The Critical Role of Velocity Storage in Production of Motion Sickness

We propose that motion sickness is mediated through the orientation properties of velocity storage in the vestibular system that tend to align eye velocity produced by the angular vestibulo‐ocular reflex (aVOR) with gravito‐inertial acceleration (GIA). (GIA is the sum of the linear accelerations acting on the head. In the absence of translational accelerations, gravity is the GIA.) We further postulate that motion sickness produced by cross‐coupled vestibular stimulation can be characterized by a metric composed of the disparity between the axis of eye rotation and the GIA, the strength of the response to angular motion, and the response duration, as determined by the central vestibular time constant, that is, by the time constant of velocity storage. The nodulus and uvula of the vestibulocerebellum are likely to be the central sites where the disparity is sensed, where the vestibular time constants are habituated, and where links are made to the autonomic system to produce the symptoms and signs.

[1]  L R Young,et al.  Artificial gravity: head movements during short-radius centrifugation. , 2001, Acta astronautica.

[2]  B. Cohen,et al.  Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula. , 1985, Science.

[3]  W. E. Collins,et al.  REDUCTION OF NYSTAGMUS AND DISORIENTATION IN HUMAN SUBJECTS , 1962 .

[4]  C. Balaban,et al.  Background and history of the interface between anxiety and vertigo. , 2001, Journal of anxiety disorders.

[5]  B. Yates,et al.  Physiological basis and pharmacology of motion sickness: an update , 1998, Brain Research Bulletin.

[6]  I. Howard,et al.  Human Spatial Orientation , 1966 .

[7]  Theodore Raphan,et al.  The Nodulus and Uvula: Source of Cerebellar Control of Spatial Orientation of the Angular Vestibulo‐Ocular Reflex , 2002, Annals of the New York Academy of Sciences.

[8]  G. Singleton,et al.  Relationships of the cerebellar nodulus to vestibular function: A study of the effects of nodulectomy on habituation , 1967, The Laryngoscope.

[9]  B. Cohen,et al.  Stabilization of gaze during circular locomotion in darkness. II. Contribution of velocity storage to compensatory eye and head nystagmus in the running monkey. , 1992, Journal of neurophysiology.

[10]  D. Tweed,et al.  Rotational kinematics of the human vestibuloocular reflex. III. Listing's law. , 1994, Journal of neurophysiology.

[11]  B Cohen,et al.  Organizational Principles of Velocity Storage in Three Dimensions , 1988, Annals of the New York Academy of Sciences.

[12]  L R Young,et al.  Artificial Gravity Considerations for a Mars Exploration Mission , 1999, Annals of the New York Academy of Sciences.

[13]  C. W. Greene THE AMERICAN PHYSIOLOGICAL SOCIETY. , 1922, Science.

[14]  J. Goldberg,et al.  Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. , 1971, Journal of neurophysiology.

[15]  W Bles,et al.  Eye movements to yaw, pitch, and roll about vertical and horizontal axes: adaptation and motion sickness. , 2002, Aviation, space, and environmental medicine.

[16]  M. Treisman Motion sickness: an evolutionary hypothesis. , 1977, Science.

[17]  B Cohen,et al.  Spatial Orientation of the Vestibular System a , 1992, Annals of the New York Academy of Sciences.

[18]  M. Reschke,et al.  Motion sickness and development of synergy within the spatial orientation system. a hypothetical unifying concept , 1998, Brain Research Bulletin.

[19]  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.

[20]  J R Lackner,et al.  The effective intensity of Coriolis, cross-coupling stimulation is gravitoinertial force dependent: implications for space motion sickness. , 1986, Aviation, space, and environmental medicine.

[21]  J R Lackner,et al.  Elicitation of motion sickness by head movements in the microgravity phase of parabolic flight maneuvers. , 1984, Aviation, space, and environmental medicine.

[22]  F E Guedry,et al.  Habituation to Complex Vestibular Stimulation in Man: Transfer and Retention of Effects from Twelve Days of Rotation at 10 Rpm , 1965, Perceptual and motor skills.

[23]  J R Lackner,et al.  Use of Promethazine to Hasten Adaptation to Provocative Motion , 1994, Journal of clinical pharmacology.

[24]  Theodore Raphan,et al.  Habituation and adaptation of the vestibuloocular reflex: a model of differential control by the vestibulocerebellum , 2004, Experimental Brain Research.

[25]  H Misslisch,et al.  Rotational kinematics of the human vestibuloocular reflex. II. Velocity steps. , 1994, Journal of neurophysiology.

[26]  David Solomon,et al.  Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex , 2004, Experimental Brain Research.

[27]  L R Young,et al.  Orientation illusions and heart-rate changes during short-radius centrifugation. , 2001, Journal of vestibular research : equilibrium & orientation.

[28]  B Cohen,et al.  Control of Spatial Orientation of the Angular Vestibulo‐Ocular Reflex by the Nodulus and Uvula of the Vestibulocerebellum , 1999, Annals of the New York Academy of Sciences.

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

[30]  Gilles Clément,et al.  Effects of cosmonaut vestibular training on vestibular function prior to spaceflight , 2001, European Journal of Applied Physiology.

