Convergence of linear acceleration and yaw rotation signals on non-eye movement neurons in the vestibular nucleus of macaques.

Roughly half of all vestibular nucleus neurons without eye movement sensitivity respond to both angular rotation and linear acceleration. Linear acceleration signals arise from otolith organs, and rotation signals arise from semicircular canals. In the vestibular nerve, these signals are carried by different afferents. Vestibular nucleus neurons represent the first point of convergence for these distinct sensory signals. This study systematically evaluated how rotational and translational signals interact in single neurons in the vestibular nuclei: multisensory integration at the first opportunity for convergence between these two independent vestibular sensory signals. Single-unit recordings were made from the vestibular nuclei of awake macaques during yaw rotation, translation in the horizontal plane, and combinations of rotation and translation at different frequencies. The overall response magnitude of the combined translation and rotation was generally less than the sum of the magnitudes in responses to the stimuli applied independently. However, we found that under conditions in which the peaks of the rotational and translational responses were coincident these signals were approximately additive. With presentation of rotation and translation at different frequencies, rotation was attenuated more than translation, regardless of which was at a higher frequency. These data suggest a nonlinear interaction between these two sensory modalities in the vestibular nuclei, in which coincident peak responses are proportionally stronger than other, off-peak interactions. These results are similar to those reported for other forms of multisensory integration, such as audio-visual integration in the superior colliculus. NEW & NOTEWORTHY This is the first study to systematically explore the interaction of rotational and translational signals in the vestibular nuclei through independent manipulation. The results of this study demonstrate nonlinear integration leading to maximum response amplitude when the timing and direction of peak rotational and translational responses are coincident.

Responses of non-eye-movement central vestibular neurons to sinusoidal yaw rotation in compensated macaques after unilateral semicircular canal plugging.

After vestibular labyrinth injury, behavioral measures of vestibular performance recover to variable degrees (vestibular compensation). Central neuronal responses after unilateral labyrinthectomy (UL), which eliminates both afferent resting activity and sensitivity to movement, have been well-studied. However, unilateral semicircular canal plugging (UCP), which attenuates angular-velocity detection while leaving afferent resting activity intact, has not been extensively studied. The current study reports response properties of yaw-sensitive non-eye-movement rhesus macaque vestibular neurons after compensation from UCP. The responses at a series of frequencies (0.1-2 Hz) and peak velocities (15-210°/s) were compared between neurons recorded before and at least 6 wk after UCP. The gain (sp/s/°/s) of central type I neurons (responding to ipsilateral yaw rotation) on the side of UCP was reduced relative to normal controls at 0.5 Hz, ±60°/s [0.48 ± 0.30 (SD) normal, 0.32 ± 0.15 ipsilesion; 0.44 ± 0.2 contralesion]. Type II neurons (responding to contralateral yaw rotation) after UCP have reduced gain (0.40 ± 0.27 normal, 0.35 ± 0.25 ipsilesion; 0.25 ± 0.18 contralesion). The difference between responses after UCP and after UL is primarily the distribution of type I and type II neurons in the vestibular nuclei (type I neurons comprise 66% in vestibular nuclei normally; 51% ipsilesion UCP; 59% contralesion UCP; 38% ipsilesion UL; 65% contralesion UL) and the magnitude of the responses of type II neurons ipsilateral to the lesion. These differences suggest that the need to compensate for unilateral loss of resting vestibular nerve activity after UL necessitates a different strategy for recovery of dynamic vestibular responses compared to after UCP.

Convergence of vestibular and neck proprioceptive sensory signals in the cerebellar interpositus.

The cerebellar interpositus nucleus (IN) contributes to controlling voluntary limb movements. We hypothesized that the vestibular signals within the IN might be transformed into coordinates describing the body's movement, appropriate for controlling limb movement. We tested this hypothesis by recording from IN neurons in alert squirrel monkeys during vestibular and proprioceptive stimulation produced during (1) yaw head-on-trunk rotation about the C1-C2 axis while in an orthograde posture and (2) lateral side-to-side flexion about the C6-T3 axis while in a pronograde posture. Neurons (44/67) were sensitive to vestibular stimulation (23/44 to rotation and translation, 14/44 to rotation only, 7/44 to translation only). Most neurons responded during contralateral movement. Neurons (29/44) had proprioceptive responses; the majority (21/29) were activated during neck rotation and lateral flexion. In all 29 neurons with convergent vestibular and neck proprioceptive input those inputs functionally canceled each other during all combined sensory stimulation, whether in the orthograde or pronograde posture. These results suggest that two distinct populations of IN neurons exist, each of which has vestibular sensitivity. One population carries vestibular signals that describe the head's movement in space as is traditional for vestibular signals without proprioceptive signals. A second population of neurons demonstrated precise matching of vestibular and proprioceptive signals, even for complicated stimuli, which activated the semicircular canals and otolith organs and involved both rotation and flexion in the spine. Such neurons code body (not head) motion in space, which may be the appropriate platform for controlling limb movements.

Signal processing of semicircular canal and otolith signals in the vestibular nuclei during passive and active head movements.

The vestibular nerve sends signals to the brain that code the movement and position of the head in space. These signals are used by the brain for a variety of functions, including the control of reflex and voluntary movements and the construction of a sense of self-motion. If many of these functions are to be carried out, a distinction must be made between sensory vestibular signals related to active head movements and those related to passive head movements. Current evidence is that the distinction occurs at an early stage of sensory processing in the brain, and the results are evident in the firing behavior of neurons in the vestibular nuclei that receive direct inputs from the vestibular nerve. Several specific examples of how sensory information related to passive and active head movements is transformed in the vestibular nuclei are discussed.

Effect of side-down tilt on optokinetic nystagmus and optokinetic after-nystagmus in cats.

Slow phase velocity (SPV) of optokinetic nystagmus (OKN) and after-nystagmus (OKAN) was examined in the cat in side-down tilts. In the upright position, the axis of SPV (direction of SPV vector) during OKN was always close to the stimulus axis. In side-down positions, yaw stimulation induced OKN with the vector deviating from the stimulus axis toward the pitch-axis, so as to make the SPV rotational plane be shifted toward the earth horizontal plane, while pitch-axis stimulation induced no change in vector direction. This yaw-to-pitch cross-coupling is qualitatively similar to that previously described in primates. SPV vector size during yaw stimulation is greatest when the stimulus axis is oriented vertically, and the vector size is smaller when the stimulus is in the gravity direction than when it is in the anti-gravity direction. The SPV vector for the rapid-rise response showed no clear change with head orientation, indicating that the direct optokinetic pathway has no contribution to the induction of cross-coupling. Cross-coupling was found also during OKAN. The SPV trajectories were fitted well using the velocity storage integrator model. SPV vector change of cat OKN/OKAN in head tilt could be fitted by changing gain elements in the model.