Abstract

Inhibition plays a crucial role in neural signal processing, shaping and limiting responses. In the auditory system, inhibition already modulates second order neurons in the cochlear nucleus, e.g. spherical bushy cells (SBCs). While the physiological basis of inhibition and excitation is well described, their functional interaction in signal processing remains elusive. Using a combination of in vivo loose-patch recordings, iontophoretic drug application, and detailed signal analysis in the Mongolian Gerbil, we demonstrate that inhibition is widely co-tuned with excitation, and leads only to minor sharpening of the spectral response properties. Combinations of complex stimuli and neuronal input-output analysis based on spectrotemporal receptive fields revealed inhibition to render the neuronal output temporally sparser and more reproducible than the input. Overall, inhibition plays a central role in improving the temporal response fidelity of SBCs across a wide range of input intensities and thereby provides the basis for high-fidelity signal processing.

Highlights

  • Dynamic processing in neural networks is controlled by an interplay of excitation and inhibition

  • This study aimed for an investigation of sound-evoked inhibition on the processing of complex structured signals at the auditory nerve-to-spherical bushy cell synapse (ANF-spherical bushy cells (SBCs))

  • A total of 85 units were recorded from the rostral pole of the anteroventral cochlear nucleus (AVCN), the location of large, low-frequency coding SBCs (Bazwinsky et al, 2008)

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Summary

Introduction

Dynamic processing in neural networks is controlled by an interplay of excitation and inhibition. The dominant excitatory neurons interact reciprocally with inhibitory neurons, which serve key functions in shaping the responses (reviewed in Isaacson and Scanziani, 2011). Wehr and Zador, 2003; Renart et al, 2010) that serves to shape and accelerate network dynamics. In other modalities, inhibition was found to be co-tuned with excitation in the cortex, typically with a wider tuning, generating the well-described inhibitory sidebands (auditory: Wang et al, 2002; Wu et al, 2008, visual: Sohya et al, 2007; Niell and Stryker, 2008; Liu et al, 2009, 2011; Katzner et al, 2011, olfactory: Poo and Isaacson, 2009). Various studies have shown prominent inhibitory influences on signal processing in the cochlear nucleus (Caspary et al, 1994; Kopp-Scheinpflug et al, 2002; Gai and Carney, 2008), in the medial and lateral superior olive (Grothe and Sanes, 1993; Brand et al, 2002; Myoga et al, 2014), and in the dorsal and ventral nuclei of the lateral lemniscus (Yang and Pollak, 1994, 1998; Burger and Pollak, 2001; Nayagam et al, 2005; Pecka et al, 2007; Spencer et al, 2015)

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