Dynamical instability determines the effect of ongoing noise on neural firing

At low stimulation rates, electrically stimulated auditory nerve fibers typically fire regularly, in lock-step to the applied stimulus. At high stimulation rates, however, these same fibers fire irregularly. Firing irregularity has been attributed to the random opening and closing of voltage-gated sodium channels at the spike generation site. We demonstrate, however, that the nonlinear dynamics of neural excitation and refractoriness embodied in the FitzHugh-Nagumo (FN) model produce realistic firing irregularity at high stimulus rates, even in the complete absence of ongoing physiological noise. Indeed, we show that ongoing noise can actually regularize the response at low discharge rates. The degree of stimulus-dependent irregularity is determined not so much by the level of ongoing physiological noise as by the dynamical instability. Our work suggests that the dynamical instability, quantified by the Lyapunov exponent, controls neural sensitivity to input signals and to physiological noise, as well the amount of mutual desynchronization between similarly stimulated fibers. This instability, quantified by the value of the Lyapunov exponent, may play a critical role in determining modulation sensitivity and dynamic range in cochlear implants.