Responses of pigeon horizontal semicircular canal afferent fibers. II. High-frequency mechanical stimulation.

1. The horizontal semicircular canals of anesthetized (barbiturate/ketamine) pigeons were mechanically stimulated by the use of a piezoelectric micropusher that provided controlled indentation of the surgically exposed membranous horizontal semicircular duct. 2. Extracellular action potentials from single horizontal semicircular canal afferent (HCA) fibers were recorded during sinusoidal mechanical stimulation. This method of stimulation was shown in the companion paper to produce equivalent responses to those produced by rotation for frequencies ranging from 0.01 to 10 Hz. 3. Sinusoidal mechanical stimulation produced clearly entrained action potentials in some HCA fibers up to a frequency of 400 Hz (highest stimulus frequency tested), with stimulus probe displacements of +/- 1.0 and +/- 2.5 microns. Thirty-four HCA fibers were thoroughly studied. 4. For most HCA fibers, the number of action potentials per stimulus cycle decreased as stimulus frequency increased, until only one action potential per stimulus cycle was elicited. The point at which only one spike per stimulus cycle was observed was dependent on both the fiber's resting mean discharge rate (MDR) and the fiber's coefficient of variation (CV) obtained during the MDR. 5. Dynamic response properties of individual HCA fibers were found to be correlated with the fiber's CV and the resting level MDR. Neurons with lower CV values had less adaptation, higher short time constants, and lower high corner frequencies than did neurons with high CV values. For a given CV class of HCA fibers, neurons with higher MDRs had more enhanced gains and more advanced phase shifts at high stimulus frequencies than did neurons with lower MDRs. 6. Transfer function parameters affecting the dynamics of the high-frequency response were derived from the mean gain and phase shift values of regular-, intermediate-, and irregular-firing HCA fibers. Best-fit short time constant (tau S) values of 4.6, 1.9, and 2.0 ms; hair cell membrane time constant (tau M) values of 10.3, 13, and 7 ms; excitatory postsynaptic membrane time constant (tau E) values of 0.8, 0.4, and 0.5 ms; and synaptic delay time constant (tau D) values of 0.5, 0.5, and 1.4 ms were determined for regular, intermediate, and irregular classes of HCA fibers, respectively. 7. The values of 4.6, 1.9, and 2.0 ms derived for the regular, intermediate, and irregular afferents would suggest upper-corner frequencies of 35, 84, and 80 Hz for these classes of HCA fibers, respectively.