Variation in response dynamics of regular and irregular vestibular-nerve afferents during sinusoidal head rotations and currents in the chinchilla

Abstract

In mammals, primary vestibular afferents that innervate only type I hair cells (calyx-only afferents) respond nearly in phase with head acceleration for high-frequency motion, whereas afferents that innervate both type I and type II (dimorphic) or only type II (bouton-only) hair cells respond more in phase with head velocity. Afferents that exhibit irregular background firing rates have a larger phase lead re head velocity than those that fire more regularly. We wanted to examine what is the cause of the variation in phase lead between regular and irregular afferents at high frequency head rotations. Under the assumption that externally applied galvanic currents act directly on the nerve, we derived a transfer function describing the dynamics of a semicircular canal and its hair cells through comparison of responses to sinusoidally modulated head velocity and currents. All afferent responses were well fit with a transfer function with one zero (lead term). Best-fit lead terms describing responses to current for each group of afferents were similar to the lead term describing responses to head velocity for regular afferents (0.006s + 1). This shows that the pre synaptic/synaptic inputs to regular afferents are pure velocity transducers. However, the variation in phase lead between regular and irregular afferents cannot be explained solely by the ratio of type I to II hair cells (Baird et al. 1988) suggesting that the variation is caused by a combination of pre- (type of hair cell) and post- synaptic properties.

Galvanic Vestibular Stimulation: Cellular Substrates and Response Patterns of Neurons in the Vestibulo-Ocular Network

“…This pattern is similar to that of motion-induced responses in the same afferent population with the exception of a further increase in sensitivity above a motion frequency of 1 Hz (dark blue symbols in Fig. 7H ) and generally complies with the dynamics of mammalian afferent fibers despite their separation into different subtypes (Kim et al, 2011). The concurrent phase lead of GVS-induced responses with respect to stimulus velocity in the range of 10 -20°at 0.1 Hz was relatively constant over the tested range of stimulus frequencies for both single-unit responses (red symbols in Fig.…”

“…The recording chamber with the semi-intact X. laevis preparations was mounted on a computercontrolled, motorized two-axis turntable with the preparation centered in the horizontal and vertical rotation axes to provide optimal activation of semicircular canal organs (Lambert et al, 2008(Lambert et al, , 2013. Motion stimuli consisted of sinusoidal rotations across frequencies that ranged from 0.1 to 5.0 Hz (peak velocities: Ϯ6 -60°/s) in either the vertical (yaw) or horizontal (roll) axis to stimulate the bilateral horizontal or the ipsilateral posterior-contralateral anterior vertical semicircular canal pair preferentially as major modulatory vestibular inputs to LR and SO motoneurons, respectively.…”

“…Galvanic currents influence the discharge of otolith and semicircular canal nerve afferents (Goldberg et al, 1984;Schneider et al, 2002;Fitzpatrick and Day, 2004;Kim and Curthoys, 2004;Curthoys and Macdougall, 2012); however, different approaches are used to achieve this goal. Stimulus electrodes in different vertebrate species were either inserted unilaterally or bilaterally into the perilymphatic space of the semicircular canals (Ezure et al, 1983;Goldberg et al, 1984;Angelaki and Perachio, 1993), placed in the middle ear cavity (Kim and Curthoys, 2004;Shanidze et al, 2012;Kim, 2013aKim, , 2013b, or noninvasively attached to the neck for transmastoidal stimulation in human subjects (Fitzpatrick and Day, 2004).…”

“…Stimulus electrodes in different vertebrate species were either inserted unilaterally or bilaterally into the perilymphatic space of the semicircular canals (Ezure et al, 1983;Goldberg et al, 1984;Angelaki and Perachio, 1993), placed in the middle ear cavity (Kim and Curthoys, 2004;Shanidze et al, 2012;Kim, 2013aKim, , 2013b, or noninvasively attached to the neck for transmastoidal stimulation in human subjects (Fitzpatrick and Day, 2004). The latter two methods preserve inner ear function and thus permit experimental perturbations of motion-induced responses (Shanidze et al, 2012).…”

“…The latter two methods preserve inner ear function and thus permit experimental perturbations of motion-induced responses (Shanidze et al, 2012). Independent of the stimulus method, GVS at low intensity activates irregular vestibular afferents, whereas higher stimulus intensities also recruit regular afferents (Goldberg et al, 1984;Kim and Curthoys, 2004;Kim et al, 2011). This stimulus-amplitudedependent activation allows determining various details of vestibular signal processing, such as fiber-specific origins of monosynaptic and disynaptic inputs to central vestibular neurons (Highstein et al, 1987;Minor and Goldberg, 1991;Angelaki and Perachio, 1993;Straka and Dieringer, 2000) or the organization of vestibulo-motor and vestibulo-autonomous reflexes (Courjon et al, 1987;Cohen et al, 2011;Shanidze et al, 2012;Kim, 2013a).…”