Velocity Storage Contribution to Vestibular Self-Motion Perception in Healthy Human Subjects

Abstract

Self-motion perception after a sudden stop from a sustained rotation in darkness lasts approximately as long as reflexive eye movements. We hypothesized that, after an angular velocity step, self-motion perception and reflexive eye movements are driven by the same vestibular pathways. In 16 healthy subjects (25-71 years of age), perceived rotational velocity (PRV) and the vestibulo-ocular reflex (rVOR) after sudden decelerations (90°/s(2)) from constant-velocity (90°/s) earth-vertical axis rotations were simultaneously measured (PRV reported by hand-lever turning; rVOR recorded by search coils). Subjects were upright (yaw) or 90° left-ear-down (pitch). After both yaw and pitch decelerations, PRV rose rapidly and showed a plateau before decaying. In contrast, slow-phase eye velocity (SPV) decayed immediately after the initial increase. SPV and PRV were fitted with the sum of two exponentials: one time constant accounting for the semicircular canal (SCC) dynamics and one time constant accounting for a central process, known as velocity storage mechanism (VSM). Parameters were constrained by requiring equal SCC time constant and VSM time constant for SPV and PRV. The gains weighting the two exponential functions were free to change. SPV were accurately fitted (variance-accounted-for: 0.85 ± 0.10) and PRV (variance-accounted-for: 0.86 ± 0.07), showing that SPV and PRV curve differences can be explained by a greater relative weight of VSM in PRV compared with SPV (twofold for yaw, threefold for pitch). These results support our hypothesis that self-motion perception after angular velocity steps is be driven by the same central vestibular processes as reflexive eye movements and that no additional mechanisms are required to explain the perceptual dynamics.

Human Yaw Rotation Aftereffects with Brief Duration Rotations Are Inconsistent with Velocity Storage

“…When considered in the context of other modes of sensory perception, this finding is not surprising. But in the context of previous studies of yaw rotation perception that have focused on long duration stimuli in which velocity storage is predominant (Keller and Henn 1984;Sinha et al 2008;Bertolini et al 2011;Bertolini et al 2012), these findings may be unexpected. The reason aftereffects were not found in the previous studies was likely because the duration of stimuli was relatively long (i.e., on the order of minutes) a time course where velocity storage may be predominant.…”

“…For this reason, there is usually negative feedback built into the central velocity storage loop. To stimulate this, G i is set to −1/15 s, a value previously found to fit vestibular perception after long duration rotation (Bertolini et al 2011) and identified as a typical value in a recent review (Laurens and Angelaki 2011). However, this velocity storage model did not predict the current observations.…”

“…A control systems model of vestibular perception w a s i m p l e m e n t e d ( M A T L A B S i m u l i n k module-version 2012b) which incorporated the major features of the models previously developed for velocity storage in eye movement recording (Robinson 1977;Raphan et al 1979), then modified for use with vestibular perception with velocity (Bertolini et al 2011), and recent models of yaw perceptual thresholds (Grabherr et al 2008;Soyka et al 2012). …”

“…The challenges to the vestibular system are different in these roles, and thus, vestibular reflexes often do not correlate with perception (Barnett-Cowan et al 2005;Merfeld et al 2005a;Bertolini et al 2011). For instance the vestibulo-ocular reflex (VOR) must respond similarly to every head movement for visual stability to be maintained, while it is much less important for perception of repetitive movements be the same each time the stimulus is encountered.…”

“…Therefore, a continuous rotation cannot be encoded because the fluid will reach the velocity of the surrounding bone with a time constant of~4 s (Goldberg and Fernandez 1971;Dai et al 1999;Ifediba et al 2007). A central velocity storage mech-anism (VSM) acts to prolong this signal to a time constant of 10-30 s (Young and Oman 1969;Cohen et al 1981;Bertolini et al 2011), thus correcting for this deficiency of the semicircular canal and providing a better estimate of head motion (Laurens and Angelaki 2011). This VSM is most frequently studied during velocity steps or after such rotations have abruptly stopped (Cohen et al 1981;Keller and Henn 1984;Okada et al 1999;Sinha et al 2008;Bertolini et al 2011;Bertolini et al 2012).…”