Insights into the control of arm movement during body motion as revealed by EMG analyses

Recent studies have revealed that vestibulomotor transformations contribute to maintain the hand stationary in space during trunk rotation. Here we tested whether these vestibulomotor transformations have the same latencies and whether they are subject to similar cognitive control than the visuomotor transformations during manual tracking of a visual target. We recorded hand displacement and shoulder-muscle activity in two tasks: a stabilization task in which subjects stabilized their hand during passive 30 degrees body rotations, and a tracking task in which subjects tracked with their finger a visual target as it moved 30 degrees around them. The EMG response times recorded in the stabilization task (approximately 165 ms) were twice as short as those observed for the tracking task (approximately 350 ms). Tested with the same paradigm, a deafferented subject showed EMG response times that closely matched those recorded in healthy subjects, thus, suggesting a vestibular origin of the arm movements. Providing advance information about the direction of the required arm movement reduced the response times in the tracking task (by approximately 115 ms) but had no significant effect in the stabilization task. Generally, when providing false information about movement direction in the tracking task, an EMG burst first appeared in the muscle moving the arm in the direction opposite to the actual target motion (i.e., in accord with the precueing). This behavior was rarely observed in the stabilization task. These results show that the sensorimotor transformations that move the arm relative to the trunk have shorter latencies when they originate from vestibular inputs than from visual information and that vestibulomotor transformations are more resistant to cognitive processes than visuomotor transformations.

[1]  Christophe Bourdin,et al.  On-line versus off-line vestibular-evoked control of goal-directed arm movements , 2002, Neuroreport.

[2]  I Israël,et al.  Vestibular information contributes to update retinotopic maps. , 1999, Neuroreport.

[3]  Y. Lamarre,et al.  Postural adjustments associated with different unloadings of the forearm: effects of proprioceptive and cutaneous afferent deprivation. , 1995, Canadian journal of physiology and pharmacology.

[4]  E. C. Poulton,et al.  Human Manual Control , 2011 .

[5]  J. C. Rothwell,et al.  Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man , 2004, Experimental Brain Research.

[6]  J D Crawford,et al.  Spatial transformations for eye-hand coordination. , 2004, Journal of neurophysiology.

[7]  A G Feldman,et al.  Vestibular system may provide equivalent motor actions regardless of the number of body segments involved in the task. , 2007, Journal of neurophysiology.

[8]  B. Day,et al.  Vestibular-evoked postural responses in the absence of somatosensory information. , 2002, Brain : a journal of neurology.

[9]  Y. Ivanenko,et al.  Space-time relativity in self-motion reproduction. , 2007, Journal of neurophysiology.

[10]  H. Collewijn The vestibulo-ocular reflex: an outdated concept? , 1989, Progress in brain research.

[11]  Shunsuke Kobayashi,et al.  Modifying the Cortical Processing for Motor Preparation by Repetitive Transcranial Magnetic Stimulation , 2007, Journal of Cognitive Neuroscience.

[12]  N. Teasdale,et al.  Vestibular signal processing in a subject with somatosensory deafferentation: The case of sitting posture , 2007, BMC neurology.

[13]  Visuo-motor control: Giving the brain a hand , 2000, Current Biology.

[14]  F Lacquaniti,et al.  Effect of gaze on postural responses to neck proprioceptive and vestibular stimulation in humans , 1999, The Journal of physiology.

[15]  Jean-Louis Vercher,et al.  Updating visual space during passive and voluntary head-in-space movements , 1998, Experimental Brain Research.

[16]  B W Peterson,et al.  Mechanisms controlling human head stabilization. II. Head-neck characteristics during random rotations in the vertical plane. , 1995, Journal of neurophysiology.

[17]  Simone B. Bortolami,et al.  Kinetic analysis of arm reaching movements during voluntary and passive rotation of the torso , 2008, Experimental Brain Research.

[18]  Philip N. Sabes,et al.  Flexible strategies for sensory integration during motor planning , 2005, Nature Neuroscience.

[19]  D. Rosenbaum Human movement initiation: specification of arm, direction, and extent. , 1980, Journal of experimental psychology. General.

[20]  Borís Burle,et al.  Spatio-temporal dynamics of reach-related neural activity for visual and somatosensory targets , 2009, NeuroImage.

[21]  John C. Rothwell,et al.  What do reflex and voluntary mean? Modern views on an ancient debate , 2000, Experimental Brain Research.

[22]  J Blouin,et al.  Galvanic vestibular stimulation in humans produces online arm movement deviations when reaching towards memorized visual targets , 2002, Neuroscience Letters.

