Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task

The activity of cells in primary motor cortex (MI) and dorsal premotor cortex (PMd) were compared during reaching movements in a reaction-time (RT) task, without prior instructions, which required precise control of limb posture before and after movement. MI neurons typically showed strong, directionally tuned activity prior to and during movement as well as large gradations of tonic activity while holding the limb over different targets. The directionality of their movementand posture-related activity was generally similar. Proximal-arm muscles behaved similarly. This is consistent with a role for MI in the moment-to-moment control of motor output, including both movement and actively maintained postures, and suggests a common functional relation for MI cells to both aspects of motor behavior. In contrast, PMd cells were generally more phasic, frequently emitting only strong bursts of activity confined mainly to the behavioral reaction time before movement onset. PMd tonic activity during different postures was generally weaker than in MI, and showed a much more variable relation with their movement-related directional tuning. These results imply that the major contribution of PMd to this RT task occurred prior to the onset of movement itself, consistent with a role for PMd in the selection and planning of visually guided movements. Furthermore, the nature of the relative contribution of PMd to movement versus actively maintained postures appears to be fundamentally different from that in MI. Finally, there was a continuous gradient of changes in responses across the rostrocaudal extent of the precentral gyrus, with no abrupt transition in response properties between PMd and MI.

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

[2]  Kanti V. Mardia,et al.  Statistics of Directional Data , 1972 .

[3]  H C Kwan,et al.  Spatial organization of precentral cortex in awake primates. II. Motor outputs. , 1978, Journal of neurophysiology.

[4]  I. Hamada,et al.  Visual tracking and neuron activity in the post-arcuate area in monkeys. , 1978, Journal de physiologie.

[5]  J. Murphy,et al.  Spatial organization of precentral cortex in awake primates. III. Input-output coupling. , 1978, Journal of neurophysiology.

[6]  S P Wise,et al.  Submodality distribution in sensorimotor cortex of the unanesthetized monkey. , 1981, Journal of neurophysiology.

[7]  S. Wise,et al.  The premotor cortex of the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  J. B. Preston,et al.  Two representations of the hand in area 4 of a primate. II. Somatosensory input organization. , 1982, Journal of neurophysiology.

[9]  M. Wiesendanger,et al.  Structural and functional definition of the motor cortex in the monkey (Macaca fascicularis) , 1982, The Journal of physiology.

[10]  N. Hogan An organizing principle for a class of voluntary movements , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  S. Wise,et al.  A neurophysiological study of the premotor cortex in the rhesus monkey. , 1984, Brain : a journal of neurology.

[12]  S. P. Wise,et al.  Set-related neuronal activity in the premotor cortex of rhesus monkeys: effects of changes in motor set , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[13]  H. Freund,et al.  Lesions of premotor cortex in man. , 1985, Brain : a journal of neurology.

[14]  G. Rizzolatti,et al.  Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey , 1985, Behavioural Brain Research.

[15]  R. Passingham,et al.  Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis) , 1985, Behavioural Brain Research.

[16]  J. Tanji,et al.  Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  M. Petrides The effect of periarcuate lesions in the monkey on the performance of symmetrically and asymmetrically reinforced visual and auditory go, no- go tasks , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  S P Wise,et al.  Movement-related activity in the premotor cortex of rhesus macaques. , 1986, Progress in brain research.

[19]  D. Pandya,et al.  Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey , 1987, The Journal of comparative neurology.

[20]  J. Tanji,et al.  Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. , 1988, Journal of neurophysiology.

[21]  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.

[22]  S. Wise,et al.  Neuronal activity preceding directional and nondirectional cues in the premotor cortex of rhesus monkeys. , 1988, Somatosensory & motor research.

[23]  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.

[24]  J. Kalaska,et al.  A comparison of movement direction-related versus load direction- related activity in primate motor cortex, using a two-dimensional reaching task , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  R. Passingham Premotor cortex and the retrieval of movement. , 1989, Brain, behavior and evolution.

[26]  A. Riehle,et al.  Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. , 1989, Journal of neurophysiology.

[27]  H. Freund,et al.  Premotor cortex and conditional motor learning in man. , 1990, Brain : a journal of neurology.

[28]  PL Strick,et al.  The origin of thalamic inputs to the "hand" representation in the primary motor cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[30]  S. Wise,et al.  Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  R Caminiti,et al.  Making arm movements within different parts of space: the premotor and motor cortical representation of a coordinate system for reaching to visual targets , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Kiyoshi Kurata,et al.  Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys , 1991, Neuroscience Research.

