Incremental angular vestibulo-ocular reflex adaptation to active head rotation

Abstract

Studies on motor learning typically present a constant adaptation stimulus, corresponding to the desired final adaptive state. Studies of the auditory and optokinetic systems provide compelling evidence that neural plasticity is enhanced when the error signal driving adaptation is instead adjusted gradually throughout training. We sought to determine whether the angular vestibulo-ocular reflex (aVOR) may be adaptively increased using an incremental velocity error signal (IVE) compared with a conventional constant and large velocity-gain demand (x2). We compared the magnitude of aVOR gain change for these two paradigms across different motion contexts (active and passive). Seven individuals with normal vestibular function and six individuals with unilateral vestibular hypofunction (UVH) were exposed to the IVE and x2 (“control”) aVOR demand tasks. Each subject participated in 10 epochs of 30 active head impulses over a 15 min aVOR gain increase training session separately for the IVE and x2 paradigms, separated by either seven days (normal subjects) or 14 days (UVH subjects). For both normal and UVH subjects, both paradigms led to aVOR gain increase during the training session. For the normal subjects, the IVE paradigm led to larger aVOR gain change after training compared to the x2 paradigm, for both active (mean 17.3 ± 4% vs. mean 7.1 ± 9%, P = 0.029) and passive (mean 14.2 ± 5% vs. 4.5 ± 8%, P = 0.018) head impulses. For subjects with UVH, IVE produced a greater change in aVOR gain for active head impulses (mean 18.2 ± 9.2% vs. mean –6 ± 3.8%, P = 0.003). However, aVOR gains for passive head impulses were less consistent after IVE, with only two subjects displaying greater aVOR gain with this incremental paradigm. Some individuals generated compensatory saccades that occurred in the same direction of the deficient aVOR during either training paradigm. Our data suggest that the aVOR is modifiable when the velocity error signal is presented incrementally, and that this adaptation stimulus is particularly effective in the case of unilateral vestibular hypofunction. This has implications for programs of vestibular rehabilitation, where active head rotation is prescribed as a means to improve gaze stability.

Vestibulo-Ocular Reflex Responses to a Multichannel Vestibular Prosthesis Incorporating a 3D Coordinate Transformation for Correction of Misalignment

“…The closer we can bring the initial response to our desired outcome, the more likely it is that central adaptive mechanisms can finish the job . Vestibular rehabilitation exercises enhance vestibular compensation after unilateral labyrinthine injury by enlisting adaptive vestibulocerebellar circuits to improve gaze and postural stability (Szturm et al 1994;Scherer et al 2008;Schubert et al 2008). After unilateral labyrinthectomy, the central nervous system is quite adept at asymmetric adaptation during visuo-vestibular conflict exercises designed to augment aVOR gain during head rotations toward the deficient side (Ushio et al 2009).…”

Unilateral Adaptation of the Human Angular Vestibulo-Ocular Reflex

“…Nonvestibular motor control studies and auditory perception studies indicate that smaller and incremental error signals in learning tasks drive neural plasticity and learning more effectively than large error signals (Kagerer et al 1997;Nagarajan et al 1998Nagarajan et al , 1999Kilgard and Merzenich 2002). Recently, Schubert et al (2008) showed that the VOR can be modified similarly by smaller incremental retinal image velocity slip stimuli during self-generated head rotations (Schubert et al 2008). A×1.1 stimulus was used to increase the VOR by 10 % and, after a brief rest, a×1.2 stimulus took it a further 10 % (20 % total).…”

“…The study of Schubert et al (2008) used a bilateral stimulus of retinal image velocity slip that induced adaptation so that the VOR gain was driven up for head rotations towards both the healthy and lesioned side. This is not ideal for patients with a unilateral lesion whose VOR is under-compensatory (gainG1) only for head rotation towards the lesioned side.…”

“…Only the lesioned side needs increasing-the normal side does not. In fact, increasing the normal side gain is undesirable because it results in over-compensatory eye movements (Schubert et al 2008). The ideal is a unilateral retinal slip stimulus that incrementally increases the VOR only for rotations towards the lesioned ear.…”

Rehabilitacja przedsionkowa w zawrotach głowy i zaburzeniach równowagi

“…Wyróżnia się kilka elementów decydujących o powodzeniu adaptacyjnych ćwiczeń okoruchowych: zróż-nicowana amplituda ślizgania siatkówkowego (ruchów głowy), różna prędkość ruchów głowy i zróżnicowanie kierunków ruchów głowy. Pacjent powinien wykonywać ćwi-czenia stabilizujące spojrzenie 4-5 razy dziennie (łącznie około 20-40 minut dziennie), używając dobrze widocznego obiektu fiksacji wzrokowej [26,27,[29][30][31].…”