Single unit activity was recorded in the auditory nerves of chinchillas. Period histograms were constructed for responses to tones with frequencies 30–1000 Hz. For low‐frequency tones at near‐threshold levels, peak period histogram phases for low‐ and medium‐best‐frequency (BF) neurons (≤3 kHz) ranged from synchronous with condensation at the eardrum to 90° leading it. At near‐threshold (but high absolute) levels, high‐BF (≥8 kHz) neurons responded in phase with rarefaction. At even higher levels, period histograms for responses of high‐BF neurons tended to become bimodal, with one of the modes lagging rarefaction by 90°. Using cochlear microphonics as an indicator of basilar membrane (BM) displacement, at threshold levels, response phase of low‐ and medium‐BF neurons fall within a range between displacement and velocity of the BM toward scala vestibuli. High‐BF neurons respond, at threshold (but high) intensities, in phase with BM displacement toward scala tympani. The rates of growth of frequency sensitivity in responses of low‐BF (+18 dB/oct) and high‐BF (+12 dB/oct) neurons are consistent with preferred response phases corresponding to BM SV velocity and ST displacement, respectively. At supra‐threshold levels high‐BF neurons may fire preferentially to both scala tympani displacement and scala vestibuli velocity. These results support the notion that, for high‐intensity, low‐frequency stimuli, OHC hyperpolarization can induce excitation of the dendrites innervating IHCs.