[33]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  S P Wise,et al.  A neurophysiological comparison of three distinct regions of the primate frontal lobe. , 1991, Brain : a journal of neurology.

[35]  A. Georgopoulos Higher order motor control. , 1991, Annual review of neuroscience.

[36]  J. Kalaska,et al.  Cerebral cortical mechanisms of reaching movements. , 1992, Science.

[37]  S P Wise,et al.  Primate premotor cortex: dissociation of visuomotor from sensory signals. , 1992, Journal of neurophysiology.

[38]  E. Fetz Movement control: Are movement parameters recognizably coded in the activity of single neurons? , 1992 .

[39]  G. L. Gottlieb,et al.  Virtual trajectories of single-joint movements performed under two basic strategies , 1992, Neuroscience.

[40]  K Okano TEMPORAL PRIORITY OF PREMOTOR CORTEX OVER NEARBY AREAS IN RECEIVING VISUAL CUES IN PRIMATES , 1992, Neuroreport.

[41]  J. Tanji,et al.  The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. , 1993, Brain : a journal of neurology.

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

[43]  J. Kalaska,et al.  Motor Cortex and Visuomotor Behavior , 1993, Exercise and sport sciences reviews.

[44]  A. Georgopoulos,et al.  Cognitive neurophysiology of the motor cortex. , 1993, Science.

[45]  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.

[46]  K. Kurata,et al.  Premotor cortex of monkeys: set- and movement-related activity reflecting amplitude and direction of wrist movements. , 1993, Journal of neurophysiology.

[47]  J. Kaas,et al.  Architectionis, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys , 1993, The Journal of comparative neurology.

[48]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  S. Grossberg,et al.  A Self-Organizing Neural Model of Motor Equivalent Reaching and Tool Use by a Multijoint Arm , 1993, Journal of Cognitive Neuroscience.

[50]  S. Wise,et al.  Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  I. Darian‐Smith,et al.  Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. , 1994, Cerebral cortex.

[52]  J. Kaas,et al.  Thalamic connections of the primary motor cortex (M1) of owl monkeys , 1994, The Journal of comparative neurology.

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

[54]  A. G. Feldman,et al.  The origin and use of positional frames of reference in motor control , 1995, Behavioral and Brain Sciences.

[55]  T. Ebner,et al.  Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. , 1995, Journal of neurophysiology.

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

[57]  S. P. Wise,et al.  Premotor cortex of rhesus monkeys: set-related activity during two conditional motor tasks , 2004, Experimental Brain Research.

[58]  K. Kurata,et al.  Distribution of neurons with set- and movement-related activity before hand and foot movements in the premotor cortex of rhesus monkeys , 2004, Experimental Brain Research.

[59]  A. P. Georgopoulos,et al.  Cognitive spatial-motor processes , 2004, Experimental Brain Research.

[60]  J. Kalaska,et al.  Parietal area 5 neuronal activity encodes movement kinematics, not movement dynamics , 2004, Experimental Brain Research.

[61]  J. T. Massey,et al.  Cognitive spatial-motor processes , 2004, Experimental Brain Research.

[62]  C. Fromm,et al.  Phasic and tonic responses of premotor and primary motor cortex neurons to torque changes , 2004, Experimental Brain Research.

[63]  S. Wise,et al.  Premotor cortex of the rhesus monkey: neuronal activity in anticipation of predictable environmental events , 2004, Experimental Brain Research.

[64]  S. Wise,et al.  Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys , 2004, Experimental Brain Research.

[65]  J. Tanji,et al.  Neuronal activities in the primate motor fields of the agranular frontal cortex preceding visually triggered and self-paced movement , 2004, Experimental Brain Research.

[66]  R. Caminiti,et al.  Cortical networks for visual reaching , 2004, Experimental Brain Research.

[67]  C. Fromm,et al.  Static firing rates of premotor and primary motor cortical neurons associated with torque and joint position , 2004, Experimental Brain Research.

[68]  A. Georgopoulos,et al.  Static spatial effects in motor cortex and area 5: Quantitative relations in a two-dimensional space , 1984, Experimental Brain Research.

[69]  A. P. Georgopoulos,et al.  Cognitive spatial-motor processes , 1989, Experimental Brain Research.