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Interpositus neuron discharge in relation to a voluntary movement
Brain Research, 121 (1977) 167-172
167
© Elsevier/North-Holland Biomedical Press, Amsterdam - Printed in The Netherlands
Interpositus neuron discharge in relation to a voluntary movement
J. E. BURTON and N. ONODA
Division o[ Neurosciences, City of Hope National Medical Center, Duarte, Calif. 91010 (U.S.A.) (Accepted October 27th, 1976)
It has been suggested that the intermediate zone of the cerebellar cortex, acting through the interpositus nucleus, participates in the control of an evolving movement especially by utilizing sensory information generated by the movement itself a,~. If so, the discharge of interpositus neurons during a movement should reflect the influence of one or more parameters of either the motor output, the motion, or their immediate consequences. The present investigation was undertaken to determine if indeed such an influence could be demonstrated. Cats were trained to perform flexion and extension displacements of the right elbow joint for a food reward. This was accomplished by fastening the wrist to a handle from which a food-delivery tube protruded (Fig. 1). By flexing its elbow joint, the animal could rotate the handle in the vertical plane, thus bringing the end of the food tube to its mouth and receiving a drop of semi-liquid food (chicken liver). In order to obtain another drop, it was first required to return the handle to a mechanical stop, by extending the elbow joint, and to hold the handle against the stop for at least 1 sec. The animal's performance was otherwise self-paced, no signals being given at any time. Also, no stipulations were made as to the speed of the movements. Most animals performed from 600 to 900 flexion and extension movements in a period of 90-120 rain. The handle was mounted on the left side of the cat so that its rotation axis was aligned with the cat's elbow joint. A linear potentiometer was used to measure the angular displacement. The maximum angle of the elbow joint was maintained at approximately 90 ° and the minimum at approximately 60 °, as determined by the position of the mechanical stop and the configuration of the food tube, respectively. Note, however, that the arrest of the flexion displacement was controlled exclusively by the animal, who had to position the end of the food tube properly in order to reach the food with its tongue. Any overshoot of the movement would have resulted in a painful blow to the mouth. The extension movement, on the other hand, was terminated by a mechanical stop. lts arrest was thus largely unintentional. The handle was balanced by adding a counterweight as shown in Fig. 1. Thus, no downward torque was placed on the arm. The load presented to the animal consisted of a minimized frictional component, the inertial load of the forearm-handle complex, and the downward torque of the forearm itself.
168
Ola
4¸
",
~;.
Fig. 1. Task and apparatus. See text for description. CW. counterweight; pot., displacement potentio. meter; FT, food tube; SG -- strain gauges.
The cats were prepared for recording by attaching a fastening device and manipulator base to the skull under general anesthesia. The base was placed stereotaxically into a hole drilled through the interparietal bone overlying the posterior lobe of the cerebellum. The dura was left intacL The activity of single cerebellar neurons was recorded extracellularty, using tungsten microetectrodes. The electrodes were advanced through the dura inside a guide needle which penetrated the dura as the micromanipulator was inserted into its base. Electromyograms of the biceps and triceps muscles were recorded, using pairs of teflon-insulated silver wires inserted prior to each recording session. All data were recorded on magnetic tape for later processing. A Nicotet Instrument Corp. instrument computer, Mod. 1072, was used to average data from individual performances. The discharge of single interpositus units was averaged after first converting the spike trains into impulse density. E M G data were treated in the same manner, each spike being given equal weight regardless of its amplitude. The event used to trigger the averager was the first peak of the velocity. This was obtained by analog differentiation of the displacement waveform, using an operational amplifier. The bin width of the averager was 8 msec. Our intent has been to record from neurons of the nucleus interpositus. For
169
A
d
./I"
B
flexion 0.5
d
sec
extension
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"-.'-" "-~-":--,L._...~,...," '.. ....:j._-?.,.~-...-;'..----.~%.
