Ocular versus extraocular control of posture and equilibrium

Vision has been shown for almost a century to be heavily involved in postural control. However, the mechanism by which it operates is still an open debate. The purpose of this manuscript is to review the evidence supporting the view that there are two modes of visual detection of body sway: ocular and extraocular. The former is based on the characteristics of the visual flow (retinal slip), the second one is based on either the copy of the motor command (efference copy) or the extraocular muscle afferents (re-afferences) consecutive to eye movements. Results from the literature indicate that these two modes of visual detection of body sway are effective and can operate congruently. For sufficiently large body sway with respect to eye-target distance, the ocular and the extraocular perception systems could provide two sources of visual information about body displacements. However, the afferent system might remain the only one used for small lateral body sway.

[1]  C. R. Fox Some visual influences on human postural equilibrium: Binocular versus monocular fixation , 1990, Perception & psychophysics.

[2]  M S Redfern,et al.  Postural sway of patients with vestibular disorders during optic flow. , 1994, Journal of vestibular research : equilibrium & orientation.

[3]  R. Leigh,et al.  Oscillopsia, retinal image stabilization and congenital nystagmus. , 1988, Investigative ophthalmology & visual science.

[4]  R. Leigh,et al.  Oscillopsia suppression and foveation-period variation in congenital, latent, and acquired nystagmus , 1997 .

[5]  W Paulus,et al.  Multisensory versus monosensory stabilization of posture. , 1988, Agressologie: revue internationale de physio-biologie et de pharmacologie appliquees aux effets de l'agression.

[6]  C. Gielen,et al.  Postural responses to simulated moving environments are not invariant for the direction of gaze , 2004, Experimental Brain Research.

[7]  T. Brandt,et al.  Visual postural performance after loss of somatosensory and vestibular function. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[8]  T A Stoffregen,et al.  The role of optical velocity in the control of stance , 1986, Perception & psychophysics.

[9]  M. Flückiger,et al.  The Perception of an Optical Flow Projected on the Ground Surface , 1988, Perception.

[10]  F H Previc,et al.  The effects of dynamic visual stimulation on perception and motor control. , 1992, Journal of vestibular research : equilibrium & orientation.

[11]  T. Stoffregen Flow structure versus retinal location in the optical control of stance. , 1985, Journal of experimental psychology. Human perception and performance.

[12]  T. Brandt,et al.  Differential effects of retinal target displacement, changing size and changing disparity in the control of anterior/posterior and lateral body sway , 2004, Experimental Brain Research.

[13]  A M Bronstein,et al.  Visual control of postural orientation and equilibrium in congenital nystagmus. , 2000, Investigative ophthalmology & visual science.

[14]  A. Bronstein,et al.  Suppression of visually evoked postural responses , 2004, Experimental Brain Research.

[15]  Ma Gresty,et al.  Vestibular and Visual Control on Posture and Locomotor Equilibrium , 1986 .

[16]  T. Brandt,et al.  Postural sway during retinal image stabilisation. , 1989, Journal of neurology, neurosurgery, and psychiatry.

[17]  D J Lanska,et al.  Romberg’s sign , 2000, Neurology.

[18]  G. Bruyn Posture and gait: Development, adaptation and modulation By Bernard Amblard, Alain Berthoz and François Clarac (eds.), Excerpta Medica, Amsterdam-New York-Oxford, 1988, ICS 812, Dfl. 265.00 , 1989, Journal of the Neurological Sciences.

[19]  T. Brandt,et al.  Dependence of visual stabilization of postural sway on the cortical magnification factor of restricted visual fields , 2004, Experimental Brain Research.

[20]  A. Delorme,et al.  Roles of retinal periphery and depth periphery in linear vection and visual control of standing in humans. , 1986, Canadian journal of psychology.

[21]  G J Andersen,et al.  Spatial orientation from optic flow in the central visual field , 1989, Perception & psychophysics.

[22]  H E Rockette,et al.  Normal subject postural sway during the Romberg test. , 1982, American journal of otolaryngology.

