Quantification of Different Classes of Canal‐Related Vestibular Nuclei Neuron Responses to Linear Acceleration

Abstract

A change in otolith activity modifies the dynamic responses of both the and the vertical4 vestibuloocular reflexes (VOR). In response to rotations in vertical planes, dynamic otolith activity is necessary for compensatory eye movements in the rabbit5 and the cat.6 Therefore, significant convergence of otolith and canal information in the VOR pathway must occur.The activity of single vestibular nuclei neurons in the decerebrate rat were recorded extracellularly during sinusoidal linear translation in the horizontal head plane. Details of the experimental procedure are presented elsewhere.' Neurons from the four groups-(1) type I and (2) type I1 horizontal canal related, (3) vertical canal related, and (4) purely otolith-were systematically tested for their responses to translation at various horizontal head orientations. These responses were then used to describe a response ellipse*JO in which the semimajor axis (S1) defined the cell's direction of maximum sensitivity and its associated gain and phase and the semiminor axis (S2) defined the minimum sensitivity of the cell in the horizontal head plane. When the magnitude of the S2 vector was zero, the response was referred to as narrowly tuned and was characterized by gain values that were proportional to the cosine of the angle between S1 and the stimulus direction and phase values that were constant with respect to stimulus direction. Whereas, a response with a nonzero magnitude of the S2 vector was referred to as broadly tuned and was characterized by a response phase that varied as a function of stimulus angle. The accuracy with which the response ellipse quantitatively described the data was assessed by comparing the direction, gain, and phase values of the maximum response determined empirically with those calculated from the fitted curves (compare the data points with the curve in FIGURE 1). The calculated and experimentally measured responses had high linear regression coefficients (r = 0.93014.9976) and slopes close to unity.Broadly tuned neurons were observed in each of the four groups of neurons studied. The ratio of S2 and S, response magnitudes (tuning ratio) was calculated for all neurons.

Spatio-temporal convergence (STC) in otolith neurons

“…The simulations presented here are relevant whenever broadly-tuned response behavior may be created by convergence of narrowly-tuned inputs, as for example in primary otolith afferents (Fernandez and Goldberg 1976b;Dickman et al 1991) and vestibular nuclei neurons Bush et al 1992). The goal of the present investigation has been to attempt to explain the observed tuning ratios exhibited by primary otolith afferents (Dickman et al 1991) and central vestibular nuclei neurons ) that respond in the linear range of their force-response curves.…”

“…1A). The output of the convergent neuron could represent any broadlytuned vestibular nuclei neuron Bush et al 1992) or any broadly-tuned primary afferent (Dickman et al 1991). In the former case, the input units would correspond to narrowly-tuned primary otolith afferents projecting to the vestibular nuclei.…”

“…Primary otolith afferents and central otolith neurons have been traditionally treated as one dimensional linear sensors with spatial properties that were completely specified by a single vector in space corresponding to the direction of maximum sensitivity of the neuron (polarization vector). Recently, however, evidence has been presented that some primary otolith afferents (Fernandez and Goldberg 1976b;Dickman et al 1991) and most central otolith neurons Bush et al 1992) exhibit more complex spatial response properties. The response gain of these neurons is not always a cosine function of stimulus direction and the response phase may depend on stimulus orientation.…”

“…The authors attributed these responses to spatio-temporal convergence (STC) of signals arising from the otolith organs and the semicircular canals. However, spatio-temporal convergence may also occur between different primary otolith afferents and/or otolith hair cells since broadly-tuned response behavior has been observed during stimulation with pure linear acceleration Bush et al 1992). Given the experimental results in primary otolith afferents (Dickman et al 1991) and vestibular nuclei neurons Bush et al 1992), several questions arise.…”

“…However, spatio-temporal convergence may also occur between different primary otolith afferents and/or otolith hair cells since broadly-tuned response behavior has been observed during stimulation with pure linear acceleration Bush et al 1992). Given the experimental results in primary otolith afferents (Dickman et al 1991) and vestibular nuclei neurons Bush et al 1992), several questions arise. For example, what is the required temporal and spatial differences between two narrowly-tuned input units in order to produce a broadly-tuned response in the target neuron similar to that observed experimentally?…”