Fig. 1B, 23 spontaneous accommodation responses are superimposed, with reference to the onset time of each response. The times of occurrence of spike potentials simultaneously recorded with accommodation responses are shown in C, and the histogram of spike potentials is shown in D. The number of spike potentials in the histogram increased, on the average, 290 ms (S.D. 60 ms, n = 21) before the onset times of accommodation responses. The location of 20 out of 21 accommodation-correlated units was confirmed in histological sections. Most of them were found in the medial bank of the middle suprasylvian sulcus (the Clare-Bishop areaS), extending rostrocaudally between stereotaxic coordinates A7.0 and A2.0 (Fig. 2(]). A few of them were found in the crown of the suprasylvian gyrus.
197
A
C
/'/'
AT.0
A50
A5.0
~ss
~
B A3.0
5 mm m
Fig. 2. A: a top view of the cerebrum. Three dotted lines correspond to the levels of the 3 frontal planes shown in C. LS, lateral sulcus, MSS, medial suprasylvian sulcus. B: photomicrograph of a Nissl-stained histological section. The oblique arrow points to the marking made by injecting DC current through the recording microelectrode. Bar 1.0 ram. C: the location of units whose discharge was correlated with accommodation responses. They are pooled in 3 frontal planes at the levels of stereotaxic coordinates, A7.0, A5.0 and A3.0. Accommodation responses were evoked by microstimulation at the points marked by filled circles and were not evoked at the points marked by open circles. By microstimulation with current pulses of less than 100/~A through the recording microelectrode, accommodation responses were evoked at the recording sites of 10 out of 12 units, which were found between A5.0 and A2.0 (filled circles in Fig. 2C). On the other hand, in the anterior part of this area (A7.0 and A6.0), accommodation responses were elicited at only 2 out of 8 recording sites (open circles in Fig. 2C). There is a tendenoy for accommodation-correlated neurons in the middle and posterior parts of the Clare-Bishop area to be found in superficial positions. Since cerebellar participation has already been reported in the lens accommodation system 2,7,9, the possibility was tested that neurons in the Clare-Bishop area play a role in lens accommodation through the cerebellum. The superior cerebellar peduncle was reversibly cooled by a cooling probe 17 inserted into it. The accommodation responses evoked by bipolar stimulation of the interpositus nucleus of the cerebellum disappeared several minutes after the onset of cooling, and they recovered completely
198 about 10 min after the cessation of cooling. Accommodation responses evoked by cortical stimulation were sampled for 8 min before, during and after cooling, and compared using off-line computer data-processing8. No appreciable change was induced by cerebellar cooling in the accommodation response evoked by stimulating the Clare-Bishop area, whereas the cerebellarly induced accommodation response was completely abolished (Fig. 3). It is suggested, based on these results, that neurons in the Clare-Bishop area participate in the lens accommodation system through a pathway independent from that of the cerebellum. Only a few studies are known on the activities of the cerebral cortex correlated with lens accommodation. JampeP 0 reported increased lens accommodation, using retinoscopy, when he stimulated the surface of areas 19 and 22 around the superior temporal sulcus in monkey cerebral cortex. Elul and Marchiafava6 studied the correlation between changes in the EEGs of alert cats and dynamic responses of lens accommodation, observed using a high-speed infrared optometer. However, no systematic study on the activity of cerebral cortical neurons controlling lens accommodation is known. The lateral suprasylvian visual area, or the Clare-Bishop area, has been the target of many physiological and morphological studiesis. The retinotopic organization has been well documented13. Responses of single neurons to visual stimuli were studied4,S,14,15 and most of them respond best to a target moving at high-speed, have large receptive fields, and show direction selectivity. Because of these properties, it is suggested that these neurons in the lateral suprasylvian visual area play a role in analyzing moving targets in the visual space, rather than in the perception of shape of visual targets 4,14. Other neurons have been reported in and around the Clare-Bishop
BEFORE COOL I NG
DURING COOLI NG
AFTER COOL I NG
CEREBELLUM /~ =
0.2D
~
500 msec
CEREBRUM N= 29
Fig. 3. The effect of cooling the superior cerebellar peduncle on the evoked accommodation response. Accommodation responses were evoked by stimulating the interpositus nucleus of the cerebellum (the upper row) or the Clare-Bishop area (the lower row). A specially designed computer program was used to superimpose accommodation responses. The number of superimpositions is shown at the left(N). In the left, middle and right column, accommodation responses sampled before, during and after cooling are shown, respectively. An arrow in each trace shows the timing of the stimulus.
