Acoustic clicks activate both the canal and otolith vestibulo-ocular reflex pathways in behaving monkeys

Abstract

Acoustic activation of the vestibular system has been well documented in humans and animal models. In the past decade, sound-evoked myogenic potentials in the sternocleidomastoid muscle (cVEMP) and the extraocular muscles (oVEMP) have been extensively studied, and their potentials as new tests for vestibular function have been widely recognized. However, the extent to which sound activates the otolith and canal pathways remains controversial. In the present study, we examined this issue in a recently developed nonhuman primate model of acoustic activation of the vestibular system, i.e., sound-evoked vestibulo-ocular reflexes (VOR) in behaving monkeys. To determine whether the canal and otolith VOR pathways are activated by sound, we analyzed abducens neurons' responses to clicks that were delivered into either ear. The main finding was that clicks evoked short-latency excitatory responses in abducens neurons on both sides. The latencies of the two responses, however, were different. The mean latency of the contralateral and ipsilateral abducens neurons was 2.44 +/- 0.4 and 1.65 +/- 0.28 ms, respectively. A further analysis of the excitatory latencies, in combination with the known canal and otolith VOR pathways, suggests that the excitatory responses of the contralateral abducens neurons were mediated by the contralateral disynaptic VOR pathways that connect the lateral canal to the contralateral abducens neurons, and the excitatory responses of the ipsilateral abducens neurons were mediated by the ipsilateral monosynaptic VOR pathways that connect the utricle to the ipsilateral abducens neurons. These results provide new insights into the understanding of the neural basis for sound-evoked vestibular responses, which is essential for developing new tests for both canal and otolith functions in humans.

FIG. 1

Click-evoked responses of a typical right abducens neuron (Monkey W). A Right ear click-evoked leftward eye movements and an excitatory response in the neuron. B Left ear click-evoked rightward eye movements and an excitatory response in the neuron. Binned histograms were generated by counting the action potentials within each 0.5 ms bin from 20 ms before to 30 ms after stimulation. The calibration bar is 500 spike/s and 3 deg/s for firing rate (lower panel) and eye velocity (upper panel), respectively. Black line is for the right eye and gray line for the left eye. C Estimation of the latency of the click-evoked response by computing the cumulative probability of evoking a spike after the click. D Comparison of the latencies of the abducens neuron to ipsilateral (open square) and contralateral (open circle) clicks. The latency to ipsilateral click was 1.87 ms (indicated by the black arrow). The latency to contralateral click was 2.92 ms (indicated by the gray arrow).

FIG. 2

Comparison of abducens neurons' latencies to ipsilateral and contralateral clicks. A Abducens neurons' latencies to contralateral clicks are plotted against their latencies to ipsilateral clicks. Dotted line is the unitary line. B Distributions of abducens neurons' latencies to ipsilateral clicks (lower panel) and contralateral clicks (upper panel).

FIG. 3

Composite histograms showing the population's summed responses at the center gaze to contralateral clicks (A) and ipsilateral clicks (B).

FIG. 4

Click-evoked binocular eye movements as a function of gaze eccentricity (Monkey W). A Clicks were delivered into the left ear. B Clicks were delivered into the right ear.

FIG. 5

Separate direct VOR pathways for horizontal canal VOR (A) and utricule VOR (B). Adapted from Angelaki (2004).