Inhibition in the auditory brainstem enhances signal representation and regulates gain in complex acoustic environments

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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 preserving or even improving temporal response fidelity of SBCs across a wide range of input intensities and thereby provides the basis for high-fidelity signal processing.

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Christian Keine

Faculty of Bioscience, Pharmacy and Psychology, University of Leipzig, Leipzig, Germany

For correspondence
christian.keine@gmail.com

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8953-2593
Rudolf Rübsamen

Faculty of Bioscience, Pharmacy and Psychology, University of Leipzig, Leipzig, Germany

Competing interests
The authors declare that no competing interests exist.
Bernhard Englitz

Department of Neurophysiology, Donders Center for Neuroscience, Radboud University, Nijmegen, Netherlands

Competing interests
The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (GRK 1097)

Christian Keine

European Commission (Marie Sklodowska Curie Fellowship 660328)

Bernhard Englitz

Deutsche Forschungsgemeinschaft (RU 390/19-1)

Rudolf Rübsamen

Deutsche Forschungsgemeinschaft (RU 390/20-1)

Rudolf Rübsamen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments were approved by the Saxonian District Government, Leipzig (TVV 06/09), and conducted according to the European Communities Council Directive (86/609/EEC).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.