Mechanisms that degrade timing information in the cochlea

Action potentials of cochlear nerve fibers are synchronized to the temporal variations of sounds, but this synchronization is attenuated for high-frequency sounds. In cochleas from a number of vertebrates, the frequency dependence of synchronization can be represented as a lowpass filter process whose order is at least three (Weiss and Rose, 1988a); i.e. at least three first-order kinetic processes may be responsible for the loss of synchronization. In this paper we assess the extent to which calcium processes, that are essential for chemical transmission at the hair-cell neuron junction, contribute to this attenuation of synchronization. We analyze a model of calcium processes in hair cells (Lewis, 1985; Hudspeth and Lewis, 1988a) for sinusoidal receptor potentials. We show that: (1) the relation between the receptor potential and the calcium current, which is nonlinear, acts approximately as a first-order lowpass filter whose cut-off frequency decreases with increasing receptor potential magnitude; (2) the relation between calcium current and calcium-concentration is a first-order, lowpass filter with constant cutoff frequency. These two calcium processes plus the lowpass-filter process resulting from the electrical resistance and capacitance of the hair-cell membrane - which limits the rate at which the receptor potential can change (Weiss and Rose, 1988b) - can account for much, although perhaps not for all, of the loss of synchronization of cochlear nerve fibers.