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01-07-2010 | Research Article

Human discrimination of rotational velocities

Authors: Robert M. Mallery, Osarenoma U. Olomu, Rosalie M. Uchanski, Valentin A. Militchin, Timothy E. Hullar

Published in: Experimental Brain Research | Issue 1/2010

Abstract

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 = 0.88I ^0.37, 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.

Au Yong N, Paige GD, Seidman SH (2007) Multiple sensory cues underlying the perception of translation and path. J Neurophysiol 97:1100–1113CrossRefPubMed

Baird JC (1997) Sensation and judgment. Lawrence Erlbaum Associates, Mahwah, NJ

Baird RA, Desmadryl G, Fernandez C, Goldberg JM (1988) The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60:182–203PubMed

Benson AJ (1982) The vestibular sensory system. In: Barlow HB, Mollon JD (eds) The senses. Cambridge University Press, Cambridge, pp 333–368

Benson AJ, Brown SF (1992) Perception of liminal and supraliminal whole-body angular motion. In: Berthoz A, Graf W, Vidal PP (eds) The head-neck sensory motor system. Oxford University Press, New York, pp 483–487

Benson AJ, Spencer MB, Stott JR (1986) Thresholds for the detection of the direction of whole-body, linear movement in the horizontal plane. Aviat Space Environ Med 57:1088–1096PubMed

Benson AJ, Hutt EC, Brown SF (1989) Thresholds for the perception of whole body angular movement about a vertical axis. Aviat Space Environ Med 60:205–213PubMed

Brannon EM, Libertus ME, Meck WH, Woldorff MG (2008) Electrophysiological measures of time processing in infant and adult brains: Weber’s Law holds. J Cogn Neurosci 20:193–203CrossRefPubMed

Brown JH (1966) Magnitude estimation of angular velocity during passive rotation. J Exp Psychol 72:169–172CrossRefPubMed

Clement G, Tilikete C, Courjon JH (2008) Retention of habituation of vestibulo-ocular reflex and sensation of rotation in humans. Exp Brain Res 190:307–315CrossRefPubMed

Dai M, Klein A, Cohen B, Raphan T (1999) Model-based study of the human cupular time constant. J Vestib Res 9:293–301PubMed

Day BL, Fitzpatrick RC (2005) The vestibular system. Curr Biol 15:R583–R586CrossRefPubMed

Dehaene S (2003) The neural basis of the Weber-Fechner law: a logarithmic mental number line. Trends Cogn Sci 7:145–147CrossRefPubMed

Della Santina CC, Potyagaylo V, Migliaccio AA, Minor LB, Carey JP (2005) Orientation of human semicircular canals measured by three-dimensional multiplanar CT reconstruction. J Assoc Res Otolaryngol 6:1–16CrossRef

Fechner G (1860) Elemente der Psychophysik. Breitkopf & Härtel, Leipzig

Fernandez C, Goldberg JM (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophys 34:661–675

Francisco E, Tannan V, Zhang Z, Holden J, Tommerdahl M (2008) Vibrotactile amplitude discrimination capacity parallels magnitude changes in somatosensory cortex and follows Weber’s Law. Exp Brain Res 191:49–56CrossRefPubMed

Friedmann G (1970) The judgement of the visual vertical and horizontal with peripheral and central vestibular lesions. Brain 93:313–328CrossRefPubMed

Gescheider GA, Bolanowski SJ Jr, Verrillo RT, Arpajian DJ, Ryan TF (1990) Vibrotactile intensity discrimination measured by three methods. J Acoust Soc Am 87:330–338CrossRefPubMed

Gianna C, Heimbrand S, Gresty M (1996) Thresholds for detection of motion direction during passive lateral whole-body acceleration in normal subjects and patients with bilateral loss of labyrinthine function. Brain Res Bull 40:443–449CrossRefPubMed

Glasauer S, Amorim MA, Viaud-Delmon I, Berthoz A (2002) Differential effects of labyrinthine dysfunction on distance and direction during blindfolded walking of a triangular path. Exp Brain Res 145:489–497CrossRefPubMed

Golding JF, Benson AJ (1993) Perceptual scaling of whole-body low frequency linear oscillatory motion. Aviat Space Environ Med 64:636–640PubMed

Grabherr L, Nicoucar K, Mast FW, Merfeld DM (2008) Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency. Exp Brain Res 186:677–681CrossRefPubMed

Green DM, Swets JA (1966) Signal detection theory and psychophysics. Wiley, NY

Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476CrossRefPubMed

Guedry FEJ (1974) Psychophysics of vestibular sensation. In: Kornhuber HH (ed) Handbook of sensory physiology vestibular system. Springer, New York, pp 3–154

Guilford JP (1932) A generalized psychophysical law. Psychol Rev 39:73–85CrossRef

Hullar T (2008) Neurometric and psychometric thresholds of the semicircular canals. Soc Neurosci Abs 168:8

Hullar T, Zee D, Minor L (2005a) Evaluation of the patient with dizziness. In: Cummings C (ed) Otolaryngology—head and neck surgery. Elsevier, Philadelphia

