Principal cells of the brainstem's interaural sound level detector are temporal differentiators rather than integrators

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Abstract

The brainstem's lateral superior olive (LSO) is thought to be crucial for localizing high-frequency sounds by coding interaural sound level differences (ILD). Its neurons weigh contralateral inhibition against ipsilateral excitation, making their firing rate a function of the azimuthal position of a sound source. Since the very first in vivo recordings, LSO principal neurons have been reported to give sustained and temporally integrating 'chopper' responses to sustained sounds. Neurons with transient responses were observed but largely ignored and even considered a sign of pathology. Using the Mongolian gerbil as a model system, we have obtained the first in vivo patch clamp recordings from labeled LSO neurons and find that principal LSO neurons, the most numerous projection neurons of this nucleus, only respond at sound onset and show fast membrane features suggesting an importance for timing. These results provide a new framework to interpret previously puzzling features of this circuit.

Data availability

As stated in the Transparent Reporting Form, MATLAB figures with embedded data have been made publicly available on Figshare (https://doi.org/10.6084/m9.figshare.6493409).

The following data sets were generated

1. Tom P Franken Philip X Joris Philip H Smith
(2018) MATLAB figures for the article
Available on Figshare under a Creative Commons Attribution 4.0 International License (CC BY 4.0).

https://doi.org/10.6084/m9.figshare.6493409

Article and author information

Author details

Tom P Franken

Laboratory of Auditory Neurophysiology, KU Leuven, Leuven, Belgium

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7160-5152
Philip X Joris

Laboratory of Auditory Neurophysiology, KU Leuven, Leuven, Belgium

For correspondence
Philip.Joris@med.kuleuven.be

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9759-5375
Philip H Smith

Department of Neuroscience, University of Wisconsin-Madison, Madison, United States

Competing interests
The authors declare that no competing interests exist.

Funding

Fonds Wetenschappelijk Onderzoek (Ph.D. fellowship)

Tom P Franken

National Institute on Deafness and Other Communication Disorders (R01 grant DC006212)

Philip X Joris
Philip H Smith

Bijzonder Onderzoeksfonds (OT-14-118)

Philip X Joris

Fonds Wetenschappelijk Onderzoek (G.0961.11)

Philip X Joris

Fonds Wetenschappelijk Onderzoek (G.0A11.13)

Philip X Joris

Fonds Wetenschappelijk Onderzoek (G.091214N)

Philip X Joris

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All procedures were approved by the KU Leuven Ethics Committee for Animal Experiments (protocol numbers P155/2008, P123/2010, P167/2012, P123/2013, P005/2014).

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.