199 a r e a which discharge in c o r r e l a t i o n with saccadic eye m o v e m e n t in the d a r k 12. S o m e o f t h e m d i d n o t r e s p o n d with p h o t i c stimuli, a n d it is suggested t h a t they d e t e r m i n e eye p o s i t i o n 12. T h e present r e p o r t suggests t h a t p r e - p r o g r a m m e d n e u r o n a l activities o f the lens a c c o m m o d a t i o n system are also present in the C l a r e - B i s h o p area. T h e y are possibly related to fixation following saccadic eye m o v e m e n t . H o w e v e r , it is also possible t h a t they c o o p e r a t e with slow p u r s u i t eye m o v e m e n t , o r p l a y a role in the center o f the n e a r response 1, c o o r d i n a t i n g lens a c c o m m o d a t i o n , convergent eye m o v e m e n t a n d constrict i o n o f the pupil. W e t h a n k Miss K. K a t a y a m a for technical assistance in p r e p a r i n g histological material. This w o r k was s u p p o r t e d by grants f r o m the J a p a n e s e M i n i s t r y o f E d u c a t i o n , Science a n d Culture. 1 Alpern, M., Accommodation. In H. Davson (Ed.), The Eye, Vol. 3, Muscular Mechanisms. Academic Press, New York, 1969, pp. 217-249. 2 Bando, T., Ishihara, A. and Tsukahara, N., Interpositus neurons controlling lens accomodation, Proc. Jap. Acad., 55 (1979) 153-156. 3 Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. and Tsukahara, N., Mesencephalic neurons controlling lens accommodation in the cat, Brain Research, 213 (1981) 201-204. 4 Camarda, R. and Rizzolatti, G., Visual receptive fields in the lateral suprasylvian area (ClareBishop area) of the cat, Brain Research, 101 (1976) 427-443. 5 Campbell, F. W. and Robson, J. G., High-speed infrared optometer, J. Opt. Soc. Amer., 49 (1959) 268-272. 6 Elul, R. and Marchiafava, P. L., Accommodation of the eye as related to behavior in the cat, Arch. ital. Biol., 102 (1964) 616-644. 7 Hosoba, M., Bando, T. and Tsukahara, N., The cerebellar control of accommodation of the eye in the cat, Brain Research, 153 (1978) 495-505. 8 Hubel, D. H. and Wiesel, T. N., Visual area of the lateral suprasylvian gyrus (Clare-Bishop area) of the cat, J. Physiol. (Lond.), 202 (1969) 251-260. 9 Hultborn, H., Mori, K. and Tsukahara, N., Cerebellar influence of parasympathetic neurons innervating intraocular muscles, Brain Research, 159 (1978) 269-278. 10 Jampel, R. S., Convergence, divergence, pupillary reactions and accommodation of the eyes from faradic stimulation of the macaque brain, J. comp. Neurol., 115 (1960) 371-400. 11 Kasai, T., Unno, M., Fujii, K., Sekiguchi, M. and Shinohara, K., Dynamic characteristics of human eye accommodation system, Technol. Rep. Osaka Univ., 21 (1971) 569-586. 12 Komatsu, Y., Shibuki, K. and Toyama, K., Responses of neurons in and around the ClareBishop area during photic stimulation and eye movements of the cat, Neurosci. Lett., Suppl. 4 (1980) $69. 13 Palmer, L. A., Rosenquist, A. C. and Tusa, R. J., The retinotopic organization of lateral suprasylvian visual areas in the cat, J. comp. Neurol., 177 (1978) 237-256. 14 Toyama, K. and Kozasa, T., Responses of cat's Clare-Bishop cells to three-demensional visual stimuli, NeuroscL Lett. Suppl. 6 (1981) Sl16. 15 Spear, P. D. and Baumann, T. P., Receptive-field characteristics of single neurons in the lateral suprasylvian visual area of the cat, J. NeurophysioL, 38 (1975) 1403-1420. 16 Stark, L., Neurological Control Systems--Studies in Bioengineering, Plenum Press, New York, 1968, pp. 185-230. 17 Tsukahara, N., Bando, T., Murakami, F. and Ozawa, N., Control of the cerebellar reverberatory activities by local cooling of the cerebellar peduncles. In M. Ito, N. Tsukahara, K. Kubota and K. Yagi (Eds.), Integrative Control Functions of the Brain, VoL 1, Kodansha, Tokyo Elsevier/North-Holland, Amsterdam 1978, pp. 439--440. 18 Van Essen, D. C., Visual areas of the mammalian cerebral cortex, Ann. Rev. Neurosci., 2 (1979) 227-263.