Cerebellar Purkinje Cell Simple Spike Discharge Encodes Movement Velocity in Primates during Visuomotor Arm Tracking

Pathophysiological, lesion, and electrophysiological studies suggest that the cerebellar cortex is important for controlling the direction and speed of movement. The relationship of cerebellar Purkinje cell discharge to the control of arm movement parameters, however, remains unclear. The goal of this study was to examine how movement direction and speed and their interaction—velocity—modulate Purkinje cell simple spike discharge in an arm movement task in which direction and speed were independently controlled. The simple spike discharge of 154 Purkinje cells was recorded in two monkeys during the performance of two visuomotor tasks that required the animals to track targets that moved in one of eight directions and at one of four speeds. Single-parameter regression analyses revealed that a large proportion of cells had discharge modulation related to movement direction and speed. Most cells with significant directional tuning, however, were modulated at one speed, and most cells with speed-related discharge were modulated along one direction; this suggested that the patterns of simple spike discharge were not adequately described by single-parameter models. Therefore, a regression surface was fitted to the data, which showed that the discharge could be tuned to specific direction–speed combinations (preferred velocities). The overall variability in simple spike discharge was well described by the surface model, and the velocities corresponding to maximal and minimal discharge rates were distributed uniformly throughout the workspace. Simple spike discharge therefore appears to integrate information about both the direction and speed of arm movements, thereby encoding movement velocity.

[1]  G. Holmes THE CEREBELLUM OF MAN , 1939 .

[2]  K. Mardia Statistics of Directional Data , 1972 .

[3]  F A Miles,et al.  Visual tracking and the primate flocculus. , 1975, Science.

[4]  A. Fuchs,et al.  Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. , 1978, Journal of neurophysiology.

[5]  D. A. Suzuki,et al.  Target velocity signals of visual tracking in vermal Purkinje cells of the monkey. , 1979, Science.

[6]  A. Pellionisz,et al.  Brain modeling by tensor network theory and computer simulation. The cerebellum: Distributed processor for predictive coordination , 1979, Neuroscience.

[7]  N. Mano,et al.  Simple-spike activity of cerebellar Purkinje cells related to visually guided wrist tracking movement in the monkey. , 1980, Journal of neurophysiology.

[8]  E. Batschelet Circular statistics in biology , 1981 .

[9]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  J. Kalaska,et al.  Cerebellar cortical activity during antagonist cocontraction and reciprocal inhibition of forearm muscles. , 1984, Journal of neurophysiology.

[11]  H. Beppu,et al.  Analysis of cerebellar motor disorders by visually guided elbow tracking movement. , 1984, Brain : a journal of neurology.

[12]  J. Kalaska,et al.  Cerebellar nuclear cell activity during antagonist cocontraction and reciprocal inhibition of forearm muscles. , 1985, Journal of neurophysiology.

[13]  J. F. Stein,et al.  Role of the cerebellum in the visual guidance of movement , 1986, Nature.

[14]  George E. P. Box,et al.  Empirical Model‐Building and Response Surfaces , 1988 .

[15]  M. Deaton,et al.  Response Surfaces: Designs and Analyses , 1989 .

[16]  J F Stein,et al.  Cerebellar neuronal activity related to arm movements in trained rhesus monkeys. , 1987, The Journal of physiology.

[17]  D. A. Suzuki,et al.  The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity. , 1988, Journal of neurophysiology.

[18]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. I. Relations between single cell discharge and direction of movement , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Derek J. Pike,et al.  Empirical Model‐building and Response Surfaces. , 1988 .

[20]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  J. Kalaska,et al.  Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. , 1989, Journal of neurophysiology.

[22]  J. Stein,et al.  Neuronal activity in the lateral cerebellum of trained monkeys, related to visual stimuli or to eye movements. , 1990, The Journal of physiology.

[23]  S. Lisberger,et al.  Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. , 1990, Journal of neurophysiology.

[24]  M. Flanders Temporal patterns of muscle activation for arm movements in three- dimensional space , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  R. G. Lee,et al.  Multi-Joint Reaching Movements and Eye-Hand Tracking in Cerebellar Incoordination: Investigation of a Patient with Complete Loss of Purkinje Cells , 1991, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[26]  J. Hore,et al.  Cerebellar dysmetria at the elbow, wrist, and fingers. , 1991, Journal of neurophysiology.

