Time course and magnitude of illusory translation perception during off-vertical axis rotation.

Human spatial orientation relies on vision, somatosensory cues, and signals from the semicircular canals and the otoliths. The canals measure rotation, whereas the otoliths are linear accelerometers, sensitive to tilt and translation. To disambiguate the otolith signal, two main hypotheses have been proposed: frequency segregation and canal-otolith interaction. So far these models were based mainly on oculomotor behavior. In this study we investigated their applicability to human self-motion perception. Six subjects were rotated in yaw about an off-vertical axis (OVAR) at various speeds and tilt angles, in darkness. During the rotation, subjects indicated at regular intervals whether a briefly presented dot moved faster or slower than their perceived self-motion. Based on such responses, we determined the time course of the self-motion percept and characterized its steady state by a psychometric function. The psychophysical results were consistent with anecdotal reports. All subjects initially sensed rotation, but then gradually developed a percept of being translated along a cone. The rotation percept could be described by a decaying exponential with a time constant of about 20 s. Translation percept magnitude typically followed a delayed increasing exponential with delays up to 50 s and a time constant of about 15 s. The asymptotic magnitude of perceived translation increased with rotation speed and tilt angle, but never exceeded 14 cm/s. These results were most consistent with predictions of the canal-otolith-interaction model, but required parameter values that differed from the original proposal. We conclude that canal-otolith interaction is an important governing principle for self-motion perception that can be deployed flexibly, dependent on stimulus conditions.

[1]  Michael Fetter,et al.  Three-dimensional eye-movement responses to off-vertical axis rotations in humans , 2000, Experimental Brain Research.

[2]  L. Young,et al.  The vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt , 2004, Experimental Brain Research.

[3]  J R Lackner,et al.  Some influences of touch and pressure cues on human spatial orientation. , 1978, Aviation, space, and environmental medicine.

[4]  D E Angelaki,et al.  Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. I. Linear acceleration responses during off-vertical axis rotation. , 1996, Journal of neurophysiology.

[5]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[6]  Robert W. Massof,et al.  Nonlinear contribution of eye velocity to motion perception , 2001, Vision Research.

[7]  J R Lackner,et al.  Postural illusions experienced during Z-axis recumbent rotation and their dependence upon somatosensory stimulation of the body surface. , 1978, Aviation, space, and environmental medicine.

[8]  J. Droulez,et al.  Motion perceptions induced by off-vertical axis rotation (OVAR) at small angles of tilt , 2004, Experimental Brain Research.

[9]  W Pieter Medendorp,et al.  Motion Parallax Is Computed in the Updating of Human Spatial Memory , 2003, The Journal of Neuroscience.

[10]  W. Ehrenstein,et al.  Psychophysical Methods , 1999 .

[11]  R. Peterka,et al.  Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt. , 2000, Journal of neurophysiology.

[12]  S. Klein,et al.  Measuring, estimating, and understanding the psychometric function: A commentary , 2001, Perception & psychophysics.

[13]  S. Glasauer,et al.  Modelling Three-Dimensional Vestibular Responses During Complex Motion Stimulation , 1997 .

[14]  F. O. Black,et al.  Vestibular perception and action employ qualitatively different mechanisms. I. Frequency response of VOR and perceptual responses during Translation and Tilt. , 2005, Journal of neurophysiology.

[15]  B Cohen,et al.  Velocity storage and the ocular response to multidimensional vestibular stimuli. , 1985, Reviews of oculomotor research.

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

[17]  D. Merfeld Modeling the vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt , 2004, Experimental Brain Research.

[18]  Håkan Johansson,et al.  Modern Techniques in Neuroscience Research , 1999, Springer Berlin Heidelberg.

[19]  S Glasauer,et al.  How to explain a constant subjective vertical at constant high speed rotation about an earth-horizontal axis. , 1989, Acta oto-laryngologica. Supplementum.

[20]  W P Medendorp,et al.  Human gaze stabilization during active head translations. , 2002, Journal of neurophysiology.

[21]  L. Young,et al.  A multidimensional model of the effect of gravity on the spatial orientation of the monkey. , 1993, Journal of vestibular research : equilibrium & orientation.

[22]  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.

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

[24]  A. Berthoz,et al.  Estimation of passive horizontal linear whole-body displacement in humans. , 1993, Journal of neurophysiology.

[25]  Gary D. Paige,et al.  Canal-otolith interactions in the squirrel monkey vestibulo-ocular reflex and the influence of fixation distance , 1998, Experimental Brain Research.

[26]  Daniel M Merfeld,et al.  Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt&Translation. , 2005, Journal of neurophysiology.

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

[28]  F. Guedry Psychophysics of Vestibular Sensation , 1974 .

[29]  J. Droulez,et al.  Eye movements induced by off-vertical axis rotation (OVAR) at small angles of tilt , 2004, Experimental Brain Research.

[30]  T. Freeman,et al.  Transducer models of head-centred motion perception , 2001, Vision Research.

[31]  W P Medendorp,et al.  Context compensation in the vestibuloocular reflex during active head rotations. , 2000, Journal of neurophysiology.

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

[33]  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.

[34]  K J Ciuffreda,et al.  Stability of tonic vergence. , 1988, Investigative ophthalmology & visual science.

[35]  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.

[36]  D E Angelaki,et al.  Vestibular Discrimination of Gravity and Translational Acceleration , 2001, Annals of the New York Academy of Sciences.

[37]  B. Cohen,et al.  Velocity storage in the vestibulo-ocular reflex arc (VOR) , 1979, Experimental Brain Research.

[38]  Theodore Raphan,et al.  Compensatory and orienting eye movements induced by off-vertical axis rotation (OVAR) in monkeys. , 2002, Journal of neurophysiology.

[39]  Alexander H. Wertheim,et al.  The Direct versus Inferential controversy revisited , 2000 .

[40]  D E Angelaki,et al.  Inertial Processing of Vestibulo‐Ocular Signals , 1999, Annals of the New York Academy of Sciences.

[41]  Scott J. Wood,et al.  Human otolith–ocular reflexes during off-vertical axis rotation: effect of frequency on tilt–translation ambiguity and motion sickness , 2002, Neuroscience Letters.

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

[43]  D E Angelaki,et al.  Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. II. Inertial detection of angular velocity. , 1996, Journal of neurophysiology.

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

[45]  G D Paige,et al.  Characteristics of the VOR in Response to Linear Acceleration , 1999, Annals of the New York Academy of Sciences.

[46]  A M Bronstein,et al.  Vestibular perception of angular velocity in normal subjects and in patients with congenital nystagmus. , 1999, Brain : a journal of neurology.

[47]  J. Brown Magnitude estimation of angular velocity during passive rotation. , 1966, Journal of experimental psychology.

[48]  M Rocchetti,et al.  Enantioselective recognition of two anticonvulsants, FCE 26743 and FCE 28073, by MAO, and relationship between MAO-B inhibition and FCE 26743 concentrations in rat brain. , 1995, Progress in brain research.

[49]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

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

[51]  M. Sanders Handbook of Sensory Physiology , 1975 .

[52]  Michael Fetter,et al.  Three-Dimensional Kinematics of Eye, Head and Limb Movements , 1997 .

[53]  R. Mayne,et al.  A Systems Concept of the Vestibular Organs , 1974 .

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

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

[56]  Jelte E. Bos,et al.  Theoretical considerations on canal–otolith interaction and an observer model , 2002, Biological Cybernetics.

[57]  J. Furman,et al.  Off-Vertical Axis Rotation: A Test of the Otolith-Ocular Reflex , 1992, The Annals of otology, rhinology, and laryngology.

[58]  M. Taussig The Nervous System , 1991 .