Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations

It has been proposed that the premotor cortex plays a role in the selection of motor programs based on environmental context. To test this hypothesis, we recorded the activity of single neurons as monkeys learned visuomotor associations. The hypothesis predicts that task- related premotor cortical activity before learning should differ from that afterward. We found that a substantial population of premotor cortex neurons, over half of those adequately tested, showed the predicted learning-dependent changes in activity. The present findings support a role for premotor cortex in motor preparation, generally, and suggest a specific role in the selection of movements on the basis of arbitrary associations.

[1]  H. Harlow,et al.  The formation of learning sets. , 1949, Psychological review.

[2]  D. Marr.  A theory of cerebellar cortex , 1969, The Journal of physiology.

[3]  Y. Ben-Ari.  Plasticity at unitary level. I. An experimental design. , 1972, Electroencephalography and clinical neurophysiology.

[4]  Y. Ben-Ari,et al.  Plasticity at unitary level. II. Modifications during sensory-sensory association procedures. , 1972, Electroencephalography and clinical neurophysiology.

[5]  P. Gilbert.  How the cerebellum could memorise movements , 1975, Nature.

[6]  W. T. Thach,et al.  Purkinje cell activity during motor learning , 1977, Brain Research.

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

[8]  V. B. Brooks,et al.  Learning of pursuit visuo-motor tracking by monkeys , 1978, Physiology & Behavior.

[9]  Giacomo Rizzolatti,et al.  Neurons responding to visual stimuli in the frontal lobe of macaque monkeys , 1979, Neuroscience Letters.

[10]  G. Rizzolatti,et al.  Afferent properties of periarcuate neurons in macaque monkeys. I. Somatosensory responses , 1981, Behavioural Brain Research.

[11]  G. Rizzolatti,et al.  Response properties and behavioral modulation of ‘mouth’ neurons of the postarcuate cortex (area 6) in macaque monkeys , 1981, Brain Research.

[12]  Changes of premovement field potentials in the cerebral cortex during learning processes of visually initiated hand movements in the monkey , 1981, Neuroscience Letters.

[13]  M. Petrides.  Motor conditional associative-learning after selective prefrontal lesions in the monkey , 1982, Behavioural Brain Research.

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

[15]  R. Passingham,et al.  The role of premotor and parietal cortex in the direction of action , 1982, Brain Research.

[16]  V. B. Brooks,et al.  Movement programming depends on understanding of behavioral requirements , 1983, Physiology & Behavior.

[17]  R. Lemon,et al.  Involvement of Monkey Premotor Cortex in the Preparation of Arm Movements , 1983 .

[18]  V. Brooks.  The Cerebellum and Adaptive Tuning of Movements , 1984 .

[19]  P. Strick,et al.  The origin of thalamic inputs to the arcuate premotor and supplementary motor areas , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  伊藤 正男.  The cerebellum and neural control , 1984 .

[21]  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.

[22]  D. Pandya,et al.  Supplementary motor area structure and function: Review and hypotheses , 1985 .

[23]  S. Wise.  The primate premotor cortex: past, present, and preparatory. , 1985, Annual review of neuroscience.

[24]  Hidehiko Komatsu,et al.  Neuron activities of monkey prefrontal cortex during the learning of visual discrimination tasks with GO/NO-GO performances , 1985, Neuroscience Research.

[25]  M. Petrides.  Deficits in non-spatial conditional associative learning after periarcuate lesions in the monkey , 1985, Behavioural Brain Research.

[26]  Steven P. Wise,et al.  The primate promoter cortex fifty years after Fulton , 1985, Behavioural Brain Research.

[27]  M. Petrides.  Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man , 1985, Neuropsychologia.

[28]  R. Lemon,et al.  The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements , 1985, Behavioural Brain Research.

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

[30]  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.

[31]  E. Vaadia,et al.  Unit study of monkey frontal cortex: active localization of auditory and of visual stimuli. , 1986, Journal of neurophysiology.

[32]  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.

[33]  V B Brooks,et al.  How does the limbic system assist motor learning? A limbic comparator hypothesis. , 1986, Brain, behavior and evolution.

[34]  C. Woody.  Understanding the cellular basis of memory and learning. , 1986, Annual review of psychology.

[35]  R. Passingham.  Two cortical systems for directing movement. , 1987, Ciba Foundation symposium.

[36]  Maeve O'Connor,et al.  Ciba Foundation Symposium 132 - Motor Areas of the Cerebral Cortex , 1987 .

[37]  D. Humphrey,et al.  The compensatory role of the parvocellular division of the red nucleus in operantly conditioned rats , 1987, Neuroscience Research.

[38]  Takashi Sakamoto,et al.  Long-lasting potentiation of synaptic potentials in the motor cortex produced by stimulation of the sensory cortex in the cat: a basis of motor learning , 1987, Brain Research.

[39]  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.

[40]  Cortical control of sensory-motor integration , 1988, Neuropsychologia.

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

[42]  David Gaffan,et al.  Inferotemporal-frontal disconnection and fornix transection in visuomotor conditional learning by monkeys , 1988, Behavioural Brain Research.

[43]  D. Crowne,et al.  Unilateral periarcuate and posterior parietal lesions impair conditional position discrimination learning in the monkey , 1989, Neuropsychologia.

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

[45]  J. Wolpaw,et al.  Memory traces in spinal cord produced by H-reflex conditioning: Effects of post-tetanic potentiation , 1989, Neuroscience Letters.

[46]  B. Rockstroh,et al.  The cerebellum contributes to mental skills. , 1989 .

[47]  M E Goldberg,et al.  Participation of prefrontal neurons in the preparation of visually guided eye movements in the rhesus monkey. , 1989, Journal of neurophysiology.

[48]  J. Wolpaw,et al.  Memory traces in primate spinal cord produced by operant conditioning of H-reflex. , 1989, Journal of neurophysiology.

[49]  A. Keller,et al.  Long-term potentiation in the motor cortex. , 1989, Science.

[50]  D. Diamond,et al.  Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. , 1989, Behavioral neuroscience.

[51]  B. Rockstroh,et al.  The cerebellum contributes to mental skills , 1989 .

[52]  R. Passingham,et al.  SUPPLEMENTARY MOTOR CORTEX AND SELF-INITIATED MOVEMENT , 1989 .

[53]  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.

[54]  G. Lynch,et al.  The neurobiology of learning and memory , 1989, Cognition.

[55]  S. Wise,et al.  Trajectory-selective neuronal activity in the motor cortex of rhesus monkeys (Macaca mulatta). , 1990, Behavioral neuroscience.

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

[57]  Paul B. Johnson,et al.  Making arm movements within different parts of space: dynamic aspects in the primate motor cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  R. Beauchamp.  VISION, MEMORY, AND THE TEMPORAL LOBE , 1991 .