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A direct afferent visual pathway from the nucleus of the optic tract to the inferior olive in the cat
150
Brain Research, I 15 (I 976) 150 153 '{i) Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
A direct afferent visual pathway from the nucleus of the optic tract to the inferior olive in the cat
K.-P. H O F F M A N N , K. B E H R E N D and A. S C H O P P M A N N
lnstitut fiir Zoologie der Johannes Gutenberg-Universitiit, Arbeitsgruppe .Ill (Biophysik), Mainz (G.F.R.) (Accepted June 24th, 1976)
Recent studies have described a class of cells in the nucleus of the optic tract (NOT) of the rabbit 2 and the eaO as having properties which make it seem very likely that they are the essential visual afferents feeding into reflexes which serve to stabilize the overall retinal image. On the other hand, these findings in the NOT agree in many points with those for a visually activated climbing fiber input to the rabbit's vestibulo-cerebellums. The pretectal area around the N O T has been identified anatomically as a source of fibers projecting to the ipsilaterat dorsal cap of the inferior olive in the cat and in the rabbit 6. Neuroanatomical and neurophysiological studies have shown that cells in the caudal part of the dorsal cap project to the nodulus and fiocculus of the cerebellum and have visual response properties such as reported for the N O T cells and the climbing fiber input to the rabbit's vestibulo-cerebelluml, 5. The aim of the present study is to show with physiological methods whether there is a projection from the units in the NOT described in our recent study 4 to the inferior olive. To this end we recorded cells in the NOT and stimulated the inferior olive electrically to see whether an antidromlc action potential could be elicited. Methods for recording from units in the N O T and for visual stimulation were the same as described previously 4,7. Cats were initially anesthetized with Trapanal (i.v. injection of 10-20 mg), immobilized with Flaxedil and artificially respirated with nitrous oxide and oxygen (70 ~ : 30 ~o). Large random noise patterns projected onto a tangent screen by a slide projector via a double mirror system served as visual stimuli. These patterns were moved along a circular path without changing their orientation. The cells' responses were analysed by on-line computation of average response histograms 7(Fig. 1). One pair of electrodes was stereotactically inserted into the inferior olive ipsilateral to the NOT from which recordings were to be made. The placement of the stimulating electrodes was checked by recording the climbing fiber field potential in the cerebellar cortex a. A second pair of stimulating electrodes were placed in the optic chiasma (OX). NOT cells were located stereotactically and recorded with Insl-X varnished tungsten electrodes. All stimulating sites in the inferior olive and recording sites in the N O T were verified histologically. In 6 cats, 110 visually influenced units
15l loo
[spikes]
oo
A
90 °
18o °
270 °
oo
9o °
18°°
4
OO
100 [ spikes/s]
270 °
c
o
4
6
8
[ms]
Fig. 1. Identification of cells in the nucleus of optic tract (NOT) by their visual responses (A, B) and latency to electrical stimulation of the optic chiasma (OX) (C). A : average response histogram of one NOT cell's discharge during continuous stimulation by a large Julesz pattern moving on a circular path. Abscissa represents time and the direction in which the pattern moves. 0 ~' and starting time: right to left or towards the periphery of the visual field, 90°: upwards, 180°: left to right or towards the center of the visual field, 270 ° : downwards. Time for a movement through all directions (360 °) length of abscissa: 12.5 sec. Binwidth, 50 msec, 250 bins. Velocity of pattern movement along the circular path: 3.5°/sec. Horizontal line: level of spontaneous activity. Ordinate: discharge frequency in spikes/ sec. B: polar histogram showing the directional sensitivity of the same cell as in A. Data from A are smoothed over 7 bins by a Gaussian weighting function. Directions of movement as in A. Discharge frequency given on the 0 ° axis is scaled as in A. Circle represents spontaneous discharge level. C: poststimulus time histogram of orthodromic latencies in NOT cells after OX stimulation. Binwidth 50 /~sec. Stimulus is applied at 0 msec. Abscissa is scaled in msec. Note the three peaks due to triple discharges after one electrical stimulus.
