Human Vestibulo-Ocular Reflex Adaptation Reduces when Training Demand Variability Increases

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JARO (2020) DOI: 10.1007/s10162-020-00775-y D 2020 Association for Research in Otolaryngology

Research Article

Journal of the Association for Research in Otolaryngology

Human Vestibulo-Ocular Reflex Adaptation Reduces when Training Demand Variability Increases CARLO N. RINAUDO,1,2 MICHAEL C. SCHUBERT,3,4 WILLIAM V. C. FIGTREE,1,2 PHILLIP D. CREMER,1,5 AMERICO A. MIGLIACCIO1,2,6,7

AND

1

Balance and Vision Laboratory, Neuroscience Research Australia, Cnr Barker Street & Easy Street, Randwick, NSW 2031, Australia 2

University of New South Wales, Sydney, NSW 2033, Australia Laboratory of Vestibular NeuroAdaptation, Department of Otolaryngology - Head and Neck Surgery, Johns Hopkins University, Baltimore, MD 21205, USA 3

4

Department of Physical Medicine and Rehabilitation, Johns Hopkins University, Baltimore, MD 21205, USA Royal North Shore Hospital, Sydney, Australia

5 6

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

7

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

Received: 16 April 2020; Accepted: 14 October 2020

ABSTRACT One component of vestibular rehabilitation in patients with vestibulo-ocular reflex (VOR) hypofunction is gaze-stabilizing exercises that seek to increase (adapt) the VOR response. These prescribed home-based exercises are performed by the patient and thus their use/training is inherently variable. We sought to determine whether this variability affected VOR adaptation in ten healthy controls (× 2 training only) and ten patients with unilateral vestibular hypofunction (× 1 and × 2 training). During × 1 training, patients actively (self-generated, predictable) move their head sinusoidally while viewing a stationary fixation target; for × 2 training, they moved their outstretched hand anti-phase with their head rotation while attempting to view a handheld target. We defined the latter as manual × 2 training because the subject manually controls the target. In this study, head rotation frequency during training incrementally increased 0.5–2 Hz over 20 min. Active and passive (imposed, unpredictable) sinusoidal (1.3Hz rotations) and head impulse VOR gains were Correspondence to: Americo A. Migliaccio & Balance and Vision Laboratory & Neuroscience Research Australia & Cnr Barker Street & Easy Street, Randwick, NSW 2031, Australia. email: a.migliaccio@ neura.edu.au

measured before and after training. We show that for controls, manual × 2 training resulted in significant sinusoidal and impulse VOR adaptation of ~ 6 % and ~ 3 %, respectively, though this was ~two-thirds lower than increases after computer-controlled × 2 training (non-variable) reported in a prior study. In contrast, for patients, there was an increase in impulse but not sinusoidal VOR response after a single session of manual × 2 training. Patients had more than double the variability in VOR demand during manual × 2 training compared to controls, which could explain why adaptation was not significant in patients. Our data su