[23]  J. Kelso,et al.  Are movements prepared in parts? Not under compatible (naturalized) conditions. , 1980, Journal of experimental psychology. General.

[24]  David Goodman,et al.  Are movements prepared in parts? Not under compatible (naturalized) conditions. , 1980 .

[25]  G M Gauthier,et al.  Perception of passive whole-body rotations in the absence of neck and body proprioception. , 1995, Journal of neurophysiology.

[26]  R. Chernikoff,et al.  Reaction time to kinesthetic stimulation resulting from sudden arm displacement. , 1952, Journal of experimental psychology.

[27]  J. Fuller,et al.  Head movement propensity , 2004, Experimental Brain Research.

[28]  G. D. P. M. DipTP Introduction to Surface Electromyography , 1998 .

[29]  G. Barnes,et al.  Anticipatory VOR suppression induced by visual and nonvisual stimuli in humans. , 2004, Journal of neurophysiology.

[30]  D. Hoffman,et al.  Step-tracking movements of the wrist in humans. II. EMG analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  F B Horak,et al.  Somatosensory loss increases vestibulospinal sensitivity. , 2001, Journal of neurophysiology.

[32]  D. Guitton,et al.  Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. , 1987, Journal of neurophysiology.

[33]  J F Iles,et al.  Vestibular actions on back and lower limb muscles during postural tasks in man , 2003, The Journal of physiology.

[34]  Luc Proteau,et al.  Effects of stationary and moving textured backgrounds on the visuo-oculo-manual tracking in humans , 1995, Vision Research.

[35]  R. Fitzpatrick,et al.  Task‐dependent reflex responses and movement illusions evoked by galvanic vestibular stimulation in standing humans. , 1994, The Journal of physiology.

[36]  J. Rothwell,et al.  Cortical processing in vestibular navigation. , 2008, Progress in brain research.

[37]  D. Angelaki,et al.  Vestibular system: the many facets of a multimodal sense. , 2008, Annual review of neuroscience.

[38]  Jean-Louis Vercher,et al.  From head orientation to hand control: evidence of both neck and vestibular involvement in hand drawing , 2003, Experimental Brain Research.

[39]  A. G. Feldman,et al.  Arm–trunk coordination in the absence of proprioception , 2003, Experimental Brain Research.

[40]  Robert Shapiro,et al.  Kinematic and EMG characteristics of simple shoulder movements with proprioception and visual feedback. , 2006, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[41]  L. Snyder This way up: illusions and internal models in the vestibular system , 1999, Nature Neuroscience.

[42]  J. Lackner,et al.  Coordinated turn-and-reach movements. I. Anticipatory compensation for self-generated coriolis and interaction torques. , 2003, Journal of neurophysiology.

[43]  D M Merfeld,et al.  Humans use internal models to estimate gravity and linear acceleration , 1999, Nature.

[44]  R. Sainburg,et al.  The effect of target modality on visual and proprioceptive contributions to the control of movement distance , 2006, Experimental Brain Research.

[45]  Anatol G. Feldman,et al.  Vestibular contribution to combined arm and trunk motion , 2003, Experimental Brain Research.

[46]  J. A. Pruszynski,et al.  Long-Latency Reflexes of the Human Arm Reflect an Internal Model of Limb Dynamics , 2008, Current Biology.

[47]  F. Plum Handbook of Physiology. , 1960 .

[48]  P. Cavallari,et al.  Effects of transmastoid electrical stimulation on the triceps brachii EMG in man. , 1990, Neuroreport.

[49]  Jefferson E. Roy,et al.  Selective Processing of Vestibular Reafference during Self-Generated Head Motion , 2001, The Journal of Neuroscience.

[50]  N Nighoghossian,et al.  Evidence for interacting cortical control of vestibular function and spatial representation in man , 2003, Neuropsychologia.

[51]  Michel Guerraz,et al.  Expectation and the Vestibular Control of Balance , 2005, Journal of Cognitive Neuroscience.

[52]  Rüdiger Wenzel,et al.  Human Vestibular Cortex as Identified with Caloric Stimulation in Functional Magnetic Resonance Imaging , 2002, NeuroImage.

[53]  C. Marsden,et al.  Stretch reflex and servo action in a variety of human muscles. , 1976, The Journal of physiology.

[54]  Howard Poizner,et al.  Hand trajectory invariance in reaching movements involving the trunk , 2001, Experimental Brain Research.

[55]  Martha Flanders,et al.  Manual tracking in three dimensions , 2005, Experimental Brain Research.