Stochastic resonance controlled upregulation of internal noise after hearing loss as a putative correlate of tinnitus-related neuronal hyperactivity

Subjective tinnitus (ST) is generally assumed to be a consequence of hearing loss (HL). In animal studies acoustic trauma can lead to behavioral signs of ST, in human studies ST patients without increased hearing thresholds were found to suffer from so called hidden HL. Additionally, ST is correlated with pathologically increased spontaneous firing rates and neuronal hyperactivity (NH) along the auditory pathway. Homeostatic plasticity (HP) has been proposed as a compensation mechanism leading to the development of NH, arguing that after HL initially decreased mean firing rates of neurons are subsequently restored by increased spontaneous rates. However all HP models fundamentally lack explanatory power since the function of keeping mean firing rate constant remains elusive as does the benefit this might have in terms of information processing. Furthermore the neural circuitry being able to perform the comparison of preferred with actual mean firing rate remains unclear. Here we propose an entirely new interpretation of ST related development of NH in terms of information theory. We suggest that stochastic resonance (SR) plays a key role in short- and long-term plasticity within the auditory system and is the ultimate cause of NH and ST. SR has been found ubiquitous in neuroscience and refers to the phenomenon that sub-threshold, unperceivable signals can be transmitted by adding noise to sensor input. We argue that after HL, SR serves to lift signals above the increased hearing threshold, hence subsequently decreasing thresholds again. The increased amount of internal noise is the correlate of the NH, which finally leads to the development of ST, due to neuronal plasticity along the auditory pathway. We demonstrate the plausibility of our hypothesis by using a computational model and provide exemplarily findings of human and animal studies that are consistent with our model.