Modelling firing regularity in the ventral cochlear nucleus: Mechanisms, and effects of stimulus level and synaptopathy

Abstract

The auditory system processes temporal information at multiple scales, and disruptions to this temporal processing may lead to deficits in auditory tasks such as detecting and discriminating sounds in a noisy environment. Here, a modelling approach is used to study the temporal regularity of firing by chopper cells in the ventral cochlear nucleus, in both the normal and impaired auditory system. Chopper cells, which have a strikingly regular firing response, divide into two classes, sustained and transient, based on the time course of this regularity. Several hypotheses have been proposed to explain the behaviour of chopper cells, and the difference between sustained and transient cells in particular. However, there is no conclusive evidence so far. Here, a reduced mathematical model is developed and used to compare and test a wide range of hypotheses with a limited number of parameters. Simulation results show a continuum of cell types and behaviours: chopper-like behaviour arises for a wide range of parameters, suggesting that multiple mechanisms may underlie this behaviour. The model accounts for systematic trends in regularity as a function of stimulus level that have previously only been reported anecdotally. Finally, the model is used to predict the effects of a reduction in the number of auditory nerve fibres (deafferentation due to, for example, cochlear synaptopathy). An interactive version of this paper in which all the model parameters can be changed is available online.

A two‐path model of auditory modulation detection using temporal fine structure and envelope cues

“…More generally, the effects of age and/or hearing loss modelled here by increases in internal noise (in the E and TFS paths) may correspond to increased spontaneous activity in auditory neurons (Palombi & Caspary, ; Wang et al ., ), increased firing irregularity (Goodman et al ., ), and changes in receptive fields due to the excitatory/inhibitory imbalance (Rajan, ; Scholl & Wehr, ). This excitatory/inhibitory imbalance may, in turn, impair the decoding of both E and/or TFS cues, which may partly depend on precise inhibition between neurons of adjacent frequencies (Shamma, ; Brand et al ., ; Gleich et al ., ; however, see Franken et al ., ).…”

“…following acoustic trauma, Kale & Heinz, 2010), the TFS information at higher stages of the auditory system (e.g. cochlear nucleus, inferior colliculus) might be 'noisier' due to a reduced number of inputs (Goodman et al, 2017). Noisier TFS representation would thus lead to poorer monaural TFS sensitivity, which would in turn impact binaural TFS processing.…”

Sensorineural hearing loss impairs sensitivity but spares temporal integration for detection of frequency modulation

“…The ability to use temporal-envelope cues may be reduced in the impaired auditory system because of (1) reduced conversion of FM into temporal-envelope cues at the outputs of the cochlear filters, resulting from the loss of outer hair cells in the cochlea and the consequent broadening of the filters (Glasberg and Moore, 1986); (2) loss of auditory-nerve fibers (Kujawa and Liberman, 2009) and the consequent impoverished (i.e., more noisy) neural representation of temporal-envelope cues in the early auditory system, as suggested by the psychophysical, electrophysiological and modeling work of Bharadwaj et al (2015), Goodman et al (2017), and Paul et al (2017); (3) central changes, such as a loss of inhibition, which may affect envelope extraction and processing (Davis et al, 2010).…”

General neural mechanisms can account for rising slope preference in localization of ambiguous sounds

“…In Population mechanisms, we investigate these population level effects with a lateral inhibition mechanism. Throughout, we use abstract rate models of neurons with rich dynamics to extract the essential details while keeping the model complexity manageable (similarly to Goodman et al 2017). This enables us to investigate how the behaviour of the model depends on all of the parameters and plot the parameter spaces, which would not be possible with a biophysically detailed model with a large number of parameters.…”

“…We therefore strongly encourage researchers to investigate the extent to which new experimental results can be reproduced using simple and general models, and thoroughly explore the parameter space in detail along the lines suggested by O'Leary et al (2015) and used previously in the auditory system in Goodman et al (2017).…”