DETERMINANTS OF SEMICIRCULAR CANAL AFFERENT RESPONSE DYNAMICS IN THE TOADFISH, OPSANUS-TAU

Citation
Sm. Highstein et al., DETERMINANTS OF SEMICIRCULAR CANAL AFFERENT RESPONSE DYNAMICS IN THE TOADFISH, OPSANUS-TAU, Journal of neurophysiology, 75(2), 1996, pp. 575-596
Citations number
57
Categorie Soggetti
Neurosciences,Physiology,Neurosciences,Physiology
Journal title
ISSN journal
00223077
Volume
75
Issue
2
Year of publication
1996
Pages
575 - 596
Database
ISI
SICI code
0022-3077(1996)75:2<575:DOSCAR>2.0.ZU;2-#
Abstract
1. Present results determine the relative contributions of the biomech anical and the posttransduction-current (PTC) mechanisms to the sensor y 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 affere nt responses elicited by electrical stimuli and mechanical HC indentat ion. Individual afferent response dynamics are defined here using firs t-harmonic transfer functions presented in the form of response gain a nd phase for sinusoidal stimuli from similar to 0.02-30 Hz. Comparison of the response dynamics for the two types of stimuli distinguishes t he mechanical and the PTC transfer functions leading to the neural res ponse. 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 e ndolymphatic potential by current injection induces a differential vol tage across the apical face of the hair cells that drives the transduc tion current directly via the Nernst-Planck potential. Results show th at the electrical impedance of the apical tight junctions is much larg er than the basal impedance to ground in O. tau, such that leakage cur rent to the basolateral space is negligible and the voltage-sensitive basolateral currents remain fully functional during polarization of th e endolymph (in the frequency range tested). Extracellular afferent re sponses to endolymphatic polarization were combined with responses to HC indentation to separate the relative contributions of the mechanica l and the PTC mechanisms to the overall afferent response dynamics. Da ta show that more than one-half of the overall signal processing, as d efined by the first-harmonic transfer function, persists even when can al mechanics is bypassed. 3. Hair-cell receptor potential modulation d uring HC indentation. Sharp microelectrodes were used to record the mo dulation of hair-cell receptor potentials (intracellular voltages) in vivo during physiological levels of sinusoidal HC indentation. Recepto r potentials exhibit modulations dominated by the first harmonic and c entered about the resting potential. The average gain of the receptor- potential modulation for HC indentation is similar to 0.88 mV/mu m ind ent, 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 rec eptor potential data fall well short of spanning the full range of gai n and phase present in the afferent population. Rather, intracellular hair-cell responses are consistent with the frequency-dependent mechan ical activation of the transduction current as determined above. 4. Or igins of individual afferent responses. The population of afferent res ponses 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 (H G) afferents, and acceleration-sensitive (A) afferents. The response d ynamics of individual afferents were found to be determined by a mix o f biomechanical and biophysical factors that vary systematically betwe en these afferent groups. All afferents show low-frequency phase advan cement and gain decrease during HC indentation associated with the mec hanical lower-corner frequency and high-frequency phase and gain enhan cements associated with the PTC processing. In highly phase-advanced a fferents (A type), the mechanical response is additive with the PTC pr ocessing to achieve broad-band acceleration sensitive neural responses . In afferents having little or no phase advance (LG type), phase reta rdation >2 Hz in the mechanics cancels posttransduction-current phase advance to achieve broad-band velocity-sensitive responses. Most affer ents (including HG type) fall between the two extremes defined by LG a nd A.