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Eye-head coordination in the guinea pig II. Responses to self-generated (voluntary) head movements

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Abstract

Retinal image stability is essential for vision but may be degraded by head movements. The vestibulo-ocular reflex (VOR) compensates for passive perturbations of head position and is usually assumed to be the major neural mechanism for ocular stability. During our recent investigation of vestibular reflexes in guinea pigs free to move their heads (Shanidze et al. in Exp Brain Res, 2010), we observed compensatory eye movements that could not have been initiated either by vestibular or neck proprioceptive reflexes because they occurred with zero or negative latency with respect to head movement. These movements always occurred in association with self-generated (active) head or body movements and thus anticipated a voluntary movement. We found the anticipatory responses to differ from those produced by the VOR in two significant ways. First, anticipatory responses are characterized by temporal synchrony with voluntary head movements (latency ~1 versus ~7 ms for the VOR). Second, the anticipatory responses have higher gains (0.80 vs. 0.46 for the VOR) and thus more effectively stabilize the retinal image during voluntary head movements. We suggest that anticipatory responses act synergistically with the VOR to stabilize retinal images. Furthermore, they are independent of actual vestibular sensation since they occur in guinea pigs with complete peripheral vestibular lesions. Conceptually, anticipatory responses could be produced by a feed-forward neural controller that transforms efferent motor commands for head movement into estimates of the sensory consequences of those movements.

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Acknowledgments

We want to acknowledge the contribution of Keiji Takemura, M.D. who helped us to develop the methodology for testing guinea pigs; Kevin Lim, Ph.D. for his programing expertise; Beth Hand and James Liadis for data collection and animal care and handling. Dwayne Valliencourt designed and built the specialized animal restraints used for this study and Chris Ellinger kept our electronics running. This research was supported by the following National Institutes of Health grants: P30 NDC005188-07, R21-DC008607-01, and T32 DC000011–30.

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Authors and Affiliations

  1. Department of Otolaryngology, University of Michigan, Ann Arbor, MI, USA

    N. Shanidze, S. Loewenstein, Y. Raphael & W. M. King

  2. Kresge Hearing Research Institute, University of Michigan, 1150 W. Medical Center Drive, Room 4605, Ann Arbor, MI, 48109-5616, USA

    N. Shanidze, S. Loewenstein, Y. Raphael & W. M. King

  3. Neuroscience Graduate Program, University of Michigan, Ann Arbor, MI, USA

    N. Shanidze

  4. School of Literature, Science and the Arts, University of Michigan, Ann Arbor, MI, USA

    S. Loewenstein

  5. Department of Otolaryngology, New York Eye and Ear Infirmary, New York, NY, USA

    A. H. Kim

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  1. N. Shanidze
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  2. A. H. Kim
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  3. S. Loewenstein
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  4. Y. Raphael
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  5. W. M. King
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Correspondence to N. Shanidze.

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Shanidze, N., Kim, A.H., Loewenstein, S. et al. Eye-head coordination in the guinea pig II. Responses to self-generated (voluntary) head movements. Exp Brain Res 205, 445–454 (2010). https://doi.org/10.1007/s00221-010-2375-3

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  • DOI: https://doi.org/10.1007/s00221-010-2375-3

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