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The instantaneous training demand drives vestibulo-ocular reflex adaptation

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Abstract

The vestibulo-ocular reflex (VOR) maintains stable vision during rapid head rotations by rotating the eyes in the opposite direction to the head. The latency between onset of the head rotation and onset of the eye rotation is 5–8 ms in healthy humans. However, VOR latency can be 3–4 times larger in patients treated with intra-tympanic gentamicin. A prior study showed that latency can be trained with head rotations at 0.2 Hz. We sought to determine how the VOR is affected when a delay between vestibular and visual stimuli is added during adaptation training with high-frequency head rotations (impulses), where the VOR is the main vision-stabilizing system. Using a variant of the incremental VOR adaptation technique, the delay between head rotation onset and movement onset of a visual target was gradually increased. With this training, the instantaneous VOR gain demand (= target/head velocity) varied from less than unity to greater than unity during each head impulse, albeit in a consistent and repeatable way. We measured the active and passive VOR gain and latency before and after VOR adaptation training in healthy normal subjects. There was no significant change in VOR latency across subjects; however, there was a significant decrease in VOR gain of − 6.0 ± 4.5%. These data suggest that during high-frequency head rotations delay/latency is interpreted as a changing instantaneous VOR gain demand. Although the gain demand in this study had a complex trajectory, adaptation was evident with the VOR seeming to use an average of the instantaneous gain demand.

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Acknowledgements

A. A. Migliaccio was supported by The Garnett Passe and Rodney Williams Memorial Foundation (Grant no. SPRF2014) Senior/Principal Research Fellowship in Otorhinolaryngology.

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Authors and Affiliations

  1. Balance and Vision Laboratory, Neuroscience Research Australia, Cnr Barker Street & Easy Street, Randwick, Sydney, NSW, 2031, Australia

    William V. C. Figtree, Carlo N. Rinaudo & Americo A. Migliaccio

  2. University of New South Wales, Sydney, NSW, 2033, Australia

    Carlo N. Rinaudo & Americo A. Migliaccio

  3. Laboratory of Vestibular NeuroAdaptation, Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University, Baltimore, MD, 21205, USA

    Michael C. Schubert

  4. Department of Physical Medicine and Rehabilitation, Johns Hopkins University, Baltimore, MD, 21205, USA

    Michael C. Schubert

  5. Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University, Baltimore, MD, 21205, USA

    Americo A. Migliaccio

  6. School of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, Australia

    Americo A. Migliaccio

Authors
  1. William V. C. Figtree
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  2. Michael C. Schubert
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  3. Carlo N. Rinaudo
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  4. Americo A. Migliaccio
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Correspondence to Americo A. Migliaccio.

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Communicated by Winston D Byblow.

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Figtree, W.V.C., Schubert, M.C., Rinaudo, C.N. et al. The instantaneous training demand drives vestibulo-ocular reflex adaptation. Exp Brain Res 238, 2965–2972 (2020). https://doi.org/10.1007/s00221-020-05953-1

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