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Fig. 2. A: average discharge rate (32 trials) of an interpositus neuron (ip) in relation to average elbow flexion displacement (d), velocity (v) and biceps impulse density (bi). No EMG activity was present in the triceps muscle during this movement. B: average discharge rate (18 trials) of another interpositus neuron in relation to extension displacement. A downward torque of 900 gm• cm was added in B. identification of these neurons, we have relied upon reconstruction of electrode tracks from histological sections and micromanipulator readings. In order to facilitate the reconstruction, small coagulations were produced at regular intervals in one track just prior to sacrificing the animal. Most of the recorded units were clearly within the boundaries of the interpositus nucleus. Forty-four units (193 tested, 7 cats) have been isolated whose discharge rate changed consistently in relation to the movement. Fig. 2A shows the averaged data for 32 flexion trials obtained while recording from a single interpositus neuron. Prior to the onset of the displacement (d), the E M G activity of the biceps (bi) increases until sufficient force is generated to overcome the downward torque of the arm-handle complex. The increase in the discharge rate of the interpositus unit (lip) is seen to precede the increase in biceps activity (vertical line 1) and to reach its maximum prior to that of the biceps activity (vertical line 2). Following the onset of the displacement, the discharge rate of the interpositus unit is also seen to change inversely to the velocity of the motion, its lowest value coinciding with the highest value of the velocity (vertical line 3). The behavior of this unit is typical of 30 of the 44 units. In 18 of the above 30 units, the discharge rate also changed with the extensions. However, the fact that the time course of these movements varied considerably from trial to trial prevented the use of data averaging. In order to partially overcome this difficulty, the extension movements were made more consistent by adding a heavy weight to the handle. Fig. 2B shows the averaged data of 18 trials from one unit. Similar results were obtained with 3 other neurons. Although the initial change in
170
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100~ [ •.
I
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'i.
_5.._...
.i '
f
bi
1:.:v"
~'"~.. ,'51:- '_ •
=~,'.
.'-.:--.
I: 1
2
3
0.5
sec
Fig. 3. Average discharge rate (32 trials) of an interpositus neuron (ip) in relation to average e|bow
flexion displacement (d). velocity (v) and biceps impulse density (bi).
biceps activity is not sufficiently abrupt to allow a final conclusion concerning the time relation between this event and the initial change in discharge rate of the interpositus neuron, it can be seen that the unit discharge rate reaches a minimum (vertical line 1) well before the minimum of the biceps activity (vertical line 2). Thereafter, the discharge rate of the neuron changes in parallel with the velocity of the extension, its highest value coinciding with the highest value of that parameter (vertical line 3). The changes in discharge rate of these interpositus neurons before and during extensions were thus opposite m sign to the changes observed before and during flexions. Electrical activity in the triceps muscle was rarely observed during extensions, most probably because these movements could occur passively due to the downward torque provided by the forearm itself. The behavior illustrated in Fig. 3 is that of the remaining 14 interpositus neurons. The average discharge rate of this cell (32 trials) begins to decrease prior to the increase in biceps activity (vertical line 1) and reaches its minimum value in advance of the maximum biceps activity (vertical line 2). Soon after the onset of the flexion displacement, however, the average discharge rate suddenly increases and reaches its highest value slightly in advance of the peak velocity (vertical line 3). At this time, the biceps activity is at a minimum. Thereafter, the discharge of the neuron fluctuates in
