Role of primary sensorimotor cortices in generating inhibitory motor response in humans.

To clarify the mechanism by which inhibitory motor responses such as cortical negative myoclonus are generated in humans, three patients with medically intractable partial epilepsy (two with frontal lobe epilepsy and one with parietal lobe epilepsy) were studied by means of direct cortical stimulation with a single electric pulse through subdural electrodes. All underwent chronic long-term video/EEG monitoring, cortical mapping by 50 Hz electric cortical stimulation and recording of cortical somatosensory evoked potentials with chronically implanted subdural grid electrodes (3 mm in diameter and centre-to-centre distance of 1 cm) to map both epileptogenic and functional zones. After these clinical evaluations, cortical stimulation by single electric pulse (0.3 ms duration, 1 Hz) was carried out through pairs of subdural electrodes located at the primary sensorimotor area (MI-SI), pre-supplementary motor area (pre-SMA) and lateral negative motor area (lateral NMA), while surface EMG was recorded from the muscles of the contralateral hand. The results showed that (i) in all subjects, single pulse stimulation of MI-SI elicited a motor evoked potential (MEP) followed by a silent period (SP) in the contralateral distal hand muscles, the latter lasting 300 ms after the stimulus. The duration of SP was proportional to the size of the preceding MEP. In one subject, SP without any preceding MEP was elicited, and, in another subject, there was a short SP immediately before MEP in the contralateral thenar muscle. (ii) Following the stimulation of either pre-SMA or lateral NMA, no SP was observed. It is concluded that the inhibitory mechanism within the MI-SI, but probably not in the non-primary motor areas, either closely linked to or completely independent of excitation, most likely plays an important role in eliciting brief negative motor phenomena such as cortical negative myoclonus or SP.

[1]  H. Lüders,et al.  Movement-related potentials recorded from supplementary motor area and primary motor area. Role of supplementary motor area in voluntary movements. , 1992, Brain : a journal of neurology.

[2]  J C Rothwell,et al.  Physiological studies of electric and magnetic stimulation of the human brain. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[3]  B. Shahani,et al.  Physiological and pharmacological aids in the differential diagnosis of tremor. , 1976, Journal of neurology, neurosurgery, and psychiatry.

[4]  B LIBET,et al.  PRODUCTION OF THRESHOLD LEVELS OF CONSCIOUS SENSATION BY ELECTRICAL STIMULATION OF HUMAN SOMATOSENSORY CORTEX. , 1964, Journal of neurophysiology.

[5]  C. G. Phillips,et al.  Selective excitation of corticofugal neurones by surface‐anodal stimulation of the baboon's motor cortex , 1962, The Journal of physiology.

[6]  G. Thickbroom,et al.  Topography of excitatory and inhibitory muscle responses evoked by transcranial magnetic stimulation in the human motor cortex , 1993, Neuroscience Letters.

[7]  M Hallett,et al.  Effects of phenytoin on cortical excitability in humans , 1997, Neurology.

[8]  T. Mima,et al.  Cortical reflex negative myoclonus. , 1994, Brain : a journal of neurology.

[9]  N. Thakor,et al.  Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. , 1993, Electroencephalography and clinical neurophysiology.

[10]  C. Elger,et al.  Penicillin-induced epileptic foci in the motor cortex: vertical inhibition. , 1983, Electroencephalography and clinical neurophysiology.

[11]  E Wyllie,et al.  Cortical electrical stimulation in humans. The negative motor areas. , 1995, Advances in neurology.

[12]  H Shibasaki,et al.  Cognitive motor control in human pre-supplementary motor area studied by subdural recording of discrimination/selection-related potentials. , 1999, Brain : a journal of neurology.

[13]  B. Steinhoff,et al.  Effects of antiepileptic drugs on motor cortex excitability in humans: A transcranial magnetic stimulation study , 1996, Annals of neurology.

[14]  Jerome Engel,et al.  Surgical treatment of the epilepsies , 1993 .

[15]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[16]  K Zilles,et al.  Anatomy and transmitter receptors of the supplementary motor areas in the human and nonhuman primate brain. , 1996, Advances in neurology.

[17]  H. Luders Commentary: chronic intracranial recording and stimulation with subdural electrodes , 1987 .

[18]  H. Oguni,et al.  A Study of Unilateral Brief Focal Atonia in Childhood Partial Epilepsy , 1992, Epilepsia.

[19]  S. C. Gandevia,et al.  Effect of contraction strength on responses in biceps brachii and adductor pollicis to transcranial magnetic stimulation , 1997, Experimental Brain Research.

[20]  C. Tassinari,et al.  Frontal inhibitory spike component associated with epileptic negative myoclonus. , 1995, Electroencephalography and clinical neurophysiology.

[21]  J. Rothwell Control of Human Voluntary Movement , 1994, Springer Netherlands.

[22]  M Hallett,et al.  Transcranial magnetic stimulation. Negative effects. , 1995, Advances in neurology.

[23]  H. Lüders,et al.  Epileptic negative myoclonus , 1997, Neurology.

[24]  G. Deuschl,et al.  Differential diagnosis of tremor. , 1999, Journal of neural transmission. Supplementum.

[25]  M. Hallett,et al.  Spinal motor neuron excitability during the silent period after cortical stimulation. , 1991, Electroencephalography and clinical neurophysiology.

[26]  U. Pietrzyk,et al.  Epileptic negative myoclonus , 1996, Neurology.

[27]  K. Takahashi,et al.  Slow and fast groups of pyramidal tract cells and their respective membrane properties. , 1965, Journal of neurophysiology.

[28]  H. Lüders,et al.  Localization of Cortical Function: New Information from Extraoperative Monitoring of Patients with Epilepsy , 1988, Epilepsia.

[29]  E M Schmidt,et al.  Microstimulation mapping of precentral cortex during trained movements. , 1990, Journal of neurophysiology.

[30]  V E Amassian,et al.  A comparison of corticospinal activation by magnetic coil and electrical stimulation of monkey motor cortex. , 1990, Electroencephalography and clinical neurophysiology.

[31]  A Berardelli,et al.  Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. , 1993, The Journal of physiology.

[32]  T. Mima,et al.  Cortical myoclonus , 1998, Neurology.

[33]  C. Tassinari,et al.  Epileptic negative myoclonus , 1998, Neurology.

[34]  J. Zentner,et al.  Surgical treatment of epilepsies. , 2002, Acta neurochirurgica. Supplement.

[35]  J Valls-Solé,et al.  Topography of the inhibitory and excitatory responses to transcranial magnetic stimulation in a hand muscle. , 1993, Electroencephalography and clinical neurophysiology.

[36]  H. Shibasaki,et al.  Neurophysiology of positive and negative myoclonus. , 1998, Electroencephalography and clinical neurophysiology.

[37]  P H Ellaway,et al.  Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man. , 1994, The Journal of physiology.