[23]  M. Gresty,et al.  The differential diagnosis of congenital nystagmus. , 1984, Journal of neurology, neurosurgery, and psychiatry.

[24]  J. F. Soechting,et al.  The role of vision in the control of posture during linear motion. , 1979, Progress in brain research.

[25]  R. C. Travis An experimental analysis of dynamic and static equilibrium , 1945 .

[26]  A M Bronstein,et al.  Effect of visual surrounding motion on body sway in a three-dimensional environment , 2001, Perception & psychophysics.

[27]  A M Bronstein,et al.  Visual-vestibular control of posture and gait: physiological mechanisms and disorders. , 1999, Current opinion in neurology.

[28]  T. Raphan,et al.  VELOCITY STORAGE, NYSTAGMUS, AND VISUAL‐VESTIBULAR INTERACTIONS IN HUMANS * , 1981, Annals of the New York Academy of Sciences.

[29]  M. Guerraz,et al.  Influence of motion parallax in the control of spontaneous body sway , 2000, Experimental Brain Research.

[30]  Richard V Abadi,et al.  Oscillopsia and tolerance to retinal image movement in congenital nystagmus. , 1999, Investigative ophthalmology & visual science.

[31]  David N. Lee Visual proprioceptive control of stance , 1975 .

[32]  A. Bronstein,et al.  Vection increases the magnitude and accuracy of visually evoked postural responses , 2002, Experimental Brain Research.

[33]  J Dickinson A note on the role of peripheral vision in static balancing. , 1969, Ergonomics.

[34]  F. Owen Black,et al.  Postural Control in Four Classes of Vestibular Abnormalities1 , 1985 .

[35]  J. Crémieux,et al.  Lateral orientation and stabilization of human stance: static versus dynamic visual cues , 2004, Experimental Brain Research.

[36]  R. B. Post Circular Vection is Independent of Stimulus Eccentricity , 1988, Perception.

[37]  C C Gielen,et al.  Postural movements induced by rotations of visual scenes. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[38]  Martin A. Giese,et al.  Identification of the nonlinear state-space dynamics of the action-perception cycle for visually induced postural sway , 1996, Biological Cybernetics.

[39]  A. Bronstein,et al.  Reorientation of visually evoked postural responses by different eye-in-orbit and head-on-trunk angular positions , 1996, Experimental Brain Research.

[40]  R. Held,et al.  Moving Visual Scenes Influence the Apparent Direction of Gravity , 1972, Science.

[41]  C. C. A. M. Gielen,et al.  Postural adjustments induced by simulated motion of differently structured environments , 2004, Experimental Brain Research.

[42]  A. Straube,et al.  Visually induced motion perception and visual control of postural sway in congenital nystagmus , 1997, Behavioural Brain Research.

[43]  K H Mauritz,et al.  Postural sway in normals and atactic patients: analysis of the stabilising and destabilizing effects of vision. , 1976, Agressologie: revue internationale de physio-biologie et de pharmacologie appliquees aux effets de l'agression.

[44]  T. Brandt,et al.  Disorders of posture and gait. , 1990, Journal of vestibular research : equilibrium & orientation.

[45]  Johannes Dichgans,et al.  Characteristics of moving visual scenes influencing spatial orientation , 1975, Vision Research.

[46]  J. F. Soechting,et al.  Postural readjustments induced by linear motion of visual scenes , 1977, Experimental Brain Research.

[47]  A. Bronstein,et al.  Automatic control of postural sway by visual motion parallax , 1997, Experimental Brain Research.

[48]  Stefan Glasauer,et al.  Suppression of eye movements improves balance. , 2002, Brain : a journal of neurology.

[49]  Chris A. Johnson,et al.  Effects of reference lines on displacement thresholds at various durations of movement , 1982, Vision Research.

[50]  R. Peterka,et al.  Role of somatosensory and vestibular cues in attenuating visually induced human postural sway , 2004, Experimental Brain Research.

