A Temporal Filter for Binaural Hearing Is Dynamically Adjusted by Sound Pressure Level

In natural environments our auditory system is exposed to multiple and diverse signals of fluctuating amplitudes. Therefore, to detect, localize, and single out individual sounds the auditory system has to process and filter spectral and temporal information from both ears. It is known that the over...

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Main Authors: Ida Siveke, Andrea Lingner, Julian J. Ammer, Sarah A. Gleiss, Benedikt Grothe, Felix Felmy
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-02-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fncir.2019.00008/full
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author Ida Siveke
Ida Siveke
Andrea Lingner
Julian J. Ammer
Julian J. Ammer
Sarah A. Gleiss
Sarah A. Gleiss
Benedikt Grothe
Benedikt Grothe
Felix Felmy
Felix Felmy
author_facet Ida Siveke
Ida Siveke
Andrea Lingner
Julian J. Ammer
Julian J. Ammer
Sarah A. Gleiss
Sarah A. Gleiss
Benedikt Grothe
Benedikt Grothe
Felix Felmy
Felix Felmy
author_sort Ida Siveke
collection DOAJ
description In natural environments our auditory system is exposed to multiple and diverse signals of fluctuating amplitudes. Therefore, to detect, localize, and single out individual sounds the auditory system has to process and filter spectral and temporal information from both ears. It is known that the overall sound pressure level affects sensory signal transduction and therefore the temporal response pattern of auditory neurons. We hypothesize that the mammalian binaural system utilizes a dynamic mechanism to adjust the temporal filters in neuronal circuits to different overall sound pressure levels. Previous studies proposed an inhibitory mechanism generated by the reciprocally coupled dorsal nuclei of the lateral lemniscus (DNLL) as a temporal neuronal-network filter that suppresses rapid binaural fluctuations. Here we investigated the consequence of different sound levels on this filter during binaural processing. Our in vivo and in vitro electrophysiology in Mongolian gerbils shows that the integration of ascending excitation and contralateral inhibition defines the temporal properties of this inhibitory filter. The time course of this filter depends on the synaptic drive, which is modulated by the overall sound pressure level and N-methyl-D-aspartate receptor (NMDAR) signaling. In psychophysical experiments we tested the temporal perception of humans and show that detection and localization of two subsequent tones changes with the sound pressure level consistent with our physiological results. Together our data support the hypothesis that mammals dynamically adjust their time window for sound detection and localization within the binaural system in a sound level dependent manner.
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spelling doaj.art-0cddc7aac1de4f94af46f13c595859432022-12-21T21:59:31ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102019-02-011310.3389/fncir.2019.00008427273A Temporal Filter for Binaural Hearing Is Dynamically Adjusted by Sound Pressure LevelIda Siveke0Ida Siveke1Andrea Lingner2Julian J. Ammer3Julian J. Ammer4Sarah A. Gleiss5Sarah A. Gleiss6Benedikt Grothe7Benedikt Grothe8Felix Felmy9Felix Felmy10Department Biology II, Division of Neurobiology, Ludwig-Maximilians-Universität München, Munich, GermanyInstitute of Zoology and Neurobiology, Ruhr-Universität Bochum, Bochum, GermanyDepartment Biology II, Division of Neurobiology, Ludwig-Maximilians-Universität München, Munich, GermanyDepartment Biology II, Division of Neurobiology, Ludwig-Maximilians-Universität München, Munich, GermanyGraduate School for Systemic Neurosciences, Ludwig-Maximilians-Universität München, Munich, GermanyDepartment Biology II, Division of Neurobiology, Ludwig-Maximilians-Universität München, Munich, GermanyGraduate School for Systemic Neurosciences, Ludwig-Maximilians-Universität München, Munich, GermanyDepartment Biology II, Division of Neurobiology, Ludwig-Maximilians-Universität München, Munich, GermanyGraduate School for Systemic Neurosciences, Ludwig-Maximilians-Universität München, Munich, GermanyDepartment Biology II, Division of Neurobiology, Ludwig-Maximilians-Universität München, Munich, GermanyInstitute of Zoology, University of Veterinary Medicine Hannover, Hannover, GermanyIn natural environments our auditory system is exposed to multiple and diverse signals of fluctuating amplitudes. Therefore, to detect, localize, and single out individual sounds the auditory system has to process and filter spectral and temporal information from both ears. It is known that the overall sound pressure level affects sensory signal transduction and therefore the temporal response pattern of auditory neurons. We hypothesize that the mammalian binaural system utilizes a dynamic mechanism to adjust the temporal filters in neuronal circuits to different overall sound pressure levels. Previous studies proposed an inhibitory mechanism generated by the reciprocally coupled dorsal nuclei of the lateral lemniscus (DNLL) as a temporal neuronal-network filter that suppresses rapid binaural fluctuations. Here we investigated the consequence of different sound levels on this filter during binaural processing. Our in vivo and in vitro electrophysiology in Mongolian gerbils shows that the integration of ascending excitation and contralateral inhibition defines the temporal properties of this inhibitory filter. The time course of this filter depends on the synaptic drive, which is modulated by the overall sound pressure level and N-methyl-D-aspartate receptor (NMDAR) signaling. In psychophysical experiments we tested the temporal perception of humans and show that detection and localization of two subsequent tones changes with the sound pressure level consistent with our physiological results. Together our data support the hypothesis that mammals dynamically adjust their time window for sound detection and localization within the binaural system in a sound level dependent manner.https://www.frontiersin.org/article/10.3389/fncir.2019.00008/fulldorsal nucleus of the lateral lemniscussound pressure levelauditory filterglutamate receptorecho perception
spellingShingle Ida Siveke
Ida Siveke
Andrea Lingner
Julian J. Ammer
Julian J. Ammer
Sarah A. Gleiss
Sarah A. Gleiss
Benedikt Grothe
Benedikt Grothe
Felix Felmy
Felix Felmy
A Temporal Filter for Binaural Hearing Is Dynamically Adjusted by Sound Pressure Level
Frontiers in Neural Circuits
dorsal nucleus of the lateral lemniscus
sound pressure level
auditory filter
glutamate receptor
echo perception
title A Temporal Filter for Binaural Hearing Is Dynamically Adjusted by Sound Pressure Level
title_full A Temporal Filter for Binaural Hearing Is Dynamically Adjusted by Sound Pressure Level
title_fullStr A Temporal Filter for Binaural Hearing Is Dynamically Adjusted by Sound Pressure Level
title_full_unstemmed A Temporal Filter for Binaural Hearing Is Dynamically Adjusted by Sound Pressure Level
title_short A Temporal Filter for Binaural Hearing Is Dynamically Adjusted by Sound Pressure Level
title_sort temporal filter for binaural hearing is dynamically adjusted by sound pressure level
topic dorsal nucleus of the lateral lemniscus
sound pressure level
auditory filter
glutamate receptor
echo perception
url https://www.frontiersin.org/article/10.3389/fncir.2019.00008/full
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