On the nature of the vestibular control of arm-reaching movements during whole-body rotations

Recent studies report efficient vestibular control of goal-directed arm movements during body motion. This contribution tested whether this control relies (a) on an updating process in which vestibular signals are used to update the perceived egocentric position of surrounding objects when body orientation changes, or (b) on a sensorimotor process, i.e. a transfer function between vestibular input and the arm motor output that preserves hand trajectory in space despite body rotation. Both processes were separately and specifically adapted. We then compared the respective influences of the adapted processes on the vestibular control of arm-reaching movements. The rationale was that if a given process underlies a given behavior, any adaptive modification of this process should give rise to observable modification of the behavior. The updating adaptation adapted the matching between vestibular input and perceived body displacement in the surrounding world. The sensorimotor adaptation adapted the matching between vestibular input and the arm motor output necessary to keep the hand fixed in space during body rotation. Only the sensorimotor adaptation significantly altered the vestibular control of arm-reaching movements. Our results therefore suggest that during passive self-motion, the vestibular control of arm-reaching movements essentially derives from a sensorimotor process by which arm motor output is modified on-line to preserve hand trajectory in space despite body displacement. In contrast, the updating process maintaining up-to-date the egocentric representation of visual space seems to contribute little to generating the required arm compensation during body rotations.

[1]  F. A. Miles,et al.  Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey. , 1974, Brain research.

[2]  N Lavie,et al.  Attentional demands of perception of passive self-motion in darkness , 1999, Neuropsychologia.

[3]  A Berthoz,et al.  Spatial memory and path integration studied by self-driven passive linear displacement. I. Basic properties. , 1997, Journal of neurophysiology.

[4]  J. Vercher,et al.  Target and hand position information in the online control of goal-directed arm movements , 2003, Experimental Brain Research.

[5]  H. Deubel,et al.  Current Oculomotor Research , 1999, Springer US.

[6]  Michelle Fleury,et al.  Visual stability with goal-directed eye and arm movements toward a target displaced during saccadic suppression , 1995, Psychological research.

[7]  M. Goodale,et al.  Visual control of reaching movements without vision of the limb , 2004, Experimental Brain Research.

[8]  T. Mergner,et al.  Updating the Location of Visual Objects in Space Following Vestibular Stimulation , 1999 .

[9]  P. Huttenlocher Neurological Anatomy in Relation to Clinical Medicine , 1970, The Yale Journal of Biology and Medicine.

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

[11]  A. Berthoz,et al.  Spatial orientation in humans: perception of angular whole-body displacements in two-dimensional trajectories , 1997, Experimental Brain Research.

[12]  J. Soechting,et al.  Modification of trajectory of a pointing movement in response to a change in target location. , 1983, Journal of neurophysiology.

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

[14]  Peter Dixon,et al.  Motor adaptation to an optical illusion , 2001, Experimental Brain Research.

[15]  Jefferson E. Roy,et al.  Vestibuloocular reflex signal modulation during voluntary and passive head movements. , 2002, Journal of neurophysiology.

[16]  Dora E Angelaki,et al.  Eyes on target: what neurons must do for the vestibuloocular reflex during linear motion. , 2004, Journal of neurophysiology.

[17]  G. Jones,et al.  Adaptive plasticity in the gaze stabilizing synergy of slow and saccadic eye movements , 2004, Experimental Brain Research.

[18]  A. Berthoz,et al.  Linear head displacement measured by the otoliths can be reproduced through the saccadic system , 1987, Neuroscience Letters.

[19]  F. Horak,et al.  Vestibular stimulation affects medium latency postural muscle responses , 2002, Experimental Brain Research.

[20]  Pascale Pigeon,et al.  Compensatory arm–trunk coordination in pointing movements is preserved in the absence of visual feedback , 1998, Brain Research.

[21]  F E Guedry,et al.  Use of triangular waveforms of angular velocity in the study of vestibulbar function. , 1971, Acta oto-laryngologica.

[22]  C. Prablanc,et al.  Automatic control during hand reaching at undetected two-dimensional target displacements. , 1992, Journal of neurophysiology.

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

[24]  B. Segal,et al.  Adaptive modification of vestibularly perceived rotation , 2004, Experimental Brain Research.

[25]  D. Robinson,et al.  Adaptation of the human vestibuloocular reflex to magnifying lenses , 1975, Brain Research.

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

[27]  Peter Dixon,et al.  Dynamic effects of the Ebbinghaus illusion in grasping: Support for a planning/control model of action , 2002, Perception & psychophysics.

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

[29]  P. Dixon,et al.  Dynamic illusion effects in a reaching task: evidence for separate visual representations in the planning and control of reaching. , 2001, Journal of experimental psychology. Human perception and performance.

[30]  Ian P. Howard,et al.  Human visual orientation , 1982 .

[31]  D. Pélisson,et al.  From Eye to Hand: Planning Goal-directed Movements , 1998, Neuroscience & Biobehavioral Reviews.

[32]  Christophe Bourdin,et al.  Vestibular signals contribute to the online control of goal-directed arm movements , 2002 .

[33]  B. Peterson,et al.  Properties of projections from vestibular nuclei to medial reticular formation in the cat. , 1975, Journal of neurophysiology.

[34]  M. Goodale,et al.  Visual control of reaching movements without vision of the limb , 1986, Experimental Brain Research.

[35]  Theodore Raphan,et al.  The vestibulo-ocular reflex in three dimensions , 2002, Experimental Brain Research.

[36]  A. Berthoz,et al.  Self-motion perception during a sequence of whole-body rotations in darkness , 2000, Experimental Brain Research.

[37]  A. Brodal,et al.  Experimental studies of commissural and reticular formation projections from the vestibular nuclei in the cat. , 1968, Brain research.

[38]  B. Day,et al.  Human body‐segment tilts induced by galvanic stimulation: a vestibularly driven balance protection mechanism. , 1997, The Journal of physiology.

[39]  Scott T. Grafton,et al.  Functional Anatomy of Nonvisual Feedback Loops during Reaching: A Positron Emission Tomography Study , 2001, The Journal of Neuroscience.

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