were isolated in the pretectum and in the superior colliculus. The criteria given previously z,4 were used to identify 28 N O T cells in 4 penetrations. (l) Large patterns rich in contour are more effective stimuli than single spots or lines. (2) The cells were direction selective and preferred movement from the periphery to the center of the visual field. Fig. 1A shows the typical response of a N O T cell to a Julesz pattern moving counterclockwise along a circular path, thus presenting all possible directions of motion. As one can see in the polar histogram (Fig. 1B), the peak activity is concentrated around the region of horizontal movement from right to left,
152 i.e., f r o m the p e r i p h e r y to the center in the c a t ' s visual field. All 28 cells showed this preference. (3) O p t i m a l stimulus velocities in the preferred direction were within a range o f 1-10°/sec and, in m o s t cases, the cells r e s p o n d e d strongly to even slower m o t i o n o f the stimulus pattern. (4) L a t e n c y to O X s t i m u l a t i o n lay between 4 a n d 6 msec a n d d o u b l e o r triple discharges to single electrical shocks were c o m m o n (Fig. 1C). Latencies were c o m p a t i b l e with W-fiber i n p u t from the retina to all these cells 4. The results o f electrical s t i m u l a t i o n o f the inferior olive are shown in Fig. 2. The a n t i d r o m i c c h a r a c t e r o f the a c t i o n p o t e n t i a l i n v a r i a b l y elicited by the electrical stimulus in the inferior olive was verified by three criteria: (1) the fixed latency o f the spike with a variability o f less than at: 50/zsec (Fig. 2A); (2) the c o n s t a n t occurrence o f the spike at s t i m u l a t i o n frequencies as high as 100/sec; a n d (3) an o r t h o d r o m i c spike o b l i t e r a t e d the a n t i d r o m i c spike whenever the f o r m e r p r e c e d e d the l a t t e r by less t h a n twice the interval between s t i m u l a t i o n o f the inferior olive a n d the a n t i d r o m i c response (collision test, see Fig. 2B). A l t h o u g h the s a m p l e o f 28 cells (Fig. 2C) seems very limited, it was a consistent
2
3
4
5
(ms')
Fig. 2. Antidromic action potentials after electrical stimulation of the inferior olive recorded in cells of the nucleus of the optic tract (NOT). A: post-stimulus time histogram of NOT spikes after electrical stimuli applied to inferior olive. Abscissa is scaled in msec (ms), binwidth 10 #sec; ordinate gives the counts of action potentials. Mean latency: 1.4 msec. B: collision test demonstrated in 8 oscilloscope traces. Abscissa is scaled in msee (ms). Arrow indicates stimulus artifact, negative numbers give time before electrical stimulation, positive numbers give time after stimulation. Traces 1, 2, 3, 6 and 7 show antidromic action potentials at a stable latency of 1.1 msec. In trace 6 ortbodromic spike precedes inferior olive stimulation by more than the antidromic latency. The antidromic spike does not collide. In traces 4, 5 and 8, the antidromic and the orthodromic action potentials collide because the spontaneous spikes precede the antidromic spike by less than twice the antidromic latency. C: latency frequency distribution of 28 NOT cells activated antidromically from inferior olive. Abscissa is scaled in msec (ms), ordinate gives number of cells per 0.2 msec wide latency groups.
153 finding in every experiment that antidromic latencies fell into two groups: the first having latencies o f 0.9-2.9 msec, and the second having latencies f r o m 3.6 to 5.1 msec. There was no correlation between o r t h o d r o m i c (OX) and antidromic latencies, nor has it been possible to relate distinct differences in receptive field properties o f N O T cells to these latency groups so far. The antidromic action potential elicited by stimulation of the inferior olive proved to be an additional criterion for identifying a unit as a N O T cell with the specific properties listed above and for separating these cells as a distinct population from all other units with different receptive fields properties in neighboring and even in the same electrode penetrations. Systematic search revealed that all visually influenced cells in other pretectal nuclei (32 units) and in the superior colliculus (about 50 units) could not be driven antidromically f r o m the inferior olive. These results clearly establish a direct connection between the inferior olive and a class of cells with a specific function in the N O T . This function is to relay information a b o u t the m o v e m e n t o f large patterns f r o m the periphery towards the center o f the visual field. W h e n the cells were binocularly driven, they preferred the same direction in the visual field t h r o u g h the two eyes. Taken together with the visual field properties o f the N O T cells, this projection f r o m them to the inferior olive strongly suggests that they are the only source for the direction selective climbing fiber activity f o u n d in the vestibulo-cerebelluml, 5,8. We thank Mr. N. Beckhaus for secretarial help. This work was supported by D F G Grants H o 450/3 and H o 450/4.
