Human ocular torsion and perceived roll responses to linear acceleration.

We investigated if human ocular torsion (OT) and perceived roll (PR) are elicited in response to either dynamic interaural linear acceleration or dynamic roll tilt of the gravito-inertial force (GIF). We expanded a previous study [26] that measured only OT across a limited frequency-range (from 0.35 Hz to 1 Hz) by simultaneously measuring OT and PR at three very low (0.01, 0.02 and 0.05 Hz) and one high (1 Hz) frequencies. Three experimental conditions were investigated: (1) Y-Upright with acceleration along the interaural (Y) axis while upright, (2) Y-Supine with acceleration along the Y-axis while supine, and (3) Z-RED with acceleration along the rostro-caudal Z) axis with right-ear-down (RED). OT was measured by video-oculography, while PR was measured by use of a somatosensory bar. OT and PR were qualitatively different. Large OT responses were measured for Y-Upright and Y-Supine, while large perceived roll responses were observed for Y-Upright and Z-RED. OT for Z-RED was small, and PR for Y-Supine was absent. In conclusion, OT and PR appear governed by qualitatively different neural mechanisms. OT appears mostly influenced by central low-pass filtering of interaural graviceptor cues, while PR appears mostly influenced by roll tilt of the GIF.

[1]  I. Curthoys,et al.  Visually perceived vertical and visually perceived horizontal are not orthogonal , 1998, Vision Research.

[2]  I. Curthoys,et al.  The Effect of Ocular Torsional Position on Perception of the Roll-tilt of Visual Stimuli , 1997, Vision Research.

[3]  Dora E Angelaki,et al.  An integrative neural network for detecting inertial motion and head orientation. , 2004, Journal of neurophysiology.

[4]  S Glasauer Interaction of Semicircular Canals and Otoliths in the Processing Structure of the Subjective Zenith , 1992, Annals of the New York Academy of Sciences.

[5]  G. Paige,et al.  Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. , 1991, Journal of neurophysiology.

[6]  E. Edelman,et al.  OCULAR TORSION ON EARTH AND IN WEIGHTLESSNESS * , 1981, Annals of the New York Academy of Sciences.

[7]  B J Hess,et al.  Computation of Inertial Motion: Neural Strategies to Resolve Ambiguous Otolith Information , 1999, The Journal of Neuroscience.

[8]  L. Zupan,et al.  Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. , 2002, Journal of neurophysiology.

[9]  U. Bucher,et al.  An analysis of ocular counterrolling in response to body positions in three-dimensional space. , 1992, Journal of vestibular research : equilibrium & orientation.

[10]  L. Zupan,et al.  Neural processing of gravito-inertial cues in humans. II. Influence of the semicircular canals during eccentric rotation. , 2001, Journal of neurophysiology.

[11]  R. S. Kellogg Dynamic counterrolling of the eye in normal subjects and in persons with bilateral labyrinthine defects , 1965 .

[12]  C. Markham Anatomy and physiology of otolith-controlled ocular counterrolling , 1989 .

[13]  L. Young,et al.  Human ocular counterrolling induced by varying linear accelerations , 2004, Experimental Brain Research.

[14]  J. Holly Three-dimensional baselines for perceived self-motion during acceleration and deceleration in a centrifuge. , 1997, Journal of vestibular research : equilibrium & orientation.

[15]  Alan Cowey,et al.  Plasticity revealed by transcranial magnetic stimulation of early visual cortex , 2000, Neuroreport.

[16]  I. Howard,et al.  Visually-induced eye torsion and tilt adaptation. , 1964, Vision research.

[17]  H. Mittelstaedt A new solution to the problem of the subjective vertical , 1983, Naturwissenschaften.

[18]  Hermann Aubert,et al.  Eine scheinbare bedeutende Drehung von Objecten bei Neigung des Kopfes nach rechts oder links , 1861, Archiv für pathologische Anatomie und Physiologie und für klinische Medicin.

[19]  D M Merfeld,et al.  Modeling human vestibular responses during eccentric rotation and off vertical axis rotation. , 1995, Acta oto-laryngologica. Supplementum.

[20]  Ashton Graybiel,et al.  Counterrolling of the eyes and its dependence on the magnitude of gravitational or inertial force acting laterally on the body , 1959 .

[21]  S Glasauer,et al.  Linear acceleration perception: frequency dependence of the hilltop illusion. , 1995, Acta oto-laryngologica. Supplementum.

[22]  Michael Barnett-Cowan,et al.  Is an Internal Model of Head Orientation Necessary for Oculomotor Control? , 2005, Annals of the New York Academy of Sciences.

[23]  S. H. Seidman,et al.  Tilt perception during dynamic linear acceleration , 1998, Experimental Brain Research.

[24]  K Tokumasu,et al.  Eye movements from single utricular nerve stimulation in the cat. , 1969, Acta oto-laryngologica.

[25]  Richard A. Johnson,et al.  Applied Multivariate Statistical Analysis , 1983 .

[26]  B Cohen,et al.  Contribution of vestibular commissural pathways to spatial orientation of the angular vestibuloocular reflex. , 1997, Journal of neurophysiology.

[27]  Dora E Angelaki,et al.  Resolution of Sensory Ambiguities for Gaze Stabilization Requires a Second Neural Integrator , 2003, The Journal of Neuroscience.

[28]  A. D. Van Beuzekom,et al.  Properties of the internal representation of gravity inferred from spatial-direction and body-tilt estimates. , 2000 .

[29]  A. Clarke,et al.  Ocular counterrolling in response to asymmetric radial acceleration. , 1996, Acta oto-laryngologica.

[30]  Laurence R. Young,et al.  The dynamic contributions of the otolith organs to human ocular torsion , 1996, Experimental Brain Research.

[31]  P. Caines Linear Stochastic Systems , 1988 .

[32]  M. S. Estes,et al.  Vestibular influences on ocular accommodation in cats. , 1973, International journal of equilibrium research.

[33]  C. Markham,et al.  Ocular counterrolling as an indicator of vestibular otolith function , 1983, Neurology.

[34]  J. Goldberg,et al.  Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. , 1976, Journal of neurophysiology.

[35]  H. Collewijn,et al.  Human ocular counterroll: assessment of static and dynamic properties from electromagnetic scleral coil recordings , 2004, Experimental Brain Research.

[36]  Dora E. Angelaki,et al.  Neurons compute internal models of the physical laws of motion , 2004, Nature.

[37]  Christian Darlot,et al.  Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements , 2002, Biological Cybernetics.

[38]  D E Angelaki,et al.  Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses To translation. , 1998, Journal of neurophysiology.

[39]  G D Paige,et al.  Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance. , 1997, Journal of neurophysiology.