Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey. I. An electrophysiological analysis.

1. The electrical excitability of vestibular nerve afferents is related to their discharge regularity (23). Irregular (I) afferents are more excitable than regular (R) afferents. We explored the possibility that the differences in electrical excitability could be used to determine the profile of monosynaptic inputs from the ipsilateral vestibular nerve (Vi) to secondary neurons of the vestibular nuclei. The growth of monosynaptic Vi excitatory postsynaptic potentials (EPSPs) as shock strength is increased should reflect the kinds of afferent input that a secondary neuron receives. We were particularly interested in seeing if cells in the vestibular nuclei could be distinguished as R or I neurons depending on whether they received predominantly regular or irregular inputs. Barbiturate-anesthetized squirrel monkeys were used. 2. Recordings were made from vestibular nerve afferents. Shock strength was expressed as multiples of T, the value needed to recruit 10% of the afferents or, as determined empirically, to evoke a detectable field potential in the vestibular nuclei. Most I afferents (85/87 = 98%) were recruited below 4 X T, whereas most R afferents (197/212 = 93%) were first activated above 4 X T. The relation between latent period and electrical excitability was flat for units with thresholds in the range 1-4 X T. Latent periods increased for units with higher thresholds, especially those first activated above 8 x T. The threshold differences between I and R afferents are maximal if the shock falls at approximately half the mean interval after a naturally occurring action potential. The same results were obtained by having each unit fire to a maximal (16-32 X T) conditioning shock and then determining the threshold to a test shock presented 4 ms later. The latter stimulus configuration was used to study the Vi monosynaptic inputs to secondary neurons. The test shock was raised by successive doublings from 1 X T to the strength of the conditioning shock (16-32 X T). 3. Intracellular recordings were made from neurons located in the superior vestibular nucleus or the rostral parts of the medical or lateral vestibular nuclei. Amplitudes and latent periods of Vi EPSPs were measured from averages of several repetitions of each stimulus pair. Each EPSP was calculated by subtracting the extracellular from the intracellular averaged response. Of the 122 neurons sampled, 115 were judged to be monosynaptically related to the ipsilateral vestibular nerve because their Vi EPSPs had latent periods in the range of 0.7-1.4 ms.(ABSTRACT TRUNCATED AT 400 WORDS)