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Corollary Discharges: Motor Commands and Perception

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Abstract

The sections in this article are:

1 Historical Development
2 Terminology
3 Corollaries of Motor Commands to Limb and Trunk Muscles
3.1 Sensations of Movement
3.2 Interactions Between Corollary Discharges and Kinesthetic Afferent Inputs
3.3 Corollary Discharges and Somatosensory Afferents
3.4 Sensations of Muscular Force or Heaviness
4 Corollary Discharges and Eye Movements
4.1 Corollary Discharges and Kinesthetic Sensibility in the Eye
4.2 Corollary Discharges and Visual Perception
5 Electrophysiological Correlates of Motor Commands
6 Other Instances of Central Irradiation by Motor Commands
7 Conclusions
8 Summary
Figure 1. Figure 1.

Figure depicts circumstances important in historical development of ideas regarding corollary discharges and visual stability. Diagrams show actual positions of eye, viewed target, and retinal image. What appears to the subject to be happening is stated under each diagram.

Figure 2. Figure 2.

Efference copy‐reafference mechanism, as applied to eye.

Adapted from von Holst 85
Figure 3. Figure 3.

Index finger of left hand (circled) had been ring blocked by injection of lignocaine at base. Blindfolded subject was asked to extend all digits of affected hand starting from position of flexion. Immediately afterward, subject was to put fingers of other hand into position of affected hand. Position was then voluntarily frozen and photographed. Subject felt insentient finger failed to extend at all joints, though it actually did so.

From Goodwin, McCloskey, and Matthews 62
Figure 4. Figure 4.

Records demonstrate that upon progressive paralysis of a limb, perception of movement may be more severely impaired than actual ability to move, making it unlikely that perception of movement depends primarily on sensations of innervation. Top trace shows movements at metacarpophalangeal joint of index finger of one hand with circulation to arm occluded; interphalangeal joints were fixed in full extension by strapping. Periodically subject was asked to raise finger to full extension and then to lower it again; in between, finger lay partly flexed under action of gravity. Immediately afterward, subject was asked to make equivalent movement with index finger of other hand, thus providing an objective measure of the subject's perception of extent of movement being paralyzed. Left: circulation to whole of forearm and hand was occluded by pressure cuff above elbow, which eventually led to complete paralysis of all muscles involved and to complete loss of sensation. Even when paralyzed, subject still attempted movement at 0.5‐min intervals. Right: pressure cuff shifted to wrist so that hand remained anesthetized, but muscles of forearm recovered. Upper cuff was inflated for 13 min before beginning of records shown. There was 14‐min interval between left and right sets of records. Recordings were made by connecting fingers to freely moving potentiometers. Subject could not see hands or recordings.

From Goodwin, McCloskey, and Matthews 62
Figure 5. Figure 5.

Angular velocity of illusory movement of elbow extension induced by vibration of biceps brachii at 100 Hz, plotted against load at wrist borne by tensing vibrated biceps. Closed circles are points obtained when biceps carried its loads only briefly and so was not fatigued. Open circles are points obtained when biceps was fatigued through period of prolonged and continuous weight bearing.

From McCloskey 135
Figure 6. Figure 6.

Subject was given a 9‐Ib weight (4.09 kg) to support by contraction of biceps brachialis of one arm and, in a series of trials, was to choose apparently equal weights supported in same way by other arm. When reference arm was rested between trials (closed circles), subject chose weights close to reference weight in attempts to match it. When reference arm supported its weight continuously (open circles), it became fatigued, and weights heavier than reference weight were chosen to match it.

From McCloskey et al. 137
Figure 7. Figure 7.

Summary of factors affecting perceived muscular force or heaviness.

Figure 8. Figure 8.

False move corrected without visual feedback. At time indicated at top, visible target jumped to left. Subject responded by moving hand to left, causing marker to move in wrong direction. While marker was still behind screen and therefore invisible (shaded area), subject reversed direction of movement. Marker then became visible at left (correct) side of screen. Response was classified as false move, reversed while marker was invisible. Reversal was commenced in shorter time than kinesthetic reaction time.

From Angel 2
Figure 9. Figure 9.

Representative scheme showing typical variability of equally directed precise (solid line) or imprecise (dashed line) conditioned eye fixation movements in successive trials. Abscissa, time; ordinates, eye displacement during trials. In response to auditory signal, subjects turned their eyes toward a fixation point, the location of which was learned when it was visible some time before.

From Gurevitch 72
Figure 10. Figure 10.

Neural reconstruction of target position relative to body. Neural reconstruction of target velocity must be based on velocity signals related to same angles.

From Miles and Evarts 147. Reproduced with permission from Annu. Rev. Psychol. 30: 327–362, 1979
Figure 11. Figure 11.

