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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    • "Given the dynamic ranges (i.e., 04 frequency ranges) investigated, these measured threshold variations as a function of frequency typically reflect 05 peripheral transduction processes and typically have not told us much about decision-making dynamics. With 06 the exception of some vestibular threshold studies (e.g., Benson et al. 1989; Benson et al. 1986; Grabherr et al. 07 2008; Haburcakova et al. 2012; Karmali et al. 2014; Lewis et al. 2011a; b; Lim and Merfeld 2012; Mardirossian 08 et al. 2014; Priesol et al. 2014; Soyka et al. 2012; Soyka et al. 2011; Valko et al. 2012), decision-making 09 studies using signal detection methods have rarely focused on dynamics (e.g., perceptual decisions as a 10 function of frequency , where the frequency is in a range relevant to decision -making as opposed to sensory 11 transduction ). As discussed later in this review , such vestibular threshold studies may help inform us about 12 decision - making dynamics because behaviorally relevant stimulus frequencies overlap with frequencies 13 influenced by decision - making dynamics . "
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    ABSTRACT: Perceptual decision-making is fundamental to a broad range of fields including neurophysiology, economics, medicine, advertising, law, etc. While recent findings have yielded major advances in our understanding of perceptual decision-making, decision-making as a function of time and frequency (i.e., decision-making dynamics) is not well understood. To limit the review length, we focus most of this review on human findings. Animal findings, which are extensively reviewed elsewhere, are included when beneficial or necessary. We attempt to put these various findings and datasets - which can appear to be unrelated in the absence of a formal dynamic analysis - into context using published models. Specifically, by adding appropriate dynamic mechanisms (e.g., high-pass filters) to existing models, it appears that a number of otherwise seemingly disparate findings from the literature might be explained. One hypothesis that arises through this dynamic analysis is that decision-making includes phasic (high-pass) neural mechanisms, an evidence accumulator and/or some sort of mid-trial decision-making mechanism (e.g., peak detector and/or decision boundary).
    Preview · Article · Oct 2015 · Journal of Neurophysiology
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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.
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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.
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