Roll-dependent modulation of the subjective visual vertical: contributions of head- and trunk-based signals.

Precision and accuracy of the subjective visual vertical (SVV) modulate in the roll plane. At large roll angles, systematic SVV errors are biased toward the subject's body-longitudinal axis and SVV precision is decreased. To explain this, SVV models typically implement a bias signal, or a prior, in a head-fixed reference frame and assume the sensory input to be optimally tuned along the head-longitudinal axis. We tested the pattern of SVV adjustments both in terms of accuracy and precision in experiments in which the head and the trunk reference frames were not aligned. Twelve subjects were placed on a turntable with the head rolled about 28 degrees counterclockwise relative to the trunk by lateral tilt of the neck to dissociate the orientation of head- and trunk-fixed sensors relative to gravity. Subjects were brought to various positions (roll of head- or trunk-longitudinal axis relative to gravity: 0 degrees , +/-75 degrees ) and aligned an arrow with perceived vertical. Both accuracy and precision of the SVV were significantly (P < 0.05) better when the head-longitudinal axis was aligned with gravity. Comparing absolute SVV errors for clockwise and counterclockwise roll tilts, statistical analysis yielded no significant differences (P > 0.05) when referenced relative to head upright, but differed significantly (P < 0.001) when referenced relative to trunk upright. These findings indicate that the bias signal, which drives the SVV toward the subject's body-longitudinal axis, operates in a head-fixed reference frame. Further analysis of SVV precision supports the hypothesis that head-based graviceptive signals provide the predominant input for internal estimates of visual vertical.

[1]  S. Lechner-Steinleitner,et al.  Interaction of labyrinthine and somatoreceptor inputs as determinants of the subjective vertical , 1978, Psychological research.

[2]  A. Graybiel,et al.  Visual horizontal-perception in relation to otolith-function. , 1968, The American journal of psychology.

[3]  Jean Laurens,et al.  Bayesian processing of vestibular information , 2007, Biological Cybernetics.

[4]  J. V. Van Gisbergen,et al.  Properties of the internal representation of gravity inferred from spatial-direction and body-tilt estimates. , 2000, Journal of neurophysiology.

[5]  W. Bialek,et al.  A sensory source for motor variation , 2005, Nature.

[6]  Wei Ji Ma,et al.  Bayesian inference with probabilistic population codes , 2006, Nature Neuroscience.

[7]  B. Efron Bootstrap Methods: Another Look at the Jackknife , 1979 .

[8]  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.

[9]  C. Bockisch,et al.  Head roll dependent variability of subjective visual vertical and ocular counterroll , 2009, Experimental Brain Research.

[10]  M. Aickin,et al.  Adjusting for multiple testing when reporting research results: the Bonferroni vs Holm methods. , 1996, American journal of public health.

[11]  L. Yardley Contribution of somatosensory information to perception of the visual vertical with body tilt and rotating visual field , 1990, Perception & psychophysics.

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

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

[14]  Yoshiharu Sakata,et al.  The Vestibular Cortex , 2002 .

[15]  Per-Anders Fransson,et al.  Idiosyncratic compensation of the subjective visual horizontal and vertical in 60 patients after unilateral vestibular deafferentation , 2004, Acta oto-laryngologica.

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

[17]  D. Knill,et al.  The Bayesian brain: the role of uncertainty in neural coding and computation , 2004, Trends in Neurosciences.

[18]  Bernhard J. M. Hess,et al.  Influence of dynamic tilts on the perception of earth-vertical , 2003, Experimental Brain Research.

[19]  N. Wade Effect of Prolonged Tilt on Visual Orientation , 1970, The Quarterly journal of experimental psychology.

[20]  David Hinkley,et al.  Bootstrap Methods: Another Look at the Jackknife , 2008 .

[21]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[22]  N. Wade Visual orientation during and after lateral head, body, and trunk tilt , 1968 .

[23]  H Bekkering,et al.  Influence of visual, vestibular, cervical, and somatosensory tilt information on ocular rotation and perception of the horizontal. , 1992, Journal of vestibular research : equilibrium & orientation.

[24]  G. Friedmann The judgement of the visual vertical and horizontal with peripheral and central vestibular lesions. , 1970, Brain : a journal of neurology.

[25]  H Shimazu,et al.  Tonic and kinetic responses of cat's vestibular neurons to horizontal angular acceleration. , 1965, Journal of neurophysiology.

[26]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[27]  J Dichgans,et al.  Optokinetic-graviceptive interaction in different head positions. , 1974, Acta oto-laryngologica.

[28]  Konrad Paul Kording,et al.  Bayesian integration in sensorimotor learning , 2004, Nature.

[29]  D Straumann,et al.  Gravity dependence of subjective visual vertical variability. , 2009, Journal of neurophysiology.

[30]  R S Kennedy,et al.  The effect of water immersion on perception of the oculogravic illusion in normal and labyrinthine-defective subjects. , 1968, Acta oto-laryngologica.

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

[32]  M. Guerraz,et al.  Head Orientation Involvement in Assessment of the Subjective Vertical during Whole Body Tilt , 1998, Perceptual and motor skills.

[33]  Jan A M Van Gisbergen,et al.  Interpretation of a discontinuity in the sense of verticality at large body tilt. , 2004, Journal of neurophysiology.

[34]  U Rosenhall,et al.  Vestibular Macular Mapping in Man , 1972, The Annals of otology, rhinology, and laryngology.

[35]  S G Diamond,et al.  Binocular Counterrolling during Sustained Body Tilt in Normal Humans and in a Patient with Unilateral Vestibular Nerve Section , 1982, The Annals of otology, rhinology, and laryngology.

[36]  M. De Vrijer,et al.  Accuracy-precision trade-off in visual orientation constancy. , 2009, Journal of vision.

[37]  A M Bronstein,et al.  The perception of body verticality (subjective postural vertical) in peripheral and central vestibular disorders. , 1996, Brain : a journal of neurology.

[38]  H. Mittelstaedt,et al.  Somatic graviception , 1996, Biological Psychology.

[39]  A. Bronstein,et al.  Visually and posturally mediated tilt illusion in Parkinson's disease and in labyrinthine defective subjects , 1996, Neurology.

[40]  H Mittelstaedt,et al.  Somatic versus Vestibular Gravity Reception in Man , 1992, Annals of the New York Academy of Sciences.

[41]  T Haslwanter,et al.  The Role of Somatosensory Input for the Perception of Verticality , 1999, Annals of the New York Academy of Sciences.

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

[43]  H. Haes,et al.  Perception of gravity-vertical as a function of head and trunk position , 1968, Zeitschrift für Vergleichende Physiologie.

[44]  Marousa Pavlou,et al.  Effect of semicircular canal stimulation on the perception of the visual vertical. , 2003, Journal of neurophysiology.

[45]  T. Brandt,et al.  The Vestibular Cortex: Its Locations, Functions, and Disorders , 1999, Annals of the New York Academy of Sciences.

[46]  Jan A M Van Gisbergen,et al.  Nature of the transition between two modes of external space perception in tilted subjects. , 2005, Journal of neurophysiology.

[47]  G. DeAngelis,et al.  Multisensory integration: psychophysics, neurophysiology, and computation , 2009, Current Opinion in Neurobiology.

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

[49]  W P Medendorp,et al.  Shared computational mechanism for tilt compensation accounts for biased verticality percepts in motion and pattern vision. , 2008, Journal of neurophysiology.

[50]  A M Bronstein,et al.  The Interaction of Otolith and Proprioceptive Information in the Perception of Verticality: The Effects of Labyrinthine and CNS Disease , 1999, Annals of the New York Academy of Sciences.

[51]  Dora E Angelaki,et al.  Coordinate transformations and sensory integration in the detection of spatial orientation and self-motion: from models to experiments. , 2007, Progress in brain research.

[52]  Heinrich H. Bülthoff,et al.  A Bayesian model of the disambiguation of gravitoinertial force by visual cues , 2007, Experimental Brain Research.