Transfer characteristics of first and second order lateral canal vestibular neurons in gerbil

Abstract

Discharge patterns of first and second order vestibular neurons responding to angular acceleration in the plane of the lateral canals were studied in gerbil. The resting discharge activity of each cell was used to characterize the neuron by measureing the coefficient of variation and coefficient of skewness of the interspike interval distributions. Sinusoidal angular oscillations ranging in frequency from 0.0125 to 5.0 Hz were delivered by a velocity controlled rate-table. A PDP-12 minicomputer system was used on-line to display period and post-stimulus histograms of discriminated single unit activity. Off-line Fourier analysis of the period histograms was used to determine the phase of cell response to sinusoidal accelerations, while the average level and amplitude were determined by a least squares fitting algorithm applied over the fraction of the stimulus period where the cell discharged. First order neurons were found to have high discharge rates (average = 61.7 imp./sec) and bidirectional responses to rotation, and were of two groups called regular and irregular according to their resting discharge patterns. Second order neurons, located mainly in the medial and lateral vestibular nuclei, had low or even zero resting discharge rates (average = 17.8) resulting in more uni-directional responses and were of a single population. For frequencies less than 10 Hz, the Bode plots of the regular first order neurons are similar to that of a first order system with a time constant of about 2 sec as predicted by the torsion pendulum theory for cupula movement. The irregular first order neurons show an increasing gain above 0.5 Hz and a large phase lead relative to angular velocity above 1.0 Hz suggestive of a fractional power transfer function. The second order neurons show the phase and gain characteristics of the regular first order neurons being in phase with angular velocity above 1.0 Hz.

Responses of Irregularly Discharging Chinchilla Semicircular Canal Vestibular-Nerve Afferents During High-Frequency Head Rotations

“…Note that the average responses of low-gain irregular afferents rise to match those of high-gain irregular afferents at high frequencies. Curthoys 1982;Dickman and Correia 1989b;Fernandez and Goldberg 1971;Goldberg and Fernandez 1971;Haque et al 2004;Landolt and Correia 1980;O'Leary et al 1976;Schneider and Anderson 1976;Tomko et al 1981;Yagi et al 1977). A regression between each afferent's CV* and each of the two time constants making up the two-zero lead operator best fitting its responses was performed.…”

Afferent diversity and the organization of central vestibular pathways

“…Discharge properties of vestibular-nerve fibers have been described in several mammals Fernández 1971a, 1971b;Fernández and Goldberg 1971, 1976a, 1976bSchneider and Anderson 1976;Baird et al 1988;Goldberg et al 1990a;Lysakowski et al 1995) and in selected lower vertebrates, including the toadfish (Boyle and Highstein 1990a), frog (Honrubia et al 1989;Myers and Lewis 1990), and turtle Goldberg 1996, 2000a). In most of these species, it has proved useful to distinguish afferents as having a regular or an irregular spacing of action potentials (Fig.…”

Response Linearity of Alert Monkey Non-Eye Movement Vestibular Nucleus Neurons During Sinusoidal Yaw Rotation

“…These authors also reported on the sensitivity versus frequency relationship of central vestibular neurons in the same preparation (Jones and Milsum 1971). Their findings were expanded by subsequent investigators in nonprimate species (Broussard et al 2004;Schneider and Anderson 1976;Shinoda and Yoshida 1974) and in alert monkeys (Buttner et al 1978;Cullen and McCrea 1993;Dickman and Angelaki 2004;Fuchs and Kimm 1975;Keller and Kamath 1975;Ramachandran and Lisberger 2008). Most of these studies concerned the effect of frequency on the sensitivity and phase of responses of individual neurons and demonstrate a relatively flat relationship for frequencies between 0.1 and 2.0 Hz with an increasing phase lead relative to velocity as the frequency of rotation increases.…”

“…Thus very high sensitivity with low-stimulus amplitudes allow for detection of low-amplitude signals over the inherent noise from the spontaneous activity of these cells. Although we did not calculate the regularity of firing rate of these cells, others have noted that second-order vestibular neurons fire with a range of regularity, but on the whole demonstrate more irregularity than afferents because there is no population of central neurons as regularly firing as regular afferents (Chen-Huang et al 1997;Iwamoto et al 1990;Schneider and Anderson 1976).…”

“…These authors fit the data with a power function with an exponent of 0.28 and concluded that the nonlinear effect was "apparently very small." In anesthetized gerbils, Schneider and Anderson (1976) reported on the responses of vestibular afferents and central neurons to sinusoidal yaw rotation at frequencies ranging from 0.05 to 5 Hz. These authors also tested five central neurons for linearity of sensitivity by varying the peak velocity from 32 to 256°/s.…”