[27]  R. Ivry,et al.  Impaired Velocity Perception in Patients with Lesions of the Cerebellum , 1991, Journal of Cognitive Neuroscience.

[28]  A. Schwartz Motor cortical activity during drawing movements: single-unit activity during sinusoid tracing. , 1992, Journal of neurophysiology.

[29]  T. Ebner,et al.  Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey. , 1992, Journal of neurophysiology.

[30]  H. Diener,et al.  Pathophysiology of cerebellar ataxia , 1992, Movement disorders : official journal of the Movement Disorder Society.

[31]  J. Houk,et al.  Movement-related inputs to intermediate cerebellum of the monkey. , 1993, Journal of neurophysiology.

[32]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during sinusoid tracing. , 1993, Journal of neurophysiology.

[33]  J. Houk,et al.  Output organization of intermediate cerebellum of the monkey. , 1993, Journal of neurophysiology.

[34]  M. Kawato,et al.  Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum , 1993, Nature.

[35]  Nicholas I. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[36]  S. Bisti,et al.  Light sensitivity, adaptation and saturation in mammalian rods. , 1993, Progress in brain research.

[37]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

[38]  J. Kalaska,et al.  Comparison of cerebellar and motor cortex activity during reaching: directional tuning and response variability. , 1993, Journal of neurophysiology.

[39]  P. van Donkelaar,et al.  Interactions between the eye and hand motor systems: disruptions due to cerebellar dysfunction. , 1994, Journal of neurophysiology.

[40]  M. Hallett,et al.  Disturbances of kinaesthesia in patients with cerebellar disorders. , 1994, Brain : a journal of neurology.

[41]  J. Kalaska,et al.  Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. , 1994, Journal of neurophysiology.

[42]  S G Lisberger,et al.  Simple spike responses of gaze velocity Purkinje cells in the floccular lobe of the monkey during the onset and offset of pursuit eye movements. , 1994, Journal of neurophysiology.

[43]  K. Ohtsuka,et al.  Discharge properties of Purkinje cells in the oculomotor vermis during visually guided saccades in the macaque monkey. , 1995, Journal of neurophysiology.

[44]  M. E. Anderson,et al.  Directional variation of spatial and temporal characteristics of limb movements made by monkeys in a two-dimensional work space. , 1995, Journal of neurophysiology.

[45]  J. Houk,et al.  Motor co‐ordinates in primate red nucleus: preferential relation to muscle activation versus kinematic variables. , 1995, The Journal of physiology.

[46]  W. T. Thach,et al.  Cerebellar ataxia: abnormal control of interaction torques across multiple joints. , 1996, Journal of neurophysiology.

[47]  H. Shibutani,et al.  Chapter 31 Context dependent discharge characteristics of saccade-related Purkinje cells in the cerebellar hemispheres of the monkey , 1996 .

[48]  T. Ebner,et al.  What features of visually guided arm movements are encoded in the simple spike discharge of cerebellar Purkinje cells? , 1997, Progress in brain research.

[49]  T J Ebner,et al.  Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey. , 1997, Journal of neurophysiology.

[50]  G E Alexander,et al.  Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. , 1997, Journal of neurophysiology.

[51]  A G Barto,et al.  Prediction of complex two-dimensional trajectories by a cerebellar model of smooth pursuit eye movement. , 1997, Journal of neurophysiology.

[52]  Scott T. Grafton,et al.  Motor subcircuits mediating the control of movement velocity: a PET study. , 1998, Journal of neurophysiology.

[53]  M. Kawato,et al.  Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys I. Simple spikes. , 1998, Journal of neurophysiology.

[54]  M. Kawato,et al.  Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys II. Complex spikes. , 1998, Journal of neurophysiology.

[55]  T J Ebner,et al.  Visuomotor processing as reflected in the directional discharge of premotor and primary motor cortex neurons. , 1999, Journal of neurophysiology.

[56]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during lemniscate tracing. , 1999 .