588
Brain Research, 105 (1976) 588-590 (() Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Role of proprioceptive data in performance of a complex visuomotor tracking task
E. EIDELBERG AND F. DAVIS
Division of Neurobiology, Barrow Neurological Institute of St. Joseph's" Hospital and Medical Center, Phoenix, Ariz. 85013 (U.S.A.) (Accepted January 5th, 1975)
The early concept that sensory deafferentation of a limb, by cutting the corresponding dorsal roots, results in crippling deficits in motor function has been disproved by the work of many investigators, and most recently Taub et al. 1,2,8-1°. While it is possible that sensory afferents in the ventral roots 3 may be involved in the recovery of motor function after dorsal rhizotomy, the best evidence at this time supports the contention that purely internal mechanisms in the CNS - - such as preprogramming and/or corollary discharge 5 - - can maintain motor behaviors such as feeding, climbing, etc.2,8, 9. Since we were interested in the possible role of certain sensory pathways in the control of movement we asked a different question: is it possible to interfere, at least partially, with the central mechanisms mentioned above so as to make the animals dependent upon proprioceptive inputs for the performance of complex movements? We reasoned that this could be achieved by using a visuomotor tracking task in which the instantaneous position of the moving visual target could not be readily predicted by the subject, when the subject was denied visual information about the position of the manipulandum. If this reasoning were correct the animals trained in this task should fail to perform accurately after proprioceptive deafferentation, as indeed this experiment showed. The experimental subjects were two juvenile (4.0 and 4.5 kg) stumptailed monkeys (Macaca speciosa), trained to sit in a restraining chair and perform a visuomotor tracking task for food (fruit-flavored pellets reward). The stimulus (target) was one beam of a cathode ray oscilloscope facing the animal at eye level (30 cm × 23 cm screen). It moved only in the horizontal direction under the control of a pseudorandom voltage generator that produced a mixture of 3 non-harmonically related sine waveforms4, 7. By means of Z-axis modulation controls the beam brightness increased one step when the lever was held by the subject's right hand, and it increased a second step when the animal tracked within preset limits of error. The manipulandum was a lever with low inertial mass placed at elbow level, that could be moved only in the horizontal plane. The animal was prevented from seeing his body or the lever by an opaque neck plate. The task consisted of grasping the lever and moving it so as to keep it vertically aligned with the target, with an error not
589 exceeding 100 msec of lead or lag, for a period of 6 sec (Fig. 1). If this was accomplished a reward was delivered and the monkey could start a new 'trial' by grasping the lever and starting to track again. Each session lasted approximately 1 h, at the end of which the subject was returned to his cage and given his daily ration of solid food. At least 300 such trials/day for 5 consecutive days were required as preoperative criterion performance. During the training and postoperative testing periods an indirect visual indication of lever position was introduced when needed by turning on a second CRT beam whose position paralleled that of the lever. Both animals performed equally well preoperatively with or without this signal. The animals were trained to use only their right hand and were tested postoperatively for right hand performance. Dorsal rhizotomy from C3 to Ca was carried out, bilaterally and intradurally, using an operating microscope. The reasons for preferring a bilateral operation have been discussed in detail previously by others s. The initial deficits following rhizotomy were the same as described previously by others1, 2,s and consisted of lack of use of the (flailing) forelimbs. As reported, this effect gradually disappeared until the animals became quite agile and capable of feeding themselves and climbing, although their movements were never again as precisely and smoothly executed as before the surgery2,8-1°. We sacrificed one animal at 3 months and the other at 4 months after surgery, primarily because of self-mutilation of the deafferented digits. We then confirmed by careful dissection the completeness of the rhizotomies. Neither animal was again capable of performing in the test situation. With the right hand taped lightly to the lever (which they could not find by themselves) their attempts at tracking consisted of a few wild motions from side to side. Introduction of the visual signal of lever position (second CRO beam, see above) improved the subject's performance somewhat, in that some semblance of tracking was restored, but never even near preoperative levels and only for brief periods of time. These findings confirm previous reports that brachial rhizotomy is followed by the return of a substantial amount of useful motor function, even if the animals were clumsier and their movements less smoothly coordinated than in the preoperative state. Taub et alp used a pointing task in which the deafferented monkey had
CONTROL
POST RHIZOTOMY
TARGET LEVER ~
-
w/o
J 10 m.
Fig. 1. Recordings from one monkey, before (control) and after rhizotomy, w/o, means without visual feedback (second beam, see text) and W, with feedback.
