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

TLDR

Einstein’s equivalence principle makes inertial acceleration indistinguishable from gravity, yet primate oculomotor responses correctly compensate for translational head motion despite ambiguous otolith signals. This study investigates how the primate vestibulo‑ocular system discriminates translation from tilt, proposing nonlinear integration of otolith and semicircular canal signals. Experiments employed lateral translations, roll tilts, and combined translation–tilt paradigms, using nonlinear neural schemes that simultaneously combine otolith and canal inputs. Results show that semicircular canal signals are essential for distinguishing linear acceleration sources; when canals are inactivated, eye movements no longer track translation and instead follow erroneous otolith signals, indicating that at frequencies above 0.1 Hz the system relies on sensory integration rather than frequency segregation.

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.