Phase Locking of Auditory Nerve Fibers: The Role of Lowpass Filtering by Hair Cells.

Phase locking of auditory-nerve-fiber (ANF) responses to the temporal fine structure of acoustic stimuli, a hallmark of the auditory system's temporal precision, is important for many aspects of hearing. Previous work has shown that phase-locked period histograms are often well described by exponential transfer functions relating instantaneous stimulus pressure to instantaneous spike rate, with no observed clipping of the histograms. The operating points and slopes of these functions change with stimulus level. The mechanism underlying this apparent gain control is unclear but is distinct from mechanical compression, is independent of refractoriness and spike-rate adaptation, and is apparently instantaneous. Here we show that these findings can be accounted for by a model consisting of a static Boltzmann transducer function yielding a clipped output, followed by a lowpass filter and a static exponential transfer function. Using responses to tones of ANFs from cats of both sexes, we show that, for a given ANF, the period histograms obtained at all stimulus levels for a given stimulus frequency can be described using one set of level-independent model parameters. The model also accounts for changes in the maximum and minimum instantaneous spike rates with changes in stimulus level. Notably, the estimated cutoff frequency is lower for low- than for high-spontaneous-rate ANFs, implying a synapse-specific contribution to lowpass filtering. These findings advance our understanding of ANF phase locking by highlighting the role of peripheral filtering mechanisms in shaping responses of individual ANFs.SIGNIFICANCE STATEMENT Phase locking of auditory-nerve-fiber responses to the temporal fine structure of acoustic stimuli is important for many aspects of hearing. Period histograms typically retain an approximately sinusoidal shape across stimulus levels, with the peripheral auditory system operating as though its overall transfer function is an exponential function whose slope decreases with increasing stimulus level. This apparent gain control can be accounted for by a static saturating transducer function followed by a lowpass filter. In addition to attenuating the AC component, the filter approximately recovers the sinusoidal waveform of the stimulus. The estimated cutoff frequency varies with spontaneous rate, revealing a synaptic contribution to lowpass filtering. These findings highlight the significant impact of peripheral filtering mechanisms on phase locking.