Computation of Inertial Motion: Neural Strategies to Resolve Ambiguous Otolith Information

Abstract

According to Einstein's equivalence principle, inertial accelerations during translational motion are physically indistinguishable from gravitational accelerations experienced during tilting movements. Nevertheless, despite ambiguous sensory representation of motion in primary otolith afferents, primate oculomotor responses are appropriately compensatory for the correct translational component of the head movement. The neural computational strategies used by the brain to discriminate the two and to reliably detect translational motion were investigated in the primate vestibulo-ocular system. The experimental protocols consisted of either lateral translations, roll tilts, or combined translation-tilt paradigms. Results using both steady-state sinusoidal and transient motion profiles in darkness or near target viewing demonstrated that semicircular canal signals are necessary sensory cues for the discrimination between different sources of linear acceleration. When the semicircular canals were inactivated, horizontal eye movements (appropriate for translational motion) could no longer be correlated with head translation. Instead, translational eye movements totally reflected the erroneous primary otolith afferent signals and were correlated with the resultant acceleration, regardless of whether it resulted from translation or tilt. Therefore, at least for frequencies in which the vestibulo-ocular reflex is important for gaze stabilization (>0.1 Hz), the oculomotor system discriminates between head translation and tilt primarily by sensory integration mechanisms rather than frequency segregation of otolith afferent information. Nonlinear neural computational schemes are proposed in which not only linear acceleration information from the otolith receptors but also angular velocity signals from the semicircular canals are simultaneously used by the brain to correctly estimate the source of linear acceleration and to elicit appropriate oculomotor responses.

A Controlled Attractor Network Model of Path Integration in the Rat

“…There is evidence to suggest that the monkey vestibular system has the ability to determine an unambiguous translational acceleration relative to the current direction of the head based on inputs from the otoliths and semi-circular canals (Angelaki et al 1999). Experiments by Hess and Dieringer (1991) suggest that rats have the same ability.…”

Temporal dynamics of semicircular canal and otolith function following acute unilateral vestibular deafferentation in humans

“…Canal and otolith inputs are likely to interact centrally in synergistic rather than linear ways. It has been proposed that the canals can influence the otolith VOR (Angelaki 2004;Glasauer and Merfeld 1997;Merfeld 1995;Merfeld and Zupan 2002), since afferent information from both canals and otoliths can be integrated to distinguish translation from tilt (Angelaki 2004;Angelaki et al 1999;Glasauer and Merfeld 1997;Angelaki 2003, 2004;Merfeld 1995;Merfeld and Zupan 2002;Merfeld et al 1999;Mergner and Glasauer 1999;Zupan et al 2002). The finding of the current study is in agreement with suggestions that the otolith VOR performs better when the canal VOR is simultaneously stimulated (Angelaki et al 2002;Ramat and Zee 2003) and is thus calibrated to function synergistically (Crane et al 1997;Crane 1998, 2001;Demer and Viirre 1996;Imai et al 2001;Moore et al 2001;Raphan et al 2001).…”

Human 3-D aVOR with and without otolith stimulation

“…When the otolith organs are stimulated during head tilt, it is possible the stimulation could be interpreted as a head translation, thereby invoking the translational VOR (tVOR). The nervous system could distinguish tilt from translation through frequency segregation (Paige and Tomko 1991;Mayne 1974), or by combining otolith signals with other sensory signals such as canal signals (Merfeld and Young 1995;Merfeld et al 1993;Zupan et al 2002;Angelaki et al 1999). Our data cannot distinguish between these proposals, but they do indicate how well the tilt/translation ambiguity is resolved.…”

“…Since a change in head orientation relative to gravity is a rotation, otolith afferents also carry implicit information about head rotation. We expect that the nervous system would use all available information to compensate for any inherent limitations in sensory systems (Zupan et al 2002;Angelaki et al 1999;Bockisch et al 2003), and to adapt to changes that occur due to development, aging, disease, and injury. One limitation of the semi-circular canals is their high-pass frequency characteristics, caused primarily by the elastic restoring force of the cupula (Fernandez and Goldberg 1971).…”