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
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.