[31]  B. Cohen,et al.  Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after‐nystagmus , 1977, The Journal of physiology.

[32]  C. Oman A heuristic mathematical model for the dynamics of sensory conflict and motion sickness. , 1982, Acta oto-laryngologica. Supplementum.

[33]  J P Bagian,et al.  A Retrospective Study of Promethazine and Its Failure to Produce the Expected Incidence of Sedation During Space Flight , 1994, Journal of clinical pharmacology.

[34]  W. Bles Coriolis effects and motion sickness modelling , 1998, Brain Research Bulletin.

[35]  Alan D. Miller,et al.  Physiological evidence that the vestibular system participates in autonomic and respiratory control. , 1998, Journal of vestibular research : equilibrium & orientation.

[36]  J R Lackner,et al.  Motion sickness susceptibility in parabolic flight and velocity storage activity. , 1991, Aviation, space, and environmental medicine.

[37]  Benson Aj,et al.  Interaction of linear and angular accelerations on vestibular receptors in man. , 1966 .

[38]  J. R. Lackner,et al.  The effects of gravitoinertial force level and head movements on post-rotational nystagmus and illusory after-rotation , 2004, Experimental Brain Research.

[39]  D F Stewart,et al.  Space motion sickness during 24 flights of the space shuttle. , 1988, Aviation, space, and environmental medicine.

[40]  Theodore Raphan,et al.  Orientation of human optokinetic nystagmus to gravity: a model-based approach , 2004, Experimental Brain Research.

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

[42]  A. Graybiel,et al.  Experiment M131. Human vestibular function , 1973 .

[43]  U. Büttner,et al.  Vestibular nerve activity in the alert monkey during vestibular and optokinetic nystagmus , 2004, Experimental Brain Research.

[44]  S. C. Wang,et al.  Experimental motion sickness in dogs; importance of labyrinth and vestibular cerebellum. , 1956, The American journal of physiology.

[45]  Theodore Raphan,et al.  The vestibulo-ocular reflex in three dimensions , 2002, Experimental Brain Research.

[46]  A Graybiel,et al.  Evaluation of a new antinauseant drug for the prevention of motion sickness. , 1977, Aviation, space, and environmental medicine.

[47]  B. Cohen,et al.  Spatial orientation of caloric nystagmus in semicircular canal-plugged monkeys. , 2002, Journal of neurophysiology.

[48]  B. Cohen,et al.  Modeling the Organization of the Linear and Angular Vestibulo‐Ocular Reflexes a , 1996, Annals of the New York Academy of Sciences.

[49]  F. Guedry,et al.  Coriolis cross-coupling effects: disorienting and nauseogenic or not? , 1978, Aviation, space, and environmental medicine.

[50]  B Cohen,et al.  Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. , 1998, Journal of neurophysiology.

[51]  Willem Bles,et al.  Roll motion stimuli: sensory conflict, perceptual weighting and motion sickness , 1998, Brain Research Bulletin.

[52]  B. Cohen,et al.  Vertical optokinetic nystagmus and vestibular nystagmus in the monkey: Up-down asymmetry and effects of gravity , 2004, Experimental Brain Research.

[53]  B. Cohen,et al.  Spatial orientation of the vestibular system: dependence of optokinetic after-nystagmus on gravity. , 1991, Journal of neurophysiology.

[54]  A GRAYBIEL,et al.  VESTIBULAR HABITUATION DURING REPETITIVE COMPLEX STIMULATION: A STUDY OF TRANFER EFFECTS. , 1964, Journal of applied physiology.

[55]  C. Oman,et al.  Horizontal angular VOR, nystagmus dumping, and sensation duration in spacelab SLS-1 crewmembers. , 1993, Journal of vestibular research : equilibrium & orientation.

[56]  B. Cohen,et al.  The relation of motion sickness to the spatial–temporal properties of velocity storage , 2003, Experimental Brain Research.

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

[58]  F. O. Black,et al.  Optokinetic and vestibulo-ocular reflex responses to an unpredictable stimulus. , 1987, Aviation, space, and environmental medicine.

[59]  J R Lackner,et al.  Treatment of severe motion sickness with antimotion sickness drug injections. , 1987, Aviation, space, and environmental medicine.

[60]  A. Graybiel,et al.  Diagnostic criteria for grading the severity of acute motion sickness. , 1968, Aerospace medicine.

[61]  H. Shojaku,et al.  Secondary vestibular cholinergic projection to the cerebellum of rabbit and rat as revealed by choline acetyltransferase immunohistochemistry, retrograde and orthograde tracers , 1992, The Journal of comparative neurology.

[62]  D. Tweed,et al.  Rotational kinematics of the human vestibuloocular reflex. I. Gain matrices. , 1994, Journal of neurophysiology.

[63]  A GRAYBIEL,et al.  Observations on human subjects living in a "slow rotation room" for periods of two days. , 1960, Archives of neurology.

[64]  P. Denise,et al.  Motion sickness occurrence does not correlate with nystagmus characteristics , 2000, Neuroscience Letters.

[65]  T Raphan,et al.  Modeling the spatiotemporal organization of velocity storage in the vestibuloocular reflex by optokinetic studies. , 1991, Journal of neurophysiology.