1 Alley, K., Baker, R. and Simpson, J. I., Afferents to the vestibulo-cerebellum and the origin of the visual climbing fibers in the rabbit, Brain Research, 98 (1975) 582-589. 2 Collewijn, H., Direction-selective units in the rabbit's nucleus of the optic tract, Brain Research, 100 (1975) 489-508. 3 Eccles, J. C., Ito, M. and Szent~igothai, J., The Cerebellum as a Neuronal Machine, Springer, Berlin, 1967, p. 175. 4 Hoffmann, K.-P. and Schoppmann, A., Retinal input to direction selective cells in the nucleus tractus opticus of the cat, Brain Research, 99 (1975) 359-366. 5 Maekawa, K. and Simpson, J. I., Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system, J. Neurophysiol., 36 (1973) 649-666. 6 Mizuno, N., Nakamura, Y. and Iwahori, N., An electron microscope study of the dorsal cap of the inferior olive in the rabbit, with special reference to the pretecto-olivary fibers, Brain Research, 77 (1974) 385-395. 7 Schoppmann, A. and Hoffmann, K.-P., Continuous mapping of direction selectivity in the cat's visual cortex, Neurosci. Lett., in press. 8 Simpson, J. I. and Alley, K. E., Visual climbing fiber input to rabbit vestibulo-cerebellum : a source of direction-specific information, Brain Research, 82 (1974) 302-308.
Brain Research, I 15 (I 976) 150 153 '{i) Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
A direct afferent visual pathway from the nucleus of the optic tract to the inferior olive in the cat
K.-P. H O F F M A N N , K. B E H R E N D and A. S C H O P P M A N N
lnstitut fiir Zoologie der Johannes Gutenberg-Universitiit, Arbeitsgruppe .Ill (Biophysik), Mainz (G.F.R.) (Accepted June 24th, 1976)
Recent studies have described a class of cells in the nucleus of the optic tract (NOT) of the rabbit 2 and the eaO as having properties which make it seem very likely that they are the essential visual afferents feeding into reflexes which serve to stabilize the overall retinal image. On the other hand, these findings in the NOT agree in many points with those for a visually activated climbing fiber input to the rabbit's vestibulo-cerebellums. The pretectal area around the N O T has been identified anatomically as a source of fibers projecting to the ipsilaterat dorsal cap of the inferior olive in the cat and in the rabbit 6. Neuroanatomical and neurophysiological studies have shown that cells in the caudal part of the dorsal cap project to the nodulus and fiocculus of the cerebellum and have visual response properties such as reported for the N O T cells and the climbing fiber input to the rabbit's vestibulo-cerebelluml, 5. The aim of the present study is to show with physiological methods whether there is a projection from the units in the NOT described in our recent study 4 to the inferior olive. To this end we recorded cells in the NOT and stimulated the inferior olive electrically to see whether an antidromlc action potential could be elicited. Methods for recording from units in the N O T and for visual stimulation were the same as described previously 4,7. Cats were initially anesthetized with Trapanal (i.v. injection of 10-20 mg), immobilized with Flaxedil and artificially respirated with nitrous oxide and oxygen (70 ~ : 30 ~o). Large random noise patterns projected onto a tangent screen by a slide projector via a double mirror system served as visual stimuli. These patterns were moved along a circular path without changing their orientation. The cells' responses were analysed by on-line computation of average response histograms 7(Fig. 1). One pair of electrodes was stereotactically inserted into the inferior olive ipsilateral to the NOT from which recordings were to be made. The placement of the stimulating electrodes was checked by recording the climbing fiber field potential in the cerebellar cortex a. A second pair of stimulating electrodes were placed in the optic chiasma (OX). NOT cells were located stereotactically and recorded with Insl-X varnished tungsten electrodes. All stimulating sites in the inferior olive and recording sites in the N O T were verified histologically. In 6 cats, 110 visually influenced units
