Response of Vestibular Nerve Afferents Innervating Utricle and Saccule During Passive and Active Translations

Abstract

Jamali M, Sadeghi SG, Cullen KE. Response of vestibular-nerve afferents innervating utricle and saccule during passive and active translations. J Neurophysiol 101: 141-149, 2009. First published October 29, 2008 doi:10.1152/jn.91066.2008. The distinction between sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. In this study, we investigated whether linear translations are encoded similarly during active and passive translations by the otolith system. Vestibular nerve afferents innervating the saccule or utricle were recorded in alert macaques. Single unit responses were compared during passive whole body, passive head-on-body, and active head-on-body translations (vertical, fore-aft, or lateral) to assess the relative influence of neck proprioceptive and efference copy-related signals on translational coding. The response dynamics of utricular and saccular afferents were comparable and similarly encoded head translation during passive whole body versus head-on-body translations. Furthermore, when monkeys produced active head-on-body translations with comparable dynamics, the responses of both regular and irregular afferents remained comparable to those recorded during passive movements. Our findings refute the proposal that neck proprioceptive and/or efference copy inputs coded by the efferent system function to modulate the responses of the otolith afferents during active movements. We conclude that the vestibular periphery provides faithful information about linear movements of the head in the space coordinates, regardless of whether they are self-or externally generated.

Cervical and Ocular Vestibular Evoked Myogenic Potentials Are Sensitive to Stimulus Phase

“…At such high frequency, the receptors could be responding to a change in acceleration, termed jerk . Animal studies have identified irregular-discharging afferents which are 10 times more responsive to the jerk component than the acceleration itself [Jamali et al, 2009]. Studies of the vestibulo-ocular reflex have shown that a response to jerk can be recorded from neurones in the vestibular nuclei and may originate from the otolith organs [Angelaki et al, 1993;Angelaki and Hess, 1996].…”

Muscarinic Acetylcholine Receptors and M-Currents Underlie Efferent-Mediated Slow Excitation in Calyx-Bearing Vestibular Afferents

“…In fish and amphibians, efferent-mediated fast inhibition or excitation attenuates afferent responsiveness during self-generated movements (Boyle and Highstein, 1990;Chagnaud et al, 2015), but the evidence for similar attenuation in mammals has been less compelling Sadeghi et al, 2007b;Jamali et al, 2009). Recent studies in mice have indicated that the EVS modulates the amplitude of the vestibulo-ocular reflex (VOR) and vestibular stimulus-evoked potentials (Luebke et al, 2014;Hübner et al, 2015;Morley et al, 2016).…”

The Challenge of Understanding the Brain: Where We Stand in 2015

“…One underlying algorithm for how an animal can determine its location in an environment is called path integration, a process that depends on integrating a velocity signal (this process is what helps you find the bathroom in the dark). Velocity can be derived from the vestibular system, from optic flow, and from the motor system (how many steps have been taken) (Calton et al, 2003; Dombeck et al, 2010; Jamali et al, 2009; Ravassard et al, 2013; Stackman et al, 2002; Terrazas et al, 2005). Current ideas about the network mechanism of integration are best understood by considering a simplified one-dimensional integrator network in which cells are arranged along a line (Fig.1D).…”