17l parallel with the velocity parameter. This behavior is approximately the reciprocal of that illustrated in Fig. 2A. The discharge rate of these 14 units did not change significantly in relation to extension displacements. The data presented in this report are in good agreement with those from previous studies with monkey wrist movementsal, 1~. In both cat and monkey, the first change in discharge rate of an interpositus neuron can be either an increase or a decrease, and there can be several alterations in rate during a single movement. Two differences, however, are apparent. In the monkey, the direction of the first change in rate could be the same or different for movements of opposite direction (flexion vs. extension), whereas, in the cat the direction of the first change was never the same. This difference may be related to differences in the motor pattern. In the cat, flexion was initiated by increased biceps activity and extension by decreased biceps activity (there being no involvement of the triceps), whereas, in the monkey there was considerable co-activation of wrist flexors and extensors during both movements, with the result, for example, that both flexion and extension were associated with increased flexor activity (ref. 11, Fig. 1, 3a). The second difference is that the first change in discharge rate of all of the cat interpositus neurons began before, or coincided with, the first change in biceps activity, whereas in the monkey 58 ~ of the interpositus units changed rate only after the wrist muscles had become active 11. This difference may be related to differences in overall motor pattern. In the monkey, the secondary muscles (upper arm and trunk) did not change activity more than 10 msec before the primary muscles (wrist flexors and extensors) la, whereas in the cat many trunk and shoulder muscles became active well before the biceps or the change in interpositus activity. The earlier activity in the cat interpositus nucleus may well have been associated with this supportive muscle activity and could have been produced by either central activities or feedback from the periphery. To summarize the present data for both types of neuron, it can be stated that, during the motion, the maxima and minima of the unit discharge rate coincide with the peaks of the angular velocity. Moreover, the magnitude of the modulation of the discharge rate is roughly proportional to the magnitude of the velocity parameter. It is concluded, therefore, that there is a strong correlation between the discharge rate of interpositus neurons and the velocity of the motion. Furthermore, it is most likely that this correlation is due to input to the cerebellum generated by rate-sensitive receptors in the moving limb. Indeed, it has been shown that the output of muscle spindles influences neurons in the interpositus nucleus 3 and that the discharge rate of interpositus neurons is related to the velocity of passive elbow displacement (Burton and Onoda, unpublished observations) and to the rate of stretch of forelimb muscles 4. Finally, in the present study, the time relations between the changes in discharge rate of interpositus neurons and the biceps E M G activity are consistent with the idea that the nuclear cell acitivity is involved in regulating the motor output to the biceps throughout the performance of the task. These conclusions are in agreement with the suggestion j,2 that the intermediate zone of the cerebellar cortex and the interpositus nucleus integrates inputs from cerebrocerebellar and spinocerebellar systems to provide an output which continually updates the motor commands in the control of an evolving
172 m o v e m e n t . In this context, it has already been suggested that cerebetlar activities c o n t r i b u t e t o the regulation o f o n g o i n g m o v e m e n t s , especially by utilizing i n p u t data o n the velocity o f the m o t i o n 9,1°. M o r e o v e r , i t has been f o u n d that in the course o f fast m o v e m e n t s , the m o t o r o u t p u t depends c o n t i n u o u s l y on sensory input d a t a an d that this relationship requires the presence o f cerebellar activities 5-8,1°. O u r data are n o t only c o m p a t i b l e with these findings bu t d e m o n s t r a t e t h a t the velocity p a r a m e t e r is represented in the activity o f interpositus neurons. We wish to t h a n k Dr. C. A. T e r z u o l o an d Dr. J. E. Vaughn for their valuable criticism o f the m a n u s c r i p t a n d Mr. R. Barber for the d r a w i n g o f Fig. 1. S u p p o r t e d by N I H R e s e a r c h G r a n t N o . N S 11798 f r o m N I N D S .