15l loo
[spikes]
oo
A
90 °
18o °
270 °
oo
9o °
18°°
4
OO
100 [ spikes/s]
270 °
c
o
4
6
8
[ms]
Fig. 1. Identification of cells in the nucleus of optic tract (NOT) by their visual responses (A, B) and latency to electrical stimulation of the optic chiasma (OX) (C). A : average response histogram of one NOT cell's discharge during continuous stimulation by a large Julesz pattern moving on a circular path. Abscissa represents time and the direction in which the pattern moves. 0 ~' and starting time: right to left or towards the periphery of the visual field, 90°: upwards, 180°: left to right or towards the center of the visual field, 270 ° : downwards. Time for a movement through all directions (360 °) length of abscissa: 12.5 sec. Binwidth, 50 msec, 250 bins. Velocity of pattern movement along the circular path: 3.5°/sec. Horizontal line: level of spontaneous activity. Ordinate: discharge frequency in spikes/ sec. B: polar histogram showing the directional sensitivity of the same cell as in A. Data from A are smoothed over 7 bins by a Gaussian weighting function. Directions of movement as in A. Discharge frequency given on the 0 ° axis is scaled as in A. Circle represents spontaneous discharge level. C: poststimulus time histogram of orthodromic latencies in NOT cells after OX stimulation. Binwidth 50 /~sec. Stimulus is applied at 0 msec. Abscissa is scaled in msec. Note the three peaks due to triple discharges after one electrical stimulus.
were isolated in the pretectum and in the superior colliculus. The criteria given previously z,4 were used to identify 28 N O T cells in 4 penetrations. (l) Large patterns rich in contour are more effective stimuli than single spots or lines. (2) The cells were direction selective and preferred movement from the periphery to the center of the visual field. Fig. 1A shows the typical response of a N O T cell to a Julesz pattern moving counterclockwise along a circular path, thus presenting all possible directions of motion. As one can see in the polar histogram (Fig. 1B), the peak activity is concentrated around the region of horizontal movement from right to left,
152 i.e., f r o m the p e r i p h e r y to the center in the c a t ' s visual field. All 28 cells showed this preference. (3) O p t i m a l stimulus velocities in the preferred direction were within a range o f 1-10°/sec and, in m o s t cases, the cells r e s p o n d e d strongly to even slower m o t i o n o f the stimulus pattern. (4) L a t e n c y to O X s t i m u l a t i o n lay between 4 a n d 6 msec a n d d o u b l e o r triple discharges to single electrical shocks were c o m m o n (Fig. 1C). Latencies were c o m p a t i b l e with W-fiber i n p u t from the retina to all these cells 4. The results o f electrical s t i m u l a t i o n o f the inferior olive are shown in Fig. 2. The a n t i d r o m i c c h a r a c t e r o f the a c t i o n p o t e n t i a l i n v a r i a b l y elicited by the electrical stimulus in the inferior olive was verified by three criteria: (1) the fixed latency o f the spike with a variability o f less than at: 50/zsec (Fig. 2A); (2) the c o n s t a n t occurrence o f the spike at s t i m u l a t i o n frequencies as high as 100/sec; a n d (3) an o r t h o d r o m i c spike o b l i t e r a t e d the a n t i d r o m i c spike whenever the f o r m e r p r e c e d e d the l a t t e r by less t h a n twice the interval between s t i m u l a t i o n o f the inferior olive a n d the a n t i d r o m i c response (collision test, see Fig. 2B). A l t h o u g h the s a m p l e o f 28 cells (Fig. 2C) seems very limited, it was a consistent
2
3
4
5
(ms')
