Vestibular Perception and Action Employ Qualitatively Different Mechanisms. II. VOR and Perceptual Responses During CombinedTilt&Translation

Abstract

To compare and contrast the neural mechanisms that contribute to vestibular perception and action, we measured vestibuloocular reflexes (VOR) and perceptions of tilt and translation. We took advantage of the well-known ambiguity that the otolith organs respond to both linear acceleration and tilt with respect to gravity and investigated the mechanisms by which this ambiguity is resolved. A new motion paradigm that combined roll tilt with inter-aural translation ("Tilt&Translation") was used; subjects were sinusoidally (0.8 Hz) roll tilted but with their ears above or below the rotation axis. This paradigm provided sinusoidal roll canal cues that were the same across trials while providing otolith cues that varied linearly with ear position relative to the earth-horizontal rotation axis. We found that perceived tilt and translation depended on canal cues, with substantial roll tilt and inter-aural translation perceptions reported even when the otolith organs measured no inter-aural force. These findings match internal model predictions that rotational cues from the canals influence the neural processing of otolith cues. We also found horizontal translational VORs that varied linearly with radius; a minimal response was measured when the otolith organs transduced little or no inter-aural force. Hence, the horizontal translational VOR was dependent on otolith cues but independent of canal cues. These findings match predictions that translational VORs are elicited by simple filtering of otolith signals. We conclude that internal models govern human perception of tilt and translation at 0.8 Hz and that high-pass filtering governs the human translational VOR at this same frequency.

Frequency dependence of vestibuloocular reflex thresholds

“…6, there was a clear divergence of the perceptual and VOR thresholds, which was predominantly caused by a substantial increase in human yaw rotation thresholds, at frequencies below 0.5 Hz (Benson et al 1989;Grabherr et al 2008). While we cannot rule out a species effect, we think that such differences between vestibular perception and vestibular action (e.g., the VOR) suggest that some neural processing affects vestibular perception-specifically perceptual decision making-with little or no effect on the VOR (Merfeld et al 2005a(Merfeld et al , 2005b.…”

Visual and vestibular perceptual thresholds each demonstrate better precision at specific frequencies and also exhibit optimal integration

“…In both reflexes and perception, dynamics originate from the sensory periphery and central processing (as well as motor responses for reflexes), but these dynamics are not necessarily the same. For example, there are qualitative differences in sensory processing between the VOR and vestibular perception (Merfeld et al 2005a(Merfeld et al , 2005b, and differences in the frequency response between VOR thresholds and vestibular perceptual thresholds (Haburcakova et al 2012). In addition, perception usually involves a host of processes, including cognitive, that could be the source of our measured perceptual dynamics and differences between vestibular and visual perceptual precision.…”

“…However, higher gain responses do not dictate higher precision. Furthermore, perception need not mimic reflexive findings, as demonstrated by qualitative differences in sensory processing in the vestibulo-ocular reflex (VOR) and vestibular perception (Merfeld et al 2005a(Merfeld et al , 2005b. Therefore, we chose to measure perceptual thresholds to assay perceptual precision [as per conventional definitions, precision varies inversely to threshold and is defined as the inverse of variance i.e., 1/ 2 , and is analogous to reliability (Faisal et al 2008)].…”

Responses of Monkey Vestibular-Only Neurons to Translation and Angular Rotation

“…Extra vestibular inputs may be especially important for resolving tilt-translation ambiguities in the verylow-frequency range where canal signals imperfectly encode angular head velocity. Similarly, Merfeld and colleagues (Merfeld and Zupan 2002;Merfeld et al 1999Merfeld et al , 2005b) demonstrated that humans may use canal cues to improve their distinction of tilt and translation perceptually but that the oculomotor system appears to use high pass filtering of otolith cues to produce the translational VOR (Merfeld et al 2005a,b). The latter may be a species difference because Angelaki and co-workers' data support a multisensory convergence model for controlling eye movements in monkeys (e.g., Angelaki et al 1999Angelaki et al , 2004Green and Angelaki 2004).…”