Somatosensory cortical activity in relation to arm posture: nonuniform spatial tuning.

1. Single unitary activity in primate somatosensory cortex (SI) was recorded while monkeys maintained a range of static arm postures. Unit discharge was related to parameters defining the posture of the arm by multiple linear regression techniques. 2. Two monkeys were trained to grasp a manipulandum presented at locations distributed throughout their workspace. The discharge of single units in SI was recorded for 3 s while the monkeys maintained contact with the manipulandum and the mean discharge rate over this hold time was related to the location of the hand and to the shoulder and elbow joint angles of the arm. 3. Unitary activity of 171 neurons in the proximal arm region of areas 3, 1, and 2 was recorded during the task. Of the total, 78 neurons had activity that varied with the location of the hand in space. Neuronal discharge typically varied monotonically with the target location, reaching a maximum at the borders of the work-space. The discharge rate in most of these neurons varied with both shoulder and elbow angles. 4. Discharge rate was related to the hand's location along three axes by means of a polynomial fit. In approximately half of the neurons, activity varied significantly only for displacements along a single axis in space. However, many neurons exhibited nonlinear relations between hand location along this preferred axis and discharge rate. Discharge rate did not vary for displacements of the hand in the plane perpendicular to this preferred axis (null plane). 5. In other neurons, discharge rate varied for hand displacements in a plane, i.e., along two perpendicular axes. Displacements of the hand along the axis perpendicular to this plane (null axis) did not affect the discharge rate. In only a small minority of neurons did discharge rate vary for hand displacements along all three axes in space. 6. The distribution of the sensitivity of the neural population to hand displacements along arbitrary directions in space was not uniform. On average, hand displacement along a vertical axis led to the smallest modulation of neural discharge, and displacement of the hand along the anteroposterior direction led to the largest modulation of activity.

[1]  Mountcastle Vb,et al.  Central nervous mechanisms subserving position sense and kinesthesis. , 1959 .

[2]  Mountcastle Vb,et al.  The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatta. , 1959 .

[3]  T P POWELL,et al.  The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatta. , 1959, Bulletin of the Johns Hopkins Hospital.

[4]  T P POWELL,et al.  Central nervous mechanisms subserving position sense and kinesthesis. , 1959, Bulletin of the Johns Hopkins Hospital.

[5]  Ray S. Snider,et al.  A stereotaxic atlas of the monkey brain : (Macaca mulatta) , 1961 .

[6]  V. Mountcastle,et al.  THE RELATION OF THALAMIC CELL RESPONSE TO PERIPHERAL STIMULI VARIED OVER AN INTENSIVE CONTINUUM. , 1963, Journal of neurophysiology.

[7]  V. Mountcastle,et al.  THE FUNCTIONAL PROPERTIES OF VENTROBASAL THALAMIC NEURONSSTUDIED IN UNANESTHETIZED MONKEYS. , 1963, Journal of neurophysiology.

[8]  E. Taub,et al.  Movements in monkeys with deafferented forelimbs. , 1963, Experimental neurology.

[9]  M. Knibestöl,et al.  Single unit analysis of mechanoreceptor activity from the human glabrous skin. , 1970, Acta physiologica Scandinavica.

[10]  E. Taub,et al.  Deafferentation in monkeys: Pointing at a target without visual feedback , 1975, Experimental Neurology.

[11]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[12]  D. McCloskey Kinesthetic sensibility. , 1978, Physiological reviews.

[13]  M. Hulliger,et al.  The responses of afferent fibres from the glabrous skin of the hand during voluntary finger movements in man. , 1979, The Journal of physiology.

[14]  E. Bizzi,et al.  Characteristics of motor programs underlying arm movements in monkeys. , 1979, Journal of neurophysiology.

[15]  J. Millar Loci of joint cells in the cuneate and external cuneate nuclei of the cat , 1979, Brain Research.

[16]  E. Fetz,et al.  Responses of identified cells in postcentral cortex of awake monkeys during comparable active and passive joint movements. , 1980, Journal of neurophysiology.

[17]  Esther P. Gardner,et al.  Properties of kinesthetic neurons in somatosensory cortex of awake monkeys , 1981, Brain Research.

[18]  V. A. Jennings,et al.  Somatosensory cortex activity related to position and force. , 1983, Journal of neurophysiology.

[19]  John F. Kalaska,et al.  Spatial coding of movement: A hypothesis concerning the coding of movement direction by motor cortical populations , 1983 .

[20]  G. S. Watson Statistics on Spheres , 1983 .

[21]  J. F. Soechting,et al.  Psychophysical determination of coordinate representation of human arm orientation , 1984, Neuroscience.

[22]  Apostolos P. Georgopoulos,et al.  Static versus dynamic effects in motor cortex and area 5: Comparison during movement time , 1985, Behavioural Brain Research.

[23]  J. H. Kaas,et al.  A sequential representation of the occiput, arm, forearm and hand across the rostrocaudal dimension of areas 1, 2 and 5 in macaque monkeys , 1985, Brain Research.

[24]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

[25]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[26]  A L Towe,et al.  Properties of proprioceptive neurons in the cuneate nucleus of the cat. , 1987, Journal of neurophysiology.

[27]  E P Gardner,et al.  Somatosensory cortical mechanisms of feature detection in tactile and kinesthetic discrimination. , 1988, Canadian journal of physiology and pharmacology.

[28]  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.

[29]  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.

[30]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. III. Positional gradients and population coding of movement direction from various movement origins , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  D G Stuart,et al.  Animal solutions to problems of movement control: the role of proprioceptors. , 1988, Annual review of neuroscience.

[32]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[33]  J. F. Soechting,et al.  Errors in pointing are due to approximations in sensorimotor transformations. , 1989, Journal of neurophysiology.

[34]  C Ghez,et al.  Roles of proprioceptive input in the programming of arm trajectories. , 1990, Cold Spring Harbor symposia on quantitative biology.

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

[36]  A. Georgopoulos,et al.  The motor cortex and the coding of force. , 1992, Science.

[37]  Ziaul Hasan,et al.  Role of proprioceptors in neural control , 1992, Current Opinion in Neurobiology.

[38]  C. Ghez,et al.  Loss of proprioception produces deficits in interjoint coordination. , 1993, Journal of neurophysiology.

[39]  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.

[40]  A B Schwartz,et al.  Direct cortical representation of drawing. , 1994, Science.

[41]  J. Kalaska,et al.  Tactile activity in primate primary somatosensory cortex during active arm movements: cytoarchitectonic distribution. , 1994, Journal of neurophysiology.

[42]  J. Kalaska,et al.  Proprioceptive activity in primate primary somatosensory cortex during active arm reaching movements. , 1994, Journal of neurophysiology.

[43]  S. Scott,et al.  Changes in motor cortex activity during reaching movements with similar hand paths but different arm postures. , 1995, Journal of neurophysiology.

[44]  J. F. Soechting,et al.  Moving effortlessly in three dimensions: does Donders' law apply to arm movement? , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  A. Georgopoulos Current issues in directional motor control , 1995, Trends in Neurosciences.

[46]  F. Lacquaniti,et al.  Representing spatial information for limb movement: role of area 5 in the monkey. , 1995, Cerebral cortex.