Mean shifts in perceived direction of fixation target for various loads applied to left and right of subject's (AS) right eye. Subject's mean straight‐ahead position (based on trials when no load was applied) is shown as intersection of axes. Mean shifts in perceived direction are plotted as circles when fixation target was present straight ahead and as crosses when target was presented 13.5 deg arc to right. Rectangle on right shows objective position of displaced fixation target. Oblique lines indicate perceived shift in target direction predicted from outflow theory. Each data point is mean of 10 position measures; error bars indicate ± 1 SD.

From Skavenski et al. 179
Figure 12. Figure 12.

Pointing overshoot errors associated with complete oculomotor paralysis caused by retrobulbar injection of curare and local anesthetic. Subject was seated and head fixed with bite bar. Experimenter placed finger on table in front of subject. Subject then attempted ballistically to touch experimenter's finger. Right eye was paralyzed and left eye occluded. Each black circle represents a target point and length of arrow leading from it represents approximate error range for normal subject. Bar at top corresponds to 1 ft, and open arrow at bottom is subject. Same results were obtained under wide variety of conditions (e.g., no bite bar or no visual feedback) in this subject 190. Other subjects did not demonstrate these effects 18.

From Stevens 190
Figure 13. Figure 13.

Summary of current knowledge on several aspects of visual stability that are relevant to consideration of corollary discharges. Diagrams show actual positions of eye, viewed target and retinal image. Figure should be contrasted with Figure 1, which depicts historically important observations.

Figure 14. Figure 14.

Activity of neurons of ventral spinocerebellar tract during “fictive scratching,” that is, with animal paralyzed. AC, decerebrate cat. Each line of recording is direct continuation of preceding one. Arrows denote start and end of stimulation of 1st cervical segment of spinal cord. D, decapitated cat. Upper part of each oscillogram gives extracellular recording of neuron of ventral spinocerebellar tract; lower part gives activity in nerve activating gastrocnemius muscle.

From Arshavskii et al. 5
Figure 15. Figure 15.

Paralyzed anesthetized dog. During period of recording, respiratory pump was temporarily stopped so that animal was completely motionless. Record of phrenic‐nerve discharge (leaky integrator) shows timing of central inspiratory activity. Note that heart rate is in phase with central inspiratory cycle. Left panel shows 2 brief, selective stimuli delivered to arterial chemoreceptors at markers; right panel shows 2 brief, selective stimuli (pressure pulses) delivered to arterial baroreceptors at markers. In each panel, stimulus given during expiratory phase of central respiratory cycle (i.e., during phrenic inactivity) is shown to evoke reflex slowing of heart; stimuli given during inspiratory phase of central respiratory cycle fail to slow heart.

From Gandevia, McCloskey, and Potter 53


Figure 1.

Figure depicts circumstances important in historical development of ideas regarding corollary discharges and visual stability. Diagrams show actual positions of eye, viewed target, and retinal image. What appears to the subject to be happening is stated under each diagram.



Figure 2.

Efference copy‐reafference mechanism, as applied to eye.

Adapted from von Holst 85


Figure 3.

Index finger of left hand (circled) had been ring blocked by injection of lignocaine at base. Blindfolded subject was asked to extend all digits of affected hand starting from position of flexion. Immediately afterward, subject was to put fingers of other hand into position of affected hand. Position was then voluntarily frozen and photographed. Subject felt insentient finger failed to extend at all joints, though it actually did so.

From Goodwin, McCloskey, and Matthews 62


Figure 4.

Records demonstrate that upon progressive paralysis of a limb, perception of movement may be more severely impaired than actual ability to move, making it unlikely that perception of movement depends primarily on sensations of innervation. Top trace shows movements at metacarpophalangeal joint of index finger of one hand with circulation to arm occluded; interphalangeal joints were fixed in full extension by strapping. Periodically subject was asked to raise finger to full extension and then to lower it again; in between, finger lay partly flexed under action of gravity. Immediately afterward, subject was asked to make equivalent movement with index finger of other hand, thus providing an objective measure of the subject's perception of extent of movement being paralyzed. Left: circulation to whole of forearm and hand was occluded by pressure cuff above elbow, which eventually led to complete paralysis of all muscles involved and to complete loss of sensation. Even when paralyzed, subject still attempted movement at 0.5‐min intervals. Right: pressure cuff shifted to wrist so that hand remained anesthetized, but muscles of forearm recovered. Upper cuff was inflated for 13 min before beginning of records shown. There was 14‐min interval between left and right sets of records. Recordings were made by connecting fingers to freely moving potentiometers. Subject could not see hands or recordings.

From Goodwin, McCloskey, and Matthews 62


Figure 5.