590 to aim his forelimb to one o f 3 fixed targets a n d hold it there for a p e r i o d o f time. Their animals p e r f o r m e d this task, albeit tess well t h a n preoperatively, b u t it is imp o r t a n t to note t h a t their subjects were required to c a r r y o u t ballistic m o v e m e n t s a n d static holds, which are believed to be p r e p r o g r a m m e d by cerebellar c o n t r o l mechanisms w i t h o u t significant p r o p r i o c e p t i v e f e e d b a c k 6. The essential difference between this e x p e r i m e n t by T a u b et al. a n d ours is n o t so much t h a t o u r task was m u c h m o r e c o m p l i c a t e d a n d difficult, which we believe it was, b u t t h a t it forced the a n i m a l to d e p e n d u p o n p r o p r i o c e p t i v e data. This is because in an u n p r e d i c t a b l e t r a c k i n g t a s k the usefulness o f p r e p r o g r a m m i n g o r ' m e m o r y ' devices should be cons i d e r a b l y less in a i m i n g the l i m b t h a n it can be in ' s p o n t a n e o u s ' m o v e m e n t s (such as feeding a n d climbing) o r when the final p o s i t i o n o f the target is ' k n o w n ' a n d only a s t a r t signal is needed. Also, T a u b et al. d i d their e x p e r i m e n t to test whether or not central mechanisms were c a p a b l e o f controlling m o v e m e n t in the absence o f p r o prioceptive feedback, a n d showed t h a t they p r o b a b l y are. The fact t h a t o u r m o n k e y s were quite c a p a b l e o f p e r f o r m i n g the t r a c k i n g task p r e o p e r a t i v e l y in the absence o f visual feedback, a n d that they failed to do so after deafferentation, clearly indicates t h a t they d e p e n d e d u p o n p r o p r i o c e p t i v e d a t a before surgery. T h e same m e t h o d o l o g y has been used in a series o f experiments, to be rep o r t e d separately, where we a n a l y z e d the relative role o f certain central p a t h w a y s in conveying the p r o p r i o c e p t i v e d a t a for m o t o r control. T h e assistance o f Ms. C. J. Kreinick, Ms. B. W o o l f a n d Ms. C. J. W a t k i n s is gratefully acknowledged. S u p p o r t e d by G R S G r a n t No. R R 05575 from the U.S.P.H.S.
1 BOSSOM,J., Time of recovery of voluntary movement following dorsal rhizotomy, Brain Research, 45 (1972) 247-250. 2 BOSSOM,J., Movement without proprioception, Brain Research, 71 (1974) 285-296. 3 COGOBSHALL,R. E., COULTER,J. D., AND WILLIS,W. D., JR., Unmyelinated axons in the ventral roots of the cat lumbosacral enlargement, J. comp. NeuroL, 153 (1974) 39-58. 4 EIDELBERG,E., AND DUNMIRE, I. D., Linear systems analysis of motor control in Parkinsonism. In Proc. Regulation and Control in Physiol. Systems Conf. August, 1973, Rochester, N.Y. pp. 239-240. 5 EVARTS, E. V., Feedback and corollary discharge: a merging of the concepts, Neurosci. Res. Progr. Bull., 9 (1971) 86-112. 6 KORNHUBER, H. H., Cerebral cortex, cerebellum, and basal ganglia: an introduction to their motor functions. In F. O. SCHMITTAND F. G. WORDEN(Eds.), Neuroscience Third Study Program, MIT Press, Cambridge, Mass., 1974, pp. 267-280. 7 STARK.,L., Neurological'Control Systems, Plenum Press, New York, 1968, pp. 325-331. 8 TAUa, E., AND BERMAN, A. J., Movement and learning in the absence of sensory feedback. In S. J. FREEDMAN(Ed.), The Neuropsychology of Spatially Oriented Behavior, Dorsey Press, Homewood, Ill., 1968, pp. 173-192. 9 TAUB, E., GOLDBERG, 1. A., AND TAUB, P., Deafferentation in monkeys: pointing at a target without visual feedback, Exp. Neurol., 46 (1975) 178-186. 10 TERZUOLO,C. A., SOECHT~NO,J. F., AND RANISH,N. A., Studies on the control of some simple motor tasks. V. Changes in motor output following dorsal root section in squirrel monkey, Brain Research, 70 (1974) 521-526.