Hullar TE, Della Santina CC, Hirvonen TP, Lasker DM, Carey JP, Minor LB (2005b) Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93:2777–2786CrossRefPubMed

Kiesow E (1926) Über die Vergleichung linearer Strecken und ihre Beziehung zum Weberschen Gesetze. Arch Gesamte Psychol 56:421–462

Kingma H (2005) Thresholds for perception of direction of linear acceleration as a possible evaluation of the otolith function. BMC Ear Nose Throat Disord 5:5CrossRefPubMed

Laming D (1986) Weber’s law. In: Sensory analysis. Academic Press, London, pp 1–17

Leek MR (2001) Adaptive procedures in psychophysical research. Percept Psychophys 63:1279–1292PubMed

Leek MR, Dubno JR, He N, Ahlstrom JB (2000) Experience with a yes–no single-interval maximum-likelihood procedure. J Acoust Soc Am 107:2674–2684CrossRefPubMed

Leigh R, Zee D (2006) The neurology of eye movements. Oxford University Press, New York

MacDougall HG, Moore ST (2005) Marching to the beat of the same drummer: the spontaneous tempo of human locomotion. J Appl Physiol 99:1164–1173CrossRefPubMed

Mach E (1875) Grundlinien der Lehre von den Bewegungsempfindungen. Engelman, Leipzig

Macmillan NA, Creelman CD (2005) Detection theory: a user’s guide. Lawrence Erlbaum Associates, Mahwah

McGill WJ, Goldberg JP (1968) Pure-tone intensity discrimination and energy detection. J Acoust Soc Am 44:576–581CrossRefPubMed

Merfeld DM, Park S, Gianna-Poulin C, Black FO, Wood S (2005a) Vestibular perception and action employ qualitatively different mechanisms. I. Frequency response of VOR and perceptual responses during Translation and Tilt. J Neurophysiol 94:186–198CrossRefPubMed

Merfeld DM, Park S, Gianna-Poulin C, Black FO, Wood S (2005b) Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt & Translation. J Neurophysiol 94:199–205CrossRefPubMed

Mittelstaedt H (1998) Origin and processing of postural information. Neurosci Biobeh Rev 22:473–478CrossRef

Okada T, Grunfeld E, Shallo-Hoffmann J, Bronstein AM (1999) Vestibular perception of angular velocity in normal subjects and in patients with congenital nystagmus. Brain 122:1293–1303CrossRefPubMed

Pulaski PD, Zee DS, Robinson DA (1981) The behavior of the vestibulo-ocular reflex at high velocities of head rotation. Brain Res 222:159–165CrossRefPubMed

Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:229–248CrossRefPubMed

Sadeghi SG, Chacron MJ, Taylor MC, Cullen KE (2007) Neural variability, detection thresholds, and information transmission in the vestibular system. J Neurosci 27:771–781CrossRefPubMed

Seemungal BM, Gunaratne IA, Fleming IO, Gresty MA, Bronstein AM (2004) Perceptual and nystagmic thresholds of vestibular function in yaw. J Vestib Res 14:461–466PubMed

Seidman SH (2008) Translational motion perception and vestiboocular responses in the absence of non-inertial cues. Exp Brain Res 184:13–29CrossRefPubMed

Sinha N, Zaher N, Shaikh AG, Lasker AG, Zee DS, Tarnutzer AA (2008) Perception of self motion during and after passive rotation of the body around an earth-vertical axis. Prog Brain Res 171:277–281CrossRefPubMed

Stevens SS (1961) To honor Fechner and repeal his law: a power function, not a log function, describes the operating characteristic of a sensory system. Science 133:80–86CrossRefPubMed

Walsh EG (1961) Role of the vestibular apparatus in the perception of motion on a parallel swing. J Physiol (Lond) 155:506–513

Weber KP, Aw ST, Todd MJ, McGarvie LA, Curthoys IS, Halmagyi GM (2008) Head impulse test in unilateral vestibular loss: vestibulo-ocular reflex and catch-up saccades. Neurology 70:454–463CrossRefPubMed

Wichmann FA, Hill NJ (2001) The psychometric function: I. Fitting, sampling, and goodness of fit. Percept Psychophys 63:1293–1313PubMed

Wilson VJ, Jones GM (1979) Mammalian vestibular physiology. Plenum, London

Wood SJ, Reschke MF, Sarmiento LA, Clement G (2007) Tilt and translation motion perception during off-vertical axis rotation. Exp Brain Res 182:365–377CrossRefPubMed

Zanker JM (1995) Does motion perception follow Weber’s law? Perception 24:363–372CrossRefPubMed

Title: Human discrimination of rotational velocities
Authors: Robert M. Mallery
Osarenoma U. Olomu
Rosalie M. Uchanski
Valentin A. Militchin
Timothy E. Hullar
Publication date: 01-07-2010
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 1/2010
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-010-2288-1

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Human discrimination of rotational velocities

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