A canonical oscillator model of cochlear dynamics.

Nonlinear responses to acoustic signals arise through active processes in the cochlea, which has an exquisite sensitivity and wide dynamic range that can be explained by critical nonlinear oscillations of outer hair cells. Here we ask how the interaction of critical nonlinearities with the basilar membrane and other organ of Corti components could determine tuning properties of the mammalian cochlea. We propose a canonical oscillator model that captures the dynamics of the interaction between the basilar membrane and organ of Corti, using a pair of coupled oscillators for each place along the cochlea. We analyze two models in which a linear oscillator, representing basilar membrane dynamics, is coupled to a nonlinear oscillator poised at a Hopf instability. The coupling in the first model is unidirectional, and that of the second is bidirectional. Parameters are determined by fitting 496 auditory-nerve (AN) tuning curves of macaque monkeys. We find that the unidirectionally and bidirectionally coupled models account equally well for threshold tuning. In addition, however, the bidirectionally coupled model exhibits low-amplitude, spontaneous oscillation in the absence of stimulation, predicting that phase locking will occur before a significant increase in firing frequency, in accordance with well known empirical observations. This leads us to a canonical oscillator cochlear model based on the fundamental principles of critical nonlinear oscillation and coupling dynamics. The model is more biologically realistic than widely used linear or nonlinear filter-based models, yet parsimoniously displays key features of nonlinear mechanistic models. It is efficient enough for computational studies of auditory perception and auditory physiology.