Stochastic Resonance Controlled Upregulation of Internal Noise after Hearing Loss as a Putative Cause of Tinnitus-Related Neuronal Hyperactivity.

Subjective tinnitus is generally assumed to be a consequence of hearing loss. In animal studies it has been demonstrated that acoustic trauma induced cochlear damage can lead to behavioral signs of tinnitus. In addition it was shown that noise trauma may lead to deafferentation of cochlear inner hair cells (IHC) even in the absence of elevated hearing thresholds, and it seems conceivable that such hidden hearing loss may be sufficient to cause tinnitus. Numerous studies have indicated that tinnitus is correlated with pathologically increased spontaneous firing rates and hyperactivity of neurons along the auditory pathway. It has been proposed that this hyperactivity is the consequence of a mechanism aiming to compensate for reduced input to the auditory system by increasing central neuronal gain, a mechanism referred to as homeostatic plasticity (HP), thereby maintaining mean firing rates over longer timescales for stabilization of neuronal processing. Here we propose an alternative, new interpretation of tinnitus-related development of neuronal hyperactivity in terms of information theory. In particular, we suggest that stochastic resonance (SR) plays a key role in both short- and long-term plasticity within the auditory system and that SR is the primary cause of neuronal hyperactivity and tinnitus. We argue that following hearing loss, SR serves to lift signals above the increased neuronal thresholds, thereby partly compensating for the hearing loss. In our model, the increased amount of internal noise-which is crucial for SR to work-corresponds to neuronal hyperactivity which subsequently causes neuronal plasticity along the auditory pathway and finally may lead to the development of a phantom percept, i.e., subjective tinnitus. We demonstrate the plausibility of our hypothesis using a computational model and provide exemplary findings in human patients that are consistent with that model. Finally we discuss the observed asymmetry in human tinnitus pitch distribution as a consequence of asymmetry of the distribution of auditory nerve type I fibers along the cochlea in the context of our model.