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

Abstract

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.

Acute and long-term circuit-level effects in the auditory cortex after sound trauma

“…5, right panel) which is in line with the increased activity in the medial geniculate body (MGb) reported after noise exposure (Kalappa et al, 2014). It seems likely that increased thalamic activation of ACx is the result of mechanisms of compensatory, homeostatic plasticity (Mossop et al, 2000;Schaette and Kempter, 2006;Noreña, 2011;Tighilet et al, 2016) or stochastic resonance (Krauss et al, 2016(Krauss et al, , 2018 within the subcortical auditory pathway (Eggermont, 2017a). This conclusion is further supported by our layerspecific analysis, demonstrating that early sink activity in both thalamocortical-recipient layers III/IV and Vb/VIa was significantly increased after recovery (Fig.…”

“…Exposure to high sound levels can severely damage the peripheral sensory receptor epithelia within the cochlea which presents the most reasonable initial factor for such pathological disturbances: Cochlear damage causes altered auditory processing and, in consequence, may lead to compensatory and/or erroneous functional map plasticity in higher sensory brain areas, as for instance the auditory cortex. Such maladaptive map plasticity has been proposed to underlie the development of central tinnitus (Eggermont, 2003;Engineer et al, 2011), although these classical models of tinnitus development have recently been challenged by alternative models (Schaette and Kempter, 2006;Krauss et al, 2016). In humans, as well as in animal models, plastic changes of the tonotopic organization of the auditory cortex (ACx) have been found after noise exposure (Muhlnickel et al, 1998;Eggermont and Komiya, 2000;Dietrich et al, 2001;Norena, 2005;Chen et al, 2016).…”

“…It has been hypothesized that this phenomenon might be explained by selective amplification of previously subthreshold cortical inputs which then provide the major contribution to cortical activation during tinnitus (Irvine, 2018). Other models explain the subcortical enhancement of activations by means of homeostatic plasticity (Schaette and Kempter, 2006;Schaette and McAlpine, 2011) or stochastic resonance (Krauss et al, 2016). Gathering experimental data with respect to the involved specific local and corticocortical synaptic populations in cortex during such plastic adaptations to altered cochlear input is technically challenging and hence still elusive.…”

Prolonged low-level noise-induced plasticity in the peripheral and central auditory system of rats

“…One well accepted theory is homeostatic plasticity, which describes central gain as a neural compensatory mechanism for hearing loss (Auerbach, Rodrigues et al 2014). More recently, computational modeling has suggested that the central gain phenomena may result from stochastic resonance (Krauss, Tziridis et al 2016), a phenomenon where signal intensity is enhanced with the introduction of noise to a system. This phenomenon has been shown to exist within the auditory system of humans (Zeng, Fu et al 2000), and may play a primary role in the response changes observed in the present study.…”

Improved pure tone sensitivity after simulated hearing loss

“…However, until recently the underlying neural processes remained rather elusive. In recent studies, we argued that a processing principle called adaptive stochastic resonance is exploited by the auditory system in order to continuously maintain optimal sensitivity even to highly variable sound pressure levels and changing statistics of the acoustic environment (Krauss et al, 2016;2018). The term stochastic resonance refers to a phenomenon, where a signal of arbitrary kind, which is too weak for a certain sensor for being detected, can be made detectable by adding a random signal, i.e.…”