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Brainstem processing of vestibular sensory exafference: implications for motion sickness etiology

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Abstract

The origin of the internal “sensory conflict” stimulus causing motion sickness has been debated for more than four decades. Recent studies show a subclass of neurons in the vestibular nuclei and deep cerebellar nuclei that respond preferentially to passive head movements. During active movement, the semicircular canal and otolith input (“reafference”) to these neurons are canceled by a mechanism comparing the expected consequences of self-generated movement (estimated with an internal model—presumably located in the cerebellum) with the actual sensory feedback. The un-canceled component (“exafference”) resulting from passive movement normally helps compensate for unexpected postural disturbances. Notably, the existence of such vestibular “sensory conflict” neurons had been postulated as early as 1982, but their existence and putative role in posture control and motion sickness have been long debated. Here, we review the development of “sensory conflict” theories in relation to recent evidence for brainstem and cerebellar reafference cancelation, and identify some open research questions. We propose that conditions producing persistent activity of these neurons, or their targets, stimulate nearby brainstem emetic centers—via an as yet unidentified mechanism. We discuss how such a mechanism is consistent with the notable difference in motion sickness susceptibility of drivers as opposed to passengers, human immunity to normal self-generated movement and why head restraint or lying horizontal confers relative immunity. Finally, we propose that fuller characterization of these mechanisms and their potential role in motion sickness could lead to more effective, scientifically based prevention and treatment for motion sickness.

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Acknowledgments

Dr. Oman was supported in part by the National Space Biomedical Research Institute through NASA NCC 9-58. Dr. Cullen’s research was supported by the Canadian Institutes of Health Research (CIHR), the National Institutes of Health (DC002390), the Fonds Québécois de la Recherche sur la Nature et les Technologies (FQNRT), and US National Institute of Health Grant R01 DC2390.

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  1. Man Vehicle Laboratory, Massachusetts Institute of Technology, Room 37-219, MIT 77 Massachusetts Avenue, Cambridge, MA, 02139, USA

    Charles M. Oman

  2. Aerospace Medical Research Unit, Department of Physiology, McGill University, Montreal, QC, Canada

    Kathleen E. Cullen

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  1. Charles M. Oman
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Correspondence to Charles M. Oman.

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Oman, C.M., Cullen, K.E. Brainstem processing of vestibular sensory exafference: implications for motion sickness etiology. Exp Brain Res 232, 2483–2492 (2014). https://doi.org/10.1007/s00221-014-3973-2

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