Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons.

The ventral premotor area (F5) is part of the cortical circuit controlling visuomotor grasp. F5 could influence hand motor function through at least two pathways: corticospinal projections and corticocortical projections to primary motor cortex (M1). We found that stimulation of macaque F5, which by itself evoked little or no detectable corticospinal output, could produce a robust modulation of motor outputs from M1. Arrays of fine microwires were implanted in F5 and M1. During terminal experiments under chloralose anesthesia, single stimuli delivered to M1 electrodes evoked direct (D) and indirect (I1,I2, and I3) corticospinal volleys. In contrast, single F5 shocks were ineffective; double shocks (3 msec separation) evoked small I waves but no D wave. However, when the test (T) M1 shock was conditioned (C) by single or double F5 shocks, there was strong facilitation of I2 and I3 waves from M1, with C-T intervals of <1 msec. Intracellular recordings from 79 arm and hand motoneurons (MNs) revealed no postsynaptic effects from single F5 shocks. In contrast, these stimuli produced a robust facilitation of I2 and I3 EPSPs evoked from M1 (60% of MNs); this was particularly marked in hand muscle MNs (92%). Muscimol injection in M1 reduced I waves from F5 and abolished the F5-induced facilitation of late I waves from M1, and of EPSPs associated with them. Thus, some motor effects evoked from F5 may be mediated by corticocortical inputs to M1 impinging on interneurons generating late corticospinal I waves. Similar mechanisms may allow F5 to modulate grasp-related outputs from M1.

[1]  R. Lemon,et al.  Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study , 2004, Experimental Brain Research.

[2]  R. Lemon,et al.  Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles. , 2003, Journal of neurophysiology.

[3]  D. Hoffman,et al.  Sensorimotor transformations in cortical motor areas , 2003, Neuroscience Research.

[4]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[5]  Diane Ruge,et al.  Short‐interval paired‐pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity , 2002, The Journal of physiology.

[6]  G. Rizzolatti,et al.  Motor and cognitive functions of the ventral premotor cortex , 2002, Current Opinion in Neurobiology.

[7]  R. Lemon,et al.  Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study. , 2002, Cerebral cortex.

[8]  S. Lisberger,et al.  Enhancement of multiple components of pursuit eye movement by microstimulation in the arcuate frontal pursuit area in monkeys. , 2002, Journal of neurophysiology.

[9]  J. Rothwell,et al.  Functional Connectivity of Human Premotor and Motor Cortex Explored with Repetitive Transcranial Magnetic Stimulation , 2002, The Journal of Neuroscience.

[10]  John C. Rothwell,et al.  Transcranial Magnetic Stimulation Can Be Used to Test Connections to Primary Motor Areas from Frontal and Medial Cortex in Humans , 2001, NeuroImage.

[11]  D. Hoffman,et al.  Direction of action is represented in the ventral premotor cortex , 2001, Nature Neuroscience.

[12]  G. Rizzolatti,et al.  Cortical mechanism for the visual guidance of hand grasping movements in the monkey: A reversible inactivation study. , 2001, Brain : a journal of neurology.

[13]  Stephen G. Lisberger,et al.  Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex , 2001, Nature.

[14]  J C Rothwell,et al.  I-Waves in Motor Cortex , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[15]  A. Nambu,et al.  Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: An electrophysiological study in the macaque monkey. , 2000, Cerebral cortex.

[16]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

[17]  P. Mazzone,et al.  Effects of voluntary contraction on descending volleys evoked by transcranial electrical stimulation over the motor cortex hand area in conscious humans , 1999, Experimental Brain Research.

[18]  C. Ghez,et al.  Pharmacological inactivation in the analysis of the central control of movement , 1999, Journal of Neuroscience Methods.

[19]  S. N. Baker,et al.  An investigation of the intrinsic circuitry of the motor cortex of the monkey using intra-cortical microstimulation , 1998, Experimental Brain Research.

[20]  R. Lemon,et al.  Does a C3‐C4 propriospinal system transmit corticospinal excitation in the primate? An investigation in the macaque monkey , 1998, The Journal of physiology.

[21]  Walter Paulus,et al.  Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation , 1998, The Journal of physiology.

[22]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[23]  G. Rizzolatti,et al.  Object representation in the ventral premotor cortex (area F5) of the monkey. , 1997, Journal of neurophysiology.

[24]  J C Rothwell,et al.  Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[25]  Andrew R Mitz,et al.  Somatotopy of monkey premotor cortex examined with microstimulation , 1995, Neuroscience Research.

[26]  M. Hepp-Reymond,et al.  Force-related neuronal activity in two regions of the primate ventral premotor cortex. , 1994, Canadian journal of physiology and pharmacology.

[27]  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.

[28]  R. Porter,et al.  Corticospinal Function and Voluntary Movement , 1993 .

[29]  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.

[30]  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.

[31]  B. Day,et al.  Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. , 1989, The Journal of physiology.

[32]  R Porter,et al.  Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. , 1988, The Journal of physiology.

[33]  C. G. Phillips,et al.  A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis) , 1987, The Journal of comparative neurology.

[34]  V. Amassian,et al.  Physiological basis of motor effects of a transient stimulus to cerebral cortex. , 1987, Neurosurgery.

[35]  G. Rizzolatti,et al.  Afferent and efferent projections of the inferior area 6 in the macaque monkey , 1986, The Journal of comparative neurology.

[36]  Arthur Prochazka,et al.  Methods for neuronal recording in conscious animals , 1984 .

[37]  E. Murray,et al.  Organization of corticospinal neurons in the monkey , 1981, The Journal of comparative neurology.

[38]  P. Strick,et al.  Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas , 1979, Brain Research.

[39]  H Suzuki,et al.  A glass-insulated "Elgiloy" microelectrode for recording unit activity in chronic monkey experiments. , 1976, Electroencephalography and clinical neurophysiology.

[40]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[41]  D. Kernell,et al.  Responses of the pyramidal tract to stimulation of the baboon's motor cortex , 1967, The Journal of physiology.

[42]  V. Amassian,et al.  Single and multiple-unit analysis of cortical stage of pyramidal tract activation. , 1954, Journal of neurophysiology.