Angular velocity of illusory movement of elbow extension induced by vibration of biceps brachii at 100 Hz, plotted against load at wrist borne by tensing vibrated biceps. Closed circles are points obtained when biceps carried its loads only briefly and so was not fatigued. Open circles are points obtained when biceps was fatigued through period of prolonged and continuous weight bearing.

From McCloskey 135


Figure 6.

Subject was given a 9‐Ib weight (4.09 kg) to support by contraction of biceps brachialis of one arm and, in a series of trials, was to choose apparently equal weights supported in same way by other arm. When reference arm was rested between trials (closed circles), subject chose weights close to reference weight in attempts to match it. When reference arm supported its weight continuously (open circles), it became fatigued, and weights heavier than reference weight were chosen to match it.

From McCloskey et al. 137


Figure 7.

Summary of factors affecting perceived muscular force or heaviness.



Figure 8.

False move corrected without visual feedback. At time indicated at top, visible target jumped to left. Subject responded by moving hand to left, causing marker to move in wrong direction. While marker was still behind screen and therefore invisible (shaded area), subject reversed direction of movement. Marker then became visible at left (correct) side of screen. Response was classified as false move, reversed while marker was invisible. Reversal was commenced in shorter time than kinesthetic reaction time.

From Angel 2


Figure 9.

Representative scheme showing typical variability of equally directed precise (solid line) or imprecise (dashed line) conditioned eye fixation movements in successive trials. Abscissa, time; ordinates, eye displacement during trials. In response to auditory signal, subjects turned their eyes toward a fixation point, the location of which was learned when it was visible some time before.

From Gurevitch 72


Figure 10.

Neural reconstruction of target position relative to body. Neural reconstruction of target velocity must be based on velocity signals related to same angles.

From Miles and Evarts 147. Reproduced with permission from Annu. Rev. Psychol. 30: 327–362, 1979


Figure 11.

Mean shifts in perceived direction of fixation target for various loads applied to left and right of subject's (AS) right eye. Subject's mean straight‐ahead position (based on trials when no load was applied) is shown as intersection of axes. Mean shifts in perceived direction are plotted as circles when fixation target was present straight ahead and as crosses when target was presented 13.5 deg arc to right. Rectangle on right shows objective position of displaced fixation target. Oblique lines indicate perceived shift in target direction predicted from outflow theory. Each data point is mean of 10 position measures; error bars indicate ± 1 SD.

From Skavenski et al. 179


Figure 12.

Pointing overshoot errors associated with complete oculomotor paralysis caused by retrobulbar injection of curare and local anesthetic. Subject was seated and head fixed with bite bar. Experimenter placed finger on table in front of subject. Subject then attempted ballistically to touch experimenter's finger. Right eye was paralyzed and left eye occluded. Each black circle represents a target point and length of arrow leading from it represents approximate error range for normal subject. Bar at top corresponds to 1 ft, and open arrow at bottom is subject. Same results were obtained under wide variety of conditions (e.g., no bite bar or no visual feedback) in this subject 190. Other subjects did not demonstrate these effects 18.

From Stevens 190


Figure 13.

Summary of current knowledge on several aspects of visual stability that are relevant to consideration of corollary discharges. Diagrams show actual positions of eye, viewed target and retinal image. Figure should be contrasted with Figure 1, which depicts historically important observations.



Figure 14.

Activity of neurons of ventral spinocerebellar tract during “fictive scratching,” that is, with animal paralyzed. AC, decerebrate cat. Each line of recording is direct continuation of preceding one. Arrows denote start and end of stimulation of 1st cervical segment of spinal cord. D, decapitated cat. Upper part of each oscillogram gives extracellular recording of neuron of ventral spinocerebellar tract; lower part gives activity in nerve activating gastrocnemius muscle.

From Arshavskii et al. 5


Figure 15.

Paralyzed anesthetized dog. During period of recording, respiratory pump was temporarily stopped so that animal was completely motionless. Record of phrenic‐nerve discharge (leaky integrator) shows timing of central inspiratory activity. Note that heart rate is in phase with central inspiratory cycle. Left panel shows 2 brief, selective stimuli delivered to arterial chemoreceptors at markers; right panel shows 2 brief, selective stimuli (pressure pulses) delivered to arterial baroreceptors at markers. In each panel, stimulus given during expiratory phase of central respiratory cycle (i.e., during phrenic inactivity) is shown to evoke reflex slowing of heart; stimuli given during inspiratory phase of central respiratory cycle fail to slow heart.

From Gandevia, McCloskey, and Potter 53
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D. I. McCloskey. Corollary Discharges: Motor Commands and Perception. Compr Physiol 2011, Supplement 2: Handbook of Physiology, The Nervous System, Motor Control: 1415-1447. First published in print 1981. doi: 10.1002/cphy.cp010232