Brain Research, 105 (1976) 588-590 (() Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Role of proprioceptive data in performance of a complex visuomotor tracking task
E. EIDELBERG AND F. DAVIS
Division of Neurobiology, Barrow Neurological Institute of St. Joseph's" Hospital and Medical Center, Phoenix, Ariz. 85013 (U.S.A.) (Accepted January 5th, 1975)
The early concept that sensory deafferentation of a limb, by cutting the corresponding dorsal roots, results in crippling deficits in motor function has been disproved by the work of many investigators, and most recently Taub et al. 1,2,8-1°. While it is possible that sensory afferents in the ventral roots 3 may be involved in the recovery of motor function after dorsal rhizotomy, the best evidence at this time supports the contention that purely internal mechanisms in the CNS - - such as preprogramming and/or corollary discharge 5 - - can maintain motor behaviors such as feeding, climbing, etc.2,8, 9. Since we were interested in the possible role of certain sensory pathways in the control of movement we asked a different question: is it possible to interfere, at least partially, with the central mechanisms mentioned above so as to make the animals dependent upon proprioceptive inputs for the performance of complex movements? We reasoned that this could be achieved by using a visuomotor tracking task in which the instantaneous position of the moving visual target could not be readily predicted by the subject, when the subject was denied visual information about the position of the manipulandum. If this reasoning were correct the animals trained in this task should fail to perform accurately after proprioceptive deafferentation, as indeed this experiment showed. The experimental subjects were two juvenile (4.0 and 4.5 kg) stumptailed monkeys (Macaca speciosa), trained to sit in a restraining chair and perform a visuomotor tracking task for food (fruit-flavored pellets reward). The stimulus (target) was one beam of a cathode ray oscilloscope facing the animal at eye level (30 cm × 23 cm screen). It moved only in the horizontal direction under the control of a pseudorandom voltage generator that produced a mixture of 3 non-harmonically related sine waveforms4, 7. By means of Z-axis modulation controls the beam brightness increased one step when the lever was held by the subject's right hand, and it increased a second step when the animal tracked within preset limits of error. The manipulandum was a lever with low inertial mass placed at elbow level, that could be moved only in the horizontal plane. The animal was prevented from seeing his body or the lever by an opaque neck plate. The task consisted of grasping the lever and moving it so as to keep it vertically aligned with the target, with an error not
589 exceeding 100 msec of lead or lag, for a period of 6 sec (Fig. 1). If this was accomplished a reward was delivered and the monkey could start a new 'trial' by grasping the lever and starting to track again. Each session lasted approximately 1 h, at the end of which the subject was returned to his cage and given his daily ration of solid food. At least 300 such trials/day for 5 consecutive days were required as preoperative criterion performance. During the training and postoperative testing periods an indirect visual indication of lever position was introduced when needed by turning on a second CRT beam whose position paralleled that of the lever. Both animals performed equally well preoperatively with or without this signal. The animals were trained to use only their right hand and were tested postoperatively for right hand performance. Dorsal rhizotomy from C3 to Ca was carried out, bilaterally and intradurally, using an operating microscope. The reasons for preferring a bilateral operation have been discussed in detail previously by others s. The initial deficits following rhizotomy were the same as described previously by others1, 2,s and consisted of lack of use of the (flailing) forelimbs. As reported, this effect gradually disappeared until the animals became quite agile and capable of feeding themselves and climbing, although their movements were never again as precisely and smoothly executed as before the surgery2,8-1°. We sacrificed one animal at 3 months and the other at 4 months after surgery, primarily because of self-mutilation of the deafferented digits. We then confirmed by careful dissection the completeness of the rhizotomies. Neither animal was again capable of performing in the test situation. With the right hand taped lightly to the lever (which they could not find by themselves) their attempts at tracking consisted of a few wild motions from side to side. Introduction of the visual signal of lever position (second CRO beam, see above) improved the subject's performance somewhat, in that some semblance of tracking was restored, but never even near preoperative levels and only for brief periods of time. These findings confirm previous reports that brachial rhizotomy is followed by the return of a substantial amount of useful motor function, even if the animals were clumsier and their movements less smoothly coordinated than in the preoperative state. Taub et alp used a pointing task in which the deafferented monkey had
CONTROL
POST RHIZOTOMY
TARGET LEVER ~
-
w/o
J 10 m.
Fig. 1. Recordings from one monkey, before (control) and after rhizotomy, w/o, means without visual feedback (second beam, see text) and W, with feedback.
