Determinants of semicircular canal afferent response dynamics in fish

Present results separate the relative contributions of semicircular canal biomechanics from hair cell/afferent biophysics in determining the amplitude and phase of afferent responses to sinusoidal motion of the head. Separation was achieved by combining electrical polarization of the endolymph with mechanical indentation of the canal limb to modulate the instantaneous firing rate of horizontal semicircular canal afferents. The electrical stimulus drives hair cell transduction currents via modulation of the Nernst-Planck potential, whereas the mechanical stimulus mimics head rotation and modulates the open probability of the transduction channels. Responses for electrical polarization therefore reflect post-transduction-current (PTC) mechanisms, and responses for mechanical stimulation include the additional influence of canal mechanics. Linear transfer functions defining individual afferent response dynamics were obtained for low levels of each stimuli and are reported in Bode form providing gain (spikes/s per micron or mV) and phase (deg re: peak stim) over the frequency range from 0.02 to 40 Hz. Combined results for electrical and mechanical stimuli distinguish the component of sensory signal processing carried out by canal mechanics from that carried out by the hair cell/afferent complexes. Individual afferents were categorized according to their response to the mechanical stimuli as low-gain velocity (LG), high-gain velocity (HG) or acceleration (A) sensitive, groups as originally defined by Boyle and Highstein to describe interafferent diversity present within the population. In contrast to the results for mechanical stimuli, all afferent groups exhibit nearly equal increases in gain and phase for increasing frequencies of electrical stimulation. Comparison of individual afferent responses for the two stimuli leads to the conclusion that the LG, HG, and A groups are distinguished primarily by diversity in the mechanical activation of associated hair cells and not by PTC mechanisms. Even though PTC processing does not contribute significantly to determining these groups, it is the primary determinant underlying high-frequency gain and phase enhancements observed in the population average. Comparison of mechanical and electrical responses also reveals the mechanical lower-corner responsible for phase enhancements and gain decreases in all afferents at low frequencies of mechanical stimulation (< 0.05 Hz). Results imply that LG afferents encode angular head velocity by canceling a phase lag and gain attenuation due to the mechanics with a phase lead and gain enhancement due to PTC mechanisms above approximately 0.2 Hz. In contrast, A group afferents encode angular head acceleration by combining high-frequency phase leads and gain enhancements present in both the mechanics and PTC mechanisms across the physiological frequency spectrum. HG afferents fall between these two extremes, and, other than the influence of the mechanical lower-corner, their response primarily reflects PTC processing.