Determinants of semicircular canal afferent response dynamics in the toadfish, Opsanus tau

S. M. Highstein, R. D. Rabbitt, R. Boyle


1. Present results determine the relative contributions of the biomechanical and the posttransduction-current (PTC) mechanisms to the sensory process carried out by the horizontal semicircular canal (HC) in the oyster toadfish, Opsanus tau. The role of each element was estimated using in vivo measurements of hair cell receptor potentials and afferent responses elicited by electrical stimuli and mechanical HC indentation. Individual afferent response dynamics are defined here using first-harmonic transfer functions presented in the form of response gain and phase for sinusoidal stimuli from approximately 0.02-30 Hz. Comparison of the response dynamics for the two types of stimuli distinguishes the mechanical and the PTC transfer functions leading to the neural response. The results show that both mechanisms contribute significantly to the overall signal processing performed by the semicircular canals. 2. Endolymphatic polarization and HC indentation. Modulation of the endolymphatic potential by current injection induces a differential voltage across the apical face of the hair cells that drives the transduction current directly via the Nernst-Planck potential. Results show that the electrical impedance of the apical tight junctions is much larger than the basal impedance to ground in O. tau, such that leakage current to the basolateral space is negligible and the voltage-sensitive basolateral currents remain fully functional during polarization of the endolymph (in the frequency range tested). Extracellular afferent responses to endolymphatic polarization were combined with responses to HC indentation to separate the relative contributions of the mechanical and the PTC mechanisms to the overall afferent response dynamics. Data show that more than one-half of the overall signal processing, as defined by the first-harmonic transfer function, persists even when canal mechanics is bypassed. 3. Hair-cell receptor potential modulation during HC indentation. Sharp microelectrodes were used to record the modulation of hair-cell receptor potentials (intracellular voltages) in vivo during physiological levels of sinusoidal HC indentation. Receptor potentials exhibit modulations dominated by the first harmonic and centered about the resting potential. The average gain of the receptor-potential modulation for HC indentation is approximately 0.88 mV/microns indent, corresponding to a value of 0.22 mV/deg/s head velocity, centered near zero phase over the range tested from 0.1-10 Hz. The present receptor potential data fall well short of spanning the full range of gain and phase present in the afferent population. Rather, intracellular hair-cell responses are consistent with the frequency-dependent mechanical activation of the transduction current as determined above. 4. Origins of individual afferent responses. The population of afferent responses forms a continuous distribution that is discussed here in terms of three groups as defined by Boyle and Highstein: velocity-sensitive low gain (LG) afferents, velocity/acceleration-sensitive high gain (HG) afferents, and acceleration-sensitive (A) afferents. The response dynamics of individual afferents were found to be determined by a mix of biomechanical and biophysical factors that vary systematically between these afferent groups. All afferents show low-frequency phase advancement and gain decrease during HC indentation associated with the mechanical lower-corner frequency and high-frequency phase and gain enhancements associated with the PTC processing. In highly phase-advanced afferents (A type), the mechanical response is additive with the PTC processing to achieve broad-band acceleration sensitive neural responses.(ABSTRACT TRUNCATED AT 250 WORDS)