590 to aim his forelimb to one o f 3 fixed targets a n d hold it there for a p e r i o d o f time. Their animals p e r f o r m e d this task, albeit tess well t h a n preoperatively, b u t it is imp o r t a n t to note t h a t their subjects were required to c a r r y o u t ballistic m o v e m e n t s a n d static holds, which are believed to be p r e p r o g r a m m e d by cerebellar c o n t r o l mechanisms w i t h o u t significant p r o p r i o c e p t i v e f e e d b a c k 6. The essential difference between this e x p e r i m e n t by T a u b et al. a n d ours is n o t so much t h a t o u r task was m u c h m o r e c o m p l i c a t e d a n d difficult, which we believe it was, b u t t h a t it forced the a n i m a l to d e p e n d u p o n p r o p r i o c e p t i v e data. This is because in an u n p r e d i c t a b l e t r a c k i n g t a s k the usefulness o f p r e p r o g r a m m i n g o r ' m e m o r y ' devices should be cons i d e r a b l y less in a i m i n g the l i m b t h a n it can be in ' s p o n t a n e o u s ' m o v e m e n t s (such as feeding a n d climbing) o r when the final p o s i t i o n o f the target is ' k n o w n ' a n d only a s t a r t signal is needed. Also, T a u b et al. d i d their e x p e r i m e n t to test whether or not central mechanisms were c a p a b l e o f controlling m o v e m e n t in the absence o f p r o prioceptive feedback, a n d showed t h a t they p r o b a b l y are. The fact t h a t o u r m o n k e y s were quite c a p a b l e o f p e r f o r m i n g the t r a c k i n g task p r e o p e r a t i v e l y in the absence o f visual feedback, a n d that they failed to do so after deafferentation, clearly indicates t h a t they d e p e n d e d u p o n p r o p r i o c e p t i v e d a t a before surgery. T h e same m e t h o d o l o g y has been used in a series o f experiments, to be rep o r t e d separately, where we a n a l y z e d the relative role o f certain central p a t h w a y s in conveying the p r o p r i o c e p t i v e d a t a for m o t o r control. T h e assistance o f Ms. C. J. Kreinick, Ms. B. W o o l f a n d Ms. C. J. W a t k i n s is gratefully acknowledged. S u p p o r t e d by G R S G r a n t No. R R 05575 from the U.S.P.H.S.
1 BOSSOM,J., Time of recovery of voluntary movement following dorsal rhizotomy, Brain Research, 45 (1972) 247-250. 2 BOSSOM,J., Movement without proprioception, Brain Research, 71 (1974) 285-296. 3 COGOBSHALL,R. E., COULTER,J. D., AND WILLIS,W. D., JR., Unmyelinated axons in the ventral roots of the cat lumbosacral enlargement, J. comp. NeuroL, 153 (1974) 39-58. 4 EIDELBERG,E., AND DUNMIRE, I. D., Linear systems analysis of motor control in Parkinsonism. In Proc. Regulation and Control in Physiol. Systems Conf. August, 1973, Rochester, N.Y. pp. 239-240. 5 EVARTS, E. V., Feedback and corollary discharge: a merging of the concepts, Neurosci. Res. Progr. Bull., 9 (1971) 86-112. 6 KORNHUBER, H. H., Cerebral cortex, cerebellum, and basal ganglia: an introduction to their motor functions. In F. O. SCHMITTAND F. G. WORDEN(Eds.), Neuroscience Third Study Program, MIT Press, Cambridge, Mass., 1974, pp. 267-280. 7 STARK.,L., Neurological'Control Systems, Plenum Press, New York, 1968, pp. 325-331. 8 TAUa, E., AND BERMAN, A. J., Movement and learning in the absence of sensory feedback. In S. J. FREEDMAN(Ed.), The Neuropsychology of Spatially Oriented Behavior, Dorsey Press, Homewood, Ill., 1968, pp. 173-192. 9 TAUB, E., GOLDBERG, 1. A., AND TAUB, P., Deafferentation in monkeys: pointing at a target without visual feedback, Exp. Neurol., 46 (1975) 178-186. 10 TERZUOLO,C. A., SOECHT~NO,J. F., AND RANISH,N. A., Studies on the control of some simple motor tasks. V. Changes in motor output following dorsal root section in squirrel monkey, Brain Research, 70 (1974) 521-526.