Fig. 2. Antidromic action potentials after electrical stimulation of the inferior olive recorded in cells of the nucleus of the optic tract (NOT). A: post-stimulus time histogram of NOT spikes after electrical stimuli applied to inferior olive. Abscissa is scaled in msec (ms), binwidth 10 #sec; ordinate gives the counts of action potentials. Mean latency: 1.4 msec. B: collision test demonstrated in 8 oscilloscope traces. Abscissa is scaled in msee (ms). Arrow indicates stimulus artifact, negative numbers give time before electrical stimulation, positive numbers give time after stimulation. Traces 1, 2, 3, 6 and 7 show antidromic action potentials at a stable latency of 1.1 msec. In trace 6 ortbodromic spike precedes inferior olive stimulation by more than the antidromic latency. The antidromic spike does not collide. In traces 4, 5 and 8, the antidromic and the orthodromic action potentials collide because the spontaneous spikes precede the antidromic spike by less than twice the antidromic latency. C: latency frequency distribution of 28 NOT cells activated antidromically from inferior olive. Abscissa is scaled in msec (ms), ordinate gives number of cells per 0.2 msec wide latency groups.
153 finding in every experiment that antidromic latencies fell into two groups: the first having latencies o f 0.9-2.9 msec, and the second having latencies f r o m 3.6 to 5.1 msec. There was no correlation between o r t h o d r o m i c (OX) and antidromic latencies, nor has it been possible to relate distinct differences in receptive field properties o f N O T cells to these latency groups so far. The antidromic action potential elicited by stimulation of the inferior olive proved to be an additional criterion for identifying a unit as a N O T cell with the specific properties listed above and for separating these cells as a distinct population from all other units with different receptive fields properties in neighboring and even in the same electrode penetrations. Systematic search revealed that all visually influenced cells in other pretectal nuclei (32 units) and in the superior colliculus (about 50 units) could not be driven antidromically f r o m the inferior olive. These results clearly establish a direct connection between the inferior olive and a class of cells with a specific function in the N O T . This function is to relay information a b o u t the m o v e m e n t o f large patterns f r o m the periphery towards the center o f the visual field. W h e n the cells were binocularly driven, they preferred the same direction in the visual field t h r o u g h the two eyes. Taken together with the visual field properties o f the N O T cells, this projection f r o m them to the inferior olive strongly suggests that they are the only source for the direction selective climbing fiber activity f o u n d in the vestibulo-cerebelluml, 5,8. We thank Mr. N. Beckhaus for secretarial help. This work was supported by D F G Grants H o 450/3 and H o 450/4.
1 Alley, K., Baker, R. and Simpson, J. I., Afferents to the vestibulo-cerebellum and the origin of the visual climbing fibers in the rabbit, Brain Research, 98 (1975) 582-589. 2 Collewijn, H., Direction-selective units in the rabbit's nucleus of the optic tract, Brain Research, 100 (1975) 489-508. 3 Eccles, J. C., Ito, M. and Szent~igothai, J., The Cerebellum as a Neuronal Machine, Springer, Berlin, 1967, p. 175. 4 Hoffmann, K.-P. and Schoppmann, A., Retinal input to direction selective cells in the nucleus tractus opticus of the cat, Brain Research, 99 (1975) 359-366. 5 Maekawa, K. and Simpson, J. I., Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system, J. Neurophysiol., 36 (1973) 649-666. 6 Mizuno, N., Nakamura, Y. and Iwahori, N., An electron microscope study of the dorsal cap of the inferior olive in the rabbit, with special reference to the pretecto-olivary fibers, Brain Research, 77 (1974) 385-395. 7 Schoppmann, A. and Hoffmann, K.-P., Continuous mapping of direction selectivity in the cat's visual cortex, Neurosci. Lett., in press. 8 Simpson, J. I. and Alley, K. E., Visual climbing fiber input to rabbit vestibulo-cerebellum : a source of direction-specific information, Brain Research, 82 (1974) 302-308.