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

  1. Christian Keine  Is a corresponding author
  2. Rudolf Rübsamen
  3. Bernhard Englitz
  1. University of Leipzig, Germany
  2. Radboud University, Netherlands

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.

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8953-2593
  2. Rudolf Rübsamen

    Faculty of Bioscience, Pharmacy and Psychology, University of Leipzig, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. 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.

Reviewing Editor

  1. Ian Winter

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).

Version history

  1. Received: July 3, 2016
  2. Accepted: November 17, 2016
  3. Accepted Manuscript published: November 18, 2016 (version 1)
  4. Version of Record published: December 8, 2016 (version 2)

Copyright

© 2016, Keine et al.

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.

Metrics

  • 2,055
    views
  • 250
    downloads
  • 29
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Christian Keine
  2. Rudolf Rübsamen
  3. Bernhard Englitz
(2016)
Inhibition in the auditory brainstem enhances signal representation and regulates gain in complex acoustic environments
eLife 5:e19295.
https://doi.org/10.7554/eLife.19295

Share this article

https://doi.org/10.7554/eLife.19295

Further reading

    1. Neuroscience
    Katharina Eichler, Stefanie Hampel ... Andrew M Seeds
    Research Advance

    Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.