1 Allen, G. 1. and Tsukahara, N.. Cerebrocerebetlar communication systems, Physiol. Rev.. 54 (1974) 957-1006. 2 Eccles. J. C.. Circuits in the cerebellar control of movement. Proc. nat. Acad. SoL Wash. ,. 58 (1967J 336-343. 3 Kawaguchi, S. and Ohno, T., Responses of interpositus neurons to inputs from muscle receptors. Exp. Brain Res., 21 (1974) 375-386. 4 MacKay, W. A. and Murphy, J. T., Responses of interpositus neurons to passive muscle stretch, J. Neurophysiol., 27 (1974) 1410-1423. 5 Soechting, J. F., Modeling of a simple motor task m man: motor output dependence on sensory input, Kybernetik, 14 (1973) 25-34. 6 Soechting, J. F., Palminteri, R. and Terzuolo, C. A., Studies on the control of somesimple motor tasks. IV. Relation between parameters of motion and motor output in squirrel monkey, Brain Research, 62 (1973) 247-252, 7 Soechting, J. F., Ranish, N. A., Palminteri, R. and Terzuolo, C. A., Changes m a motor pattern following cerebellar and olivary lesions in the squirrel monkey, Brain Research, 105 (1976) 2144. 8 Terzuolo, C A., Soechting, J. F. and Ranish, N. A., Studies on the control of some motor tasks. V. Changes in motor output following dorsal root section in squirrel monkey, Brain Research. 70 (1974) 521-526. 9 Terzuolo, C. A., Soechting, J. F and Viviani, P., Studies on the control of some simple motor tasks. I. Relations between parameters of movements and EMG activities, Brain Research, 58 (t973) 212-216. 10 Terzuolo, C. A. and Viviani. P., Parameters of motion and EMG activities during some simple motor tasks m normal subjects and cerebellar patients, tn I. S. Cooper, M. Riklan and R. S. Snider 0Eds.). The Cerebellum, Epilepsy, and Behavior, Plenum Press. New York. 1974, pp. 173-215. 11 Thach, W, T., Discharge of cerebellar neurons related to two maintained postures and two prompt movements. I. Nuclear cell output, J. Neurophysiot., 33 (1970) 527-536. 12 Thach, W. T., Coding differences in activity of muscles, motor cortex, and cerebetlar nuclei during a more complex motor task, Neurosci. Abstr.. 1 (1975) 175.
167
© Elsevier/North-Holland Biomedical Press, Amsterdam - Printed in The Netherlands
Interpositus neuron discharge in relation to a voluntary movement
J. E. BURTON and N. ONODA
Division o[ Neurosciences, City of Hope National Medical Center, Duarte, Calif. 91010 (U.S.A.) (Accepted October 27th, 1976)
It has been suggested that the intermediate zone of the cerebellar cortex, acting through the interpositus nucleus, participates in the control of an evolving movement especially by utilizing sensory information generated by the movement itself a,~. If so, the discharge of interpositus neurons during a movement should reflect the influence of one or more parameters of either the motor output, the motion, or their immediate consequences. The present investigation was undertaken to determine if indeed such an influence could be demonstrated. Cats were trained to perform flexion and extension displacements of the right elbow joint for a food reward. This was accomplished by fastening the wrist to a handle from which a food-delivery tube protruded (Fig. 1). By flexing its elbow joint, the animal could rotate the handle in the vertical plane, thus bringing the end of the food tube to its mouth and receiving a drop of semi-liquid food (chicken liver). In order to obtain another drop, it was first required to return the handle to a mechanical stop, by extending the elbow joint, and to hold the handle against the stop for at least 1 sec. The animal's performance was otherwise self-paced, no signals being given at any time. Also, no stipulations were made as to the speed of the movements. Most animals performed from 600 to 900 flexion and extension movements in a period of 90-120 rain. The handle was mounted on the left side of the cat so that its rotation axis was aligned with the cat's elbow joint. A linear potentiometer was used to measure the angular displacement. The maximum angle of the elbow joint was maintained at approximately 90 ° and the minimum at approximately 60 °, as determined by the position of the mechanical stop and the configuration of the food tube, respectively. Note, however, that the arrest of the flexion displacement was controlled exclusively by the animal, who had to position the end of the food tube properly in order to reach the food with its tongue. Any overshoot of the movement would have resulted in a painful blow to the mouth. The extension movement, on the other hand, was terminated by a mechanical stop. lts arrest was thus largely unintentional. The handle was balanced by adding a counterweight as shown in Fig. 1. Thus, no downward torque was placed on the arm. The load presented to the animal consisted of a minimized frictional component, the inertial load of the forearm-handle complex, and the downward torque of the forearm itself.
