Corticospinal control during reach, grasp, and precision lift in man

Transcranial magnetic brain stimulation (TMS) was used to assess the influence of the corticospinal system on motor output in seven human subjects during a task in which they had to reach out, grasp, and lift an object. Stimuli, directed at the hand area of the motor cortex, were delivered at eight defined points during the task: during reach, at grip closure, during object manipulation, during the parallel isometric increase in grip and load forces, during the lifting movement, and while the object was held in air. The amplitudes of short-latency EMG responses evoked by TMS in six arm and hand muscles showed a striking modulation across the different phases of the task. This modulation may well reflect phasic changes in corticospinal excitability because: (1) it did not simply reflect phasic changes in muscular activity associated with task performance, (2) it could vary inversely with the amplitude of the background EMG, and (3) it was only obtained with weak TMS intensities, below threshold for evoking responses in hand muscles of the relaxed subject. Our results suggest that the cortical representations of extrinsic hand muscles, which act to orientate the hand and finger tips, were subjected to a strong excitatory drive throughout the reach. This drive was also observed for brachioradialis and anterior deltoid, which contribute to transport of the hand. In contrast, the intrinsic hand muscles appear to receive their strongest cortical input as the digits closed around the object, and just after the subject first touched the object at the onset of manipulation. The isometric parallel increase in load and grip forces necessary to lift the object, which is normally triggered by tactile contact, was delayed by TMS delivered late during the reach. TMS at this time may disrupt processing necessary to control this critical phase of the task.

[1]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[2]  R. Porter,et al.  Relationship between the activity of precentral neurones during active and passive movements in conscious monkeys , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[3]  B Alstermark,et al.  Integration in descending motor pathways controlling the forelimb in the cat. 9. Differential behavioural defects after spinal cord lesions interrupting defined pathways from higher centres to motoneurones. , 1981, Experimental brain research.

[4]  R. Lemon.  Functional properties of monkey motor cortex neurones receiving afferent input from the hand and fingers , 1981, The Journal of physiology.

[5]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  R. Lemon,et al.  Corticospinal neurons with a special role in precision grip , 1983, Brain Research.

[7]  E. Evarts,et al.  Motor Cortex control of finely graded forces. , 1983, Journal of neurophysiology.

[8]  M. Jeannerod.  The timing of natural prehension movements. , 1984, Journal of motor behavior.

[9]  T. Drew,et al.  Forelimb electromyographic responses to motor cortex stimulation during locomotion in the cat. , 1985, The Journal of physiology.

[10]  J. Murphy,et al.  Sequential activation of neurons in primate motor cortex during unrestrained forelimb movement. , 1985, Journal of neurophysiology.

[11]  R. Lemon,et al.  Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey. , 1986, The Journal of physiology.

[12]  M. Arbib,et al.  Opposition Space as a Structuring Concept for the Analysis of Skilled Hand Movements , 1986 .

[13]  M. Jeannerod.  The formation of finger grip during prehension. A cortically mediated visuomotor pattern , 1986, Behavioural Brain Research.

[14]  J. T. Murphy,et al.  Interaction between neurons in precentral cortical zones controlling different joints , 1987, Brain Research.

[15]  K. Mills,et al.  Responses in small hand muscles from magnetic stimulation of the human brain. , 1987, The Journal of physiology.

[16]  B L Day,et al.  Delay in the execution of voluntary movement by electrical or magnetic brain stimulation in intact man. Evidence for the storage of motor programs in the brain. , 1989, Brain : a journal of neurology.

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

[18]  H. Freund,et al.  Sensorimotor disturbances in patients with lesions of the parietal cortex. , 1989, Brain : a journal of neurology.

[19]  L M Harrison,et al.  Task‐dependent changes in the size of response to magnetic brain stimulation in human first dorsal interosseous muscle. , 1989, The Journal of physiology.

[20]  L. Toothaker.  Book Review : Nonparametric Statistics for the Behavioral Sciences (Second Edition) , 1989 .

[21]  S. Miller,et al.  Excitation of the corticospinal tract by electromagnetic and electrical stimulation of the scalp in the macaque monkey. , 1990, The Journal of physiology.

[22]  A. M. Smith,et al.  Purkinje cell simple spike activity during grasping and lifting objects of different textures and weights. , 1990, Journal of neurophysiology.

[23]  B. Day,et al.  Stimulation of the human motor cortex through the scalp , 1991, Experimental physiology.

[24]  Karl J. Friston,et al.  Regional cerebral blood flow during voluntary arm and hand movements in human subjects. , 1991, Journal of neurophysiology.

[25]  M. Hepp-Reymond,et al.  Contrasting properties of monkey somatosensory and motor cortex neurons activated during the control of force in precision grip. , 1991, Journal of neurophysiology.

[26]  J C Rothwell,et al.  Changes in the response to magnetic and electrical stimulation of the motor cortex following muscle stretch in man. , 1991, The Journal of physiology.

[27]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[28]  A. M. Smith,et al.  Primary motor cortical activity related to the weight and texture of grasped objects in the monkey. , 1992, Journal of neurophysiology.

[29]  P Ashby,et al.  Evidence that a long latency stretch reflex in humans is transcortical. , 1992, The Journal of physiology.

[30]  P Ashby,et al.  Corticospinal projections to upper limb motoneurones in humans. , 1992, The Journal of physiology.

[31]  Lemon Rn,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993 .

[32]  U. Kischka,et al.  Facilitation of motor evoked potentials from magnetic brain stimulation in man: a comparative study of different target muscles. , 1993, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[33]  R N Lemon,et al.  Task dependence of responses in first dorsal interosseous muscle to magnetic brain stimulation in man. , 1993, The Journal of physiology.

[34]  R. Lemon,et al.  Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. , 1993, Journal of neurophysiology.

[35]  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.

[36]  K. Sakai,et al.  Excitation of the motor cortex associated with the E2 phase of cutaneous reflexes in man , 1994, Brain Research.

[37]  E. Pierrot-Deseilligny,et al.  Evidence for corticospinal excitation of presumed propriospinal neurones in man. , 1994, The Journal of physiology.

[38]  R. Lemon,et al.  The influence of single monkey cortico‐motoneuronal cells at different levels of activity in target muscles. , 1994, The Journal of physiology.

[39]  R. Johansson,et al.  Time‐varying enhancement of human cortical excitability mediated by cutaneous inputs during precision grip. , 1994, The Journal of physiology.

[40]  S. Rossignol,et al.  Microstimulation of the medullary reticular formation during fictive locomotion. , 1994, Journal of neurophysiology.

[41]  R S Johansson,et al.  Grasp stability during manipulative actions. , 1994, Canadian journal of physiology and pharmacology.

[42]  E. Pierrot-Deseilligny,et al.  Non‐monosynaptic transmission of the cortical command for voluntary movement in man. , 1994, The Journal of physiology.

[43]  G. Deuschl,et al.  Effects of electric and magnetic transcranial stimulation on long latency reflexes , 2004, Experimental Brain Research.

[44]  A. M. Smith,et al.  Relation of activity in precentral cortical neurons to force and rate of force change during isometric contractions of finger muscles , 1975, Experimental Brain Research.

[45]  A. Lundberg,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 1977, Experimental Brain Research.

[46]  Etienne Olivier,et al.  Recording an identified pyramidal volley evoked by transcranial magnetic stimulation in a conscious macaque monkey , 2004, Experimental Brain Research.