[51]  A Straube,et al.  Visual stabilization of posture. Physiological stimulus characteristics and clinical aspects. , 1984, Brain : a journal of neurology.

[52]  T. Brandt,et al.  How the eyes move the body , 2005, Neurology.

[53]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[54]  W Bles,et al.  The mechanism of physiological height vertigo. I. Theoretical approach and psychophysics. , 1980, Acta oto-laryngologica.

[55]  A. Berthoz,et al.  Perception of linear horizontal self-motion induced by peripheral vision (linearvection) basic characteristics and visual-vestibular interactions , 1975, Experimental Brain Research.

[56]  J. Dichgans,et al.  Differential effects of central versus peripheral vision on egocentric and exocentric motion perception , 1973, Experimental Brain Research.

[57]  R. C. Emerson,et al.  Paralysis of the awake human: Visual perceptions , 1976, Vision Research.

[58]  Louis F. Dell'Osso,et al.  Foveation period stability and oscillopsia suppression in congenital nystagmus: An hypothesis , 1992 .

[59]  A. Bronstein,et al.  Influence of action and expectation on visual control of posture. , 2001, Brain research. Cognitive brain research.

[60]  J. Gibson,et al.  Parallax and perspective during aircraft landings. , 1955, The American journal of psychology.

[61]  C. C. A. M. Gielen,et al.  Postural responses to stationary and moving scenes as a function of distance to the scene , 1992 .

[62]  J. Dichgans,et al.  Visual-Vestibular Interaction: Effects on Self-Motion Perception and Postural Control , 1978 .

[63]  R. Snowden Sensitivity to Relative and Absolute Motion , 1992, Perception.

[64]  P. Rougier,et al.  Performing saccadic eye movements or blinking improves postural control. , 2007, Motor control.

[65]  Hiroyasu Ujike,et al.  Effects of visually simulated roll motion on vection and postural stabilization , 2007, Journal of NeuroEngineering and Rehabilitation.

[66]  B. Day,et al.  Effect of vision and stance width on human body motion when standing: implications for afferent control of lateral sway. , 1993, The Journal of physiology.

[67]  Michel Guerraz,et al.  Mechanisms underlying visually induced body sway , 2008, Neuroscience Letters.

[68]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[69]  C. Gielen,et al.  Temporal stability of the action-perception cycle for postural control in a moving visual environment , 2004, Experimental Brain Research.

[70]  J. D. Hood,et al.  Visual control of balance in cerebellar and parkinsonian syndromes. , 1990, Brain : a journal of neurology.

[71]  C. Weir,et al.  Spatial localisation: does extraocular muscle proprioception play a role? , 2000, Graefe's Archive for Clinical and Experimental Ophthalmology.

[72]  A. Bronstein,et al.  Visual vertigo: symptom assessment, spatial orientation and postural control. , 2001, Brain : a journal of neurology.

[73]  M. Braunstein,et al.  Induced self-motion in central vision. , 1985, Journal of experimental psychology. Human perception and performance.

[74]  Contribution of Central and Peripheral Vision to the Regulation of Stance: Developmental Aspects. , 1998 .

[75]  J. Pailhous,et al.  Effects of the spatio-temporal structure of optical flow on postural readjustments in man , 2004, Experimental Brain Research.

[76]  W Bles,et al.  The mechanism of physiological height vertigo. II. Posturography. , 1980, Acta oto-laryngologica.

[77]  H W Leibowitz,et al.  Saccadic eye movements and body sway. , 1980, Science.

[78]  A. Berthoz,et al.  Habituation of Postural Readjustments Induced by Motion of Visual Scenes , 1985 .

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

[80]  B. Steinhoff,et al.  Spatial-frequency-related efficacy of visual stabilisation of posture , 1998, Experimental Brain Research.

[81]  B. Amblard,et al.  Role of Foveal and Peripheral Visual Information in Maintenance of Postural Equilibrium in Man , 1980, Perceptual and motor skills.