Vestibular Labyrinth Contributions to Human Whole-Body Motion Discrimination

Departments of Otology and Laryngology and Neurology, Harvard Medical School, and Jenks Vestibular Physiology Laboratory, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts 02114.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 09/2012; 32(39):13537-42. DOI: 10.1523/JNEUROSCI.2157-12.2012
Source: PubMed


To assess the contributions of the vestibular system to whole-body motion discrimination in the dark, we measured direction recognition thresholds as a function of frequency for yaw rotation, superior-inferior translation ("z-translation"), interaural translation ("y-translation"), and roll tilt for 14 normal subjects and for 3 patients following total bilateral vestibular ablation. The patients had significantly higher average threshold measurements than normal (p < 0.01) for yaw rotation (depending upon frequency, 5.4× to 15.7× greater), z-translation (8.3× to 56.8× greater), y-translation (1.7× to 4.5× greater), and roll tilt (1.3× to 3.0× greater)-establishing the predominant contributions of the vestibular system for these motions in the dark.

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Available from: Adrian J Priesol, Dec 26, 2013
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    • "In addition to this, we measured thresholds at two different frequencies because vestibular thresholds depend on frequency (Grabherr et al. 2008; Valko et al. 2012). Importantly, Karmali et al. (2014), who directly compared visual and vestibular motion perception, found lower visual thresholds at frequencies between 0.1 and 1 Hz and observed the opposite pattern at frequencies higher than 2 Hz. "
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    ABSTRACT: Despite the close interrelation between vestibular and visual processing (e.g., vestibulo-ocular reflex), surprisingly little is known about vestibular function in visually impaired people. In this study, we investigated thresholds of passive whole-body motion discrimination (leftward vs. rightward) in nine visually impaired participants and nine age-matched sighted controls. Participants were rotated in yaw, tilted in roll, and translated along the interaural axis at two different frequencies (0.33 and 2 Hz) by means of a motion platform. Superior performance of visually impaired participants was found in the 0.33 Hz roll tilt condition. No differences were observed in the other motion conditions. Roll tilts stimulate the semicircular canals and otoliths simultaneously. The results could thus reflect a specific improvement in canal-otolith integration in the visually impaired and are consistent with the compensatory hypothesis, which implies that the visually impaired are able to compensate the absence of visual input.
    Experimental Brain Research 07/2015; DOI:10.1007/s00221-015-4389-3 · 2.04 Impact Factor
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    • "The optokinetically induced effect is likely to be stronger in vestibular patients because they rely more on visual information than healthy controls (Huygen et al. 1989; Huygen and Verhagen 2011). Recently, Valko et al. (2012) tested dynamic tilt perception in patients with total vestibular loss, showing motion discrimination thresholds during roll rotation about twice as high as healthy controls. While this indicates an important role of vestibular cues in dynamic tilt perception, caution should be taken when extrapolating their results to static tilt perception, for which contribution of other extravestibular cues might be weighted more heavily. "
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    ABSTRACT: Patients with bilateral vestibular loss have balance problems in darkness, but maintain spatial orientation rather effectively in the light. It has been suggested that these patients compensate for vestibular cues by relying on extravestibular signals, including visual and somatosensory cues, and integrating them with internal beliefs. How this integration comes about is unknown, but recent literature suggests the healthy brain remaps the various signals into a task-dependent reference frame, thereby weighting them according to their reliability. In this paper, we examined this account in six patients with bilateral vestibular a-reflexia, and compared them to six age-matched healthy controls. Subjects had to report the orientation of their body relative to a reference orientation or the orientation of a flashed luminous line relative to the gravitational vertical, by means of a two-alternative-forced-choice response. We tested both groups psychometrically in upright position (0°) and 90° sideways roll tilt. Perception of body tilt was unbiased in both patients and controls. Response variability, which was larger for 90° tilt, did not differ between groups, indicating that body somatosensory cues have tilt-dependent uncertainty. Perception of the visual vertical was unbiased when upright, but showed systematic undercompensation at 90° tilt. Variability, which was larger for 90° tilt than upright, did not differ between patients and controls. Our results suggest that extravestibular signals substitute for vestibular input in patients' perception of spatial orientation. This is in line with the current status of rehabilitation programs in acute vestibular patients, targeting at recognizing body somatosensory signals as a reliable replacement for vestibular loss. © 2015 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society.
    05/2015; 3(5). DOI:10.14814/phy2.12385
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    • "The exquisite vestibular selectivity of rotational thresholds (Seemungal et al., 2004; Cutfield et al., 2011) is in stark contrast to the multisensory nature of the process involved in detecting linear accelerations , as underlined by the fact that in some studies employing linear acceleration (Gianna et al., 1997) and tilt thresholds (Bisdorff et al., 1996) are not completely abnormal in patients with bilateral loss of vestibular function . Further support for this viewpoint is provided by a recent comprehensive dataset that demonstrates in patients with bilateral vestibular failure, thresholds for yaw rotations are considerably more abnormal than those found during y-translations (Valko et al., 2012). Therefore, our study is probably the first to show that mental imagery can modulate vestibularly mediated self-motion perception. "
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    ABSTRACT: Imagery and perception are thought to be tightly linked, however, little is known about the interaction between imagery and the vestibular sense, in particular, self-motion perception. In this study, the observers were seated in the dark on a motorised chair that could rotate either to the right or to the left. Prior to the physical rotation, observers were asked to imagine themselves rotating leftwards or rightwards. We found that if the direction of imagined rotation was different to the physical rotation of the chair (incongruent trials), the velocity of the chair needed to be higher for observers to experience themselves rotating relative to when the imagined and the physical rotation matched (on congruent trials). Accordingly, the vividness of imagined rotations was reduced on incongruent relative to congruent trials. Notably, we found that similar effects of imagery were found at the earliest stages of vestibular processing, namely, the onset of the vestibular-ocular reflex was modulated by the congruency between physical and imagined rotations. Together, the results demonstrate that mental imagery influences self-motion perception by exerting top-down influences over the earliest vestibular response and subsequent perceptual decision-making. Copyright © 2015. Published by Elsevier Ltd.
    Neuroscience 01/2015; 291. DOI:10.1016/j.neuroscience.2015.01.021 · 3.36 Impact Factor
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