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Surround suppression in mouse auditory cortex underlies auditory edge detection

Surround suppression (SS) is a fundamental property of sensory processing throughout the brain. In the auditory system, the early processