Human discrimination of rotational velocities

Vestibular reflexes are critically important for stabilizing gaze and maintaining posture, but comparatively little is known about conscious perceptions of vestibular stimuli and how they may relate to balance function. We used psychophysical methods to determine the ability of normal subjects and a vestibular-deficient subject to discriminate among velocities of earth-vertical sinusoidal rotations. Discrimination thresholds in normal subjects rose from 2.26 deg/s at a peak velocity of 20 deg/s up to 5.16 deg/s at 150 deg/s. The relationship between threshold and peak angular velocity was well described by the power law function ΔI = 0.88I0.37, where I is the magnitude of the stimulus and ΔI is the discrimination threshold. The subject with bilateral vestibular hypofunction had thresholds more than an order of magnitude worse than normals. The performance of normal subjects is much better than that predicted by Weber’s Law, which states that discrimination thresholds increase proportionally with stimulus magnitude (i.e., ΔI/I = C, where C is the “Weber fraction”). This represents a remarkable exception to other sensory systems and may reflect the vestibular system’s ability to stabilize gaze and maintain posture even at high stimulus intensities. Quantifying this relationship may help elucidate the role of higher-level processes in maintaining balance and provide information to diagnose and guide therapy of patients with central causes for imbalance.

[1]  Stanislas Dehaene,et al.  The neural basis of the Weber–Fechner law: a logarithmic mental number line , 2003, Trends in Cognitive Sciences.

[2]  J F Golding,et al.  Perceptual scaling of whole-body low frequency linear oscillatory motion. , 1993, Aviation, space, and environmental medicine.

[3]  G. Paige,et al.  Multiple sensory cues underlying the perception of translation and path. , 2007, Journal of neurophysiology.

[4]  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.

[5]  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.

[6]  H Mittelstaedt,et al.  Origin and processing of postural information , 1998, Neuroscience & Biobehavioral Reviews.

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

[8]  R. Baloh,et al.  The evaluation of a patient with dizziness. , 2011, Neurology. Clinical practice.

[9]  D. Zee,et al.  Evaluation of the Patient with Dizziness , 2010 .

[10]  Lloyd B. Minor,et al.  Orientation of Human Semicircular Canals Measured by Three-Dimensional Multiplanar CT Reconstruction , 2005, Journal of the Association for Research in Otolaryngology.

[11]  V. J. Wilson,et al.  Mammalian Vestibular Physiology , 1979, Springer US.

[12]  H Kingma,et al.  Thresholds for perception of direction of linear acceleration as a possible evaluation of the otolith function , 2005, BMC ear, nose, and throat disorders.

[13]  A. J. Benson,et al.  Perception of Liminal and Supraliminal Whole-Body Angular Motion , 1992 .

[14]  A. Berthoz,et al.  Differential effects of labyrinthine dysfunction on distance and direction during blindfolded walking of a triangular path , 2002, Experimental Brain Research.

[15]  S. H. Seidman,et al.  Translational motion perception and vestiboocular responses in the absence of non-inertial cues , 2007, Experimental Brain Research.

[16]  S S Stevens,et al.  To Honor Fechner and Repeal His Law: A power function, not a log function, describes the operating characteristic of a sensory system. , 1961, Science.

[17]  B Cohen,et al.  Model-based study of the human cupular time constant. , 1999, Journal of vestibular research : equilibrium & orientation.

[18]  J. Goldberg,et al.  The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. , 1988, Journal of neurophysiology.

[19]  J. Guilford.  A generalized psychophysical law. , 1932 .

[20]  A. J. Benson,et al.  Thresholds for the detection of the direction of whole-body, linear movement in the horizontal plane. , 1986, Aviation, space, and environmental medicine.

[21]  M R Leek,et al.  Experience with a yes-no single-interval maximum-likelihood procedure. , 2000, The Journal of the Acoustical Society of America.

[22]  R. Fitzpatrick,et al.  The vestibular system , 2005, Current Biology.

[23]  Alain Berthoz,et al.  The Head-neck sensory motor system , 1992 .

[24]  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.

[25]  J. Goldberg,et al.  Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. , 1971, Journal of neurophysiology.

[26]  Benson Aj,et al.  Perceptual scaling of whole-body low frequency linear oscillatory motion. , 1993 .

[27]  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 .

[28]  E. Walsh,et al.  Role of the vestibular apparatus in the perception of motion on a parallel swing , 1961, The Journal of physiology.

[29]  T. Hirvonen,et al.  Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. , 2005, Journal of neurophysiology.

[30]  I S Curthoys,et al.  Head impulse test in unilateral vestibular loss , 2008, Neurology.

[31]  M. Reschke,et al.  Tilt and translation motion perception during off-vertical axis rotation , 2007, Experimental Brain Research.

[32]  D. Robinson,et al.  The behavior of the vestibulo-ocular reflex at high velocities of head rotation , 1981, Brain Research.

[33]  Donald Laming,et al.  Weber's Law , 2008 .

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

[35]  G. Fechner.  Elemente der Psychophysik , 1998 .

[36]  W. J. McGill,et al.  Pure-tone intensity discrimination and energy detection. , 1968, The Journal of the Acoustical Society of America.

[37]  M. Chacron,et al.  Neural Variability, Detection Thresholds, and Information Transmission in the Vestibular System , 2007, Journal of Neuroscience.

[38]  J. Goldberg,et al.  Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. 3. Variations among units in their discharge properties. , 1971, Journal of neurophysiology.

[39]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[40]  R. J. Leigh,et al.  Frequency and velocity of rotational head perturbations during locomotion , 2004, Experimental Brain Research.

[41]  Ernst Mach,et al.  Grundlinien der Lehre von den Bewegungsempfindungen , 1967 .

[42]  A M Bronstein,et al.  Perceptual and nystagmic thresholds of vestibular function in yaw. , 2004, Journal of vestibular research : equilibrium & orientation.

[43]  C. Tilikete,et al.  Retention of habituation of vestibulo-ocular reflex and sensation of rotation in humans , 2008, Experimental Brain Research.

[44]  D. Zee,et al.  Perception of self motion during and after passive rotation of the body around an earth-vertical axis. , 2008, Progress in brain research.

[45]  M. Gresty,et al.  Thresholds for detection of motion direction during passive lateral whole-body acceleration in normal subjects and patients with bilateral loss of labyrinthine function , 1996, Brain Research Bulletin.

[46]  A. J. Benson,et al.  Thresholds for the perception of whole body angular movement about a vertical axis. , 1989, Aviation, space, and environmental medicine.

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

[48]  J M Zanker,et al.  Does Motion Perception Follow Weber's Law? , 1995, Perception.

[49]  M. Leek.  Adaptive procedures in psychophysical research , 2001, Perception & psychophysics.

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

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

[52]  S. Bolanowski,et al.  Vibrotactile intensity discrimination measured by three methods. , 1990, The Journal of the Acoustical Society of America.

[53]  E. Francisco,et al.  Vibrotactile amplitude discrimination capacity parallels magnitude changes in somatosensory cortex and follows Weber’s Law , 2008, Experimental Brain Research.

[54]  Hamish G MacDougall,et al.  Marching to the beat of the same drummer: the spontaneous tempo of human locomotion. , 2005, Journal of applied physiology.

[55]  R. Leigh,et al.  The neurology of eye movements , 2006 .

[56]  Elizabeth M. Brannon,et al.  Electrophysiological Measures of Time Processing in Infant and Adult Brains: Weber's Law Holds , 2008, Journal of Cognitive Neuroscience.

[57]  D. Straumann,et al.  Head-Shaking Nystagmus Depends on Gravity , 2005, Journal of the Association for Research in Otolaryngology.

[58]  Fred W. Mast,et al.  Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency , 2008, Experimental Brain Research.