168
Ola
4¸
",
~;.
Fig. 1. Task and apparatus. See text for description. CW. counterweight; pot., displacement potentio. meter; FT, food tube; SG -- strain gauges.
The cats were prepared for recording by attaching a fastening device and manipulator base to the skull under general anesthesia. The base was placed stereotaxically into a hole drilled through the interparietal bone overlying the posterior lobe of the cerebellum. The dura was left intacL The activity of single cerebellar neurons was recorded extracellularty, using tungsten microetectrodes. The electrodes were advanced through the dura inside a guide needle which penetrated the dura as the micromanipulator was inserted into its base. Electromyograms of the biceps and triceps muscles were recorded, using pairs of teflon-insulated silver wires inserted prior to each recording session. All data were recorded on magnetic tape for later processing. A Nicotet Instrument Corp. instrument computer, Mod. 1072, was used to average data from individual performances. The discharge of single interpositus units was averaged after first converting the spike trains into impulse density. E M G data were treated in the same manner, each spike being given equal weight regardless of its amplitude. The event used to trigger the averager was the first peak of the velocity. This was obtained by analog differentiation of the displacement waveform, using an operational amplifier. The bin width of the averager was 8 msec. Our intent has been to record from neurons of the nucleus interpositus. For
169
A
d
./I"
B
flexion 0.5
d
sec
extension
i
i i
, ,'..
v
[
4-
i.: i " ~j..i , . , v . / ~ ~
lOO I '
!'":": '
"........
i ip
~ :...-::.:--..." !
I.
•-I"o
"
-
/1:
"-.'-" "-~-":--,L._...~,...," '.. ....:j._-?.,.~-...-;'..----.~%.
o ../',.
;:;._:~:~:-,~...j-
bi
--., :-.~ .,. 1 2 3
1
2 3
Fig. 2. A: average discharge rate (32 trials) of an interpositus neuron (ip) in relation to average elbow flexion displacement (d), velocity (v) and biceps impulse density (bi). No EMG activity was present in the triceps muscle during this movement. B: average discharge rate (18 trials) of another interpositus neuron in relation to extension displacement. A downward torque of 900 gm• cm was added in B. identification of these neurons, we have relied upon reconstruction of electrode tracks from histological sections and micromanipulator readings. In order to facilitate the reconstruction, small coagulations were produced at regular intervals in one track just prior to sacrificing the animal. Most of the recorded units were clearly within the boundaries of the interpositus nucleus. Forty-four units (193 tested, 7 cats) have been isolated whose discharge rate changed consistently in relation to the movement. Fig. 2A shows the averaged data for 32 flexion trials obtained while recording from a single interpositus neuron. Prior to the onset of the displacement (d), the E M G activity of the biceps (bi) increases until sufficient force is generated to overcome the downward torque of the arm-handle complex. The increase in the discharge rate of the interpositus unit (lip) is seen to precede the increase in biceps activity (vertical line 1) and to reach its maximum prior to that of the biceps activity (vertical line 2). Following the onset of the displacement, the discharge rate of the interpositus unit is also seen to change inversely to the velocity of the motion, its lowest value coinciding with the highest value of the velocity (vertical line 3). The behavior of this unit is typical of 30 of the 44 units. In 18 of the above 30 units, the discharge rate also changed with the extensions. However, the fact that the time course of these movements varied considerably from trial to trial prevented the use of data averaging. In order to partially overcome this difficulty, the extension movements were made more consistent by adding a heavy weight to the handle. Fig. 2B shows the averaged data of 18 trials from one unit. Similar results were obtained with 3 other neurons. Although the initial change in
170
O
J
100~ [ •.
I
*_p
'i.
_5.._...
.i '
f
bi
1:.:v"
~'"~.. ,'51:- '_ •
=~,'.
.'-.:--.
I: 1
2
3
0.5
sec
Fig. 3. Average discharge rate (32 trials) of an interpositus neuron (ip) in relation to average e|bow
flexion displacement (d). velocity (v) and biceps impulse density (bi).
biceps activity is not sufficiently abrupt to allow a final conclusion concerning the time relation between this event and the initial change in discharge rate of the interpositus neuron, it can be seen that the unit discharge rate reaches a minimum (vertical line 1) well before the minimum of the biceps activity (vertical line 2). Thereafter, the discharge rate of the neuron changes in parallel with the velocity of the extension, its highest value coinciding with the highest value of that parameter (vertical line 3). The changes in discharge rate of these interpositus neurons before and during extensions were thus opposite m sign to the changes observed before and during flexions. Electrical activity in the triceps muscle was rarely observed during extensions, most probably because these movements could occur passively due to the downward torque provided by the forearm itself. The behavior illustrated in Fig. 3 is that of the remaining 14 interpositus neurons. The average discharge rate of this cell (32 trials) begins to decrease prior to the increase in biceps activity (vertical line 1) and reaches its minimum value in advance of the maximum biceps activity (vertical line 2). Soon after the onset of the flexion displacement, however, the average discharge rate suddenly increases and reaches its highest value slightly in advance of the peak velocity (vertical line 3). At this time, the biceps activity is at a minimum. Thereafter, the discharge of the neuron fluctuates in
17l parallel with the velocity parameter. This behavior is approximately the reciprocal of that illustrated in Fig. 2A. The discharge rate of these 14 units did not change significantly in relation to extension displacements. The data presented in this report are in good agreement with those from previous studies with monkey wrist movementsal, 1~. In both cat and monkey, the first change in discharge rate of an interpositus neuron can be either an increase or a decrease, and there can be several alterations in rate during a single movement. Two differences, however, are apparent. In the monkey, the direction of the first change in rate could be the same or different for movements of opposite direction (flexion vs. extension), whereas, in the cat the direction of the first change was never the same. This difference may be related to differences in the motor pattern. In the cat, flexion was initiated by increased biceps activity and extension by decreased biceps activity (there being no involvement of the triceps), whereas, in the monkey there was considerable co-activation of wrist flexors and extensors during both movements, with the result, for example, that both flexion and extension were associated with increased flexor activity (ref. 11, Fig. 1, 3a). The second difference is that the first change in discharge rate of all of the cat interpositus neurons began before, or coincided with, the first change in biceps activity, whereas in the monkey 58 ~ of the interpositus units changed rate only after the wrist muscles had become active 11. This difference may be related to differences in overall motor pattern. In the monkey, the secondary muscles (upper arm and trunk) did not change activity more than 10 msec before the primary muscles (wrist flexors and extensors) la, whereas in the cat many trunk and shoulder muscles became active well before the biceps or the change in interpositus activity. The earlier activity in the cat interpositus nucleus may well have been associated with this supportive muscle activity and could have been produced by either central activities or feedback from the periphery. To summarize the present data for both types of neuron, it can be stated that, during the motion, the maxima and minima of the unit discharge rate coincide with the peaks of the angular velocity. Moreover, the magnitude of the modulation of the discharge rate is roughly proportional to the magnitude of the velocity parameter. It is concluded, therefore, that there is a strong correlation between the discharge rate of interpositus neurons and the velocity of the motion. Furthermore, it is most likely that this correlation is due to input to the cerebellum generated by rate-sensitive receptors in the moving limb. Indeed, it has been shown that the output of muscle spindles influences neurons in the interpositus nucleus 3 and that the discharge rate of interpositus neurons is related to the velocity of passive elbow displacement (Burton and Onoda, unpublished observations) and to the rate of stretch of forelimb muscles 4. Finally, in the present study, the time relations between the changes in discharge rate of interpositus neurons and the biceps E M G activity are consistent with the idea that the nuclear cell acitivity is involved in regulating the motor output to the biceps throughout the performance of the task. These conclusions are in agreement with the suggestion j,2 that the intermediate zone of the cerebellar cortex and the interpositus nucleus integrates inputs from cerebrocerebellar and spinocerebellar systems to provide an output which continually updates the motor commands in the control of an evolving
172 m o v e m e n t . In this context, it has already been suggested that cerebetlar activities c o n t r i b u t e t o the regulation o f o n g o i n g m o v e m e n t s , especially by utilizing i n p u t data o n the velocity o f the m o t i o n 9,1°. M o r e o v e r , i t has been f o u n d that in the course o f fast m o v e m e n t s , the m o t o r o u t p u t depends c o n t i n u o u s l y on sensory input d a t a an d that this relationship requires the presence o f cerebellar activities 5-8,1°. O u r data are n o t only c o m p a t i b l e with these findings bu t d e m o n s t r a t e t h a t the velocity p a r a m e t e r is represented in the activity o f interpositus neurons. We wish to t h a n k Dr. C. A. T e r z u o l o an d Dr. J. E. Vaughn for their valuable criticism o f the m a n u s c r i p t a n d Mr. R. Barber for the d r a w i n g o f Fig. 1. S u p p o r t e d by N I H R e s e a r c h G r a n t N o . N S 11798 f r o m N I N D S .
1 Allen, G. 1. and Tsukahara, N.. Cerebrocerebetlar communication systems, Physiol. Rev.. 54 (1974) 957-1006. 2 Eccles. J. C.. Circuits in the cerebellar control of movement. Proc. nat. Acad. SoL Wash. ,. 58 (1967J 336-343. 3 Kawaguchi, S. and Ohno, T., Responses of interpositus neurons to inputs from muscle receptors. Exp. Brain Res., 21 (1974) 375-386. 4 MacKay, W. A. and Murphy, J. T., Responses of interpositus neurons to passive muscle stretch, J. Neurophysiol., 27 (1974) 1410-1423. 5 Soechting, J. F., Modeling of a simple motor task m man: motor output dependence on sensory input, Kybernetik, 14 (1973) 25-34. 6 Soechting, J. F., Palminteri, R. and Terzuolo, C. A., Studies on the control of somesimple motor tasks. IV. Relation between parameters of motion and motor output in squirrel monkey, Brain Research, 62 (1973) 247-252, 7 Soechting, J. F., Ranish, N. A., Palminteri, R. and Terzuolo, C. A., Changes m a motor pattern following cerebellar and olivary lesions in the squirrel monkey, Brain Research, 105 (1976) 2144. 8 Terzuolo, C A., Soechting, J. F. and Ranish, N. A., Studies on the control of some motor tasks. V. Changes in motor output following dorsal root section in squirrel monkey, Brain Research. 70 (1974) 521-526. 9 Terzuolo, C. A., Soechting, J. F and Viviani, P., Studies on the control of some simple motor tasks. I. Relations between parameters of movements and EMG activities, Brain Research, 58 (t973) 212-216. 10 Terzuolo, C. A. and Viviani. P., Parameters of motion and EMG activities during some simple motor tasks m normal subjects and cerebellar patients, tn I. S. Cooper, M. Riklan and R. S. Snider 0Eds.). The Cerebellum, Epilepsy, and Behavior, Plenum Press. New York. 1974, pp. 173-215. 11 Thach, W, T., Discharge of cerebellar neurons related to two maintained postures and two prompt movements. I. Nuclear cell output, J. Neurophysiot., 33 (1970) 527-536. 12 Thach, W. T., Coding differences in activity of muscles, motor cortex, and cerebetlar nuclei during a more complex motor task, Neurosci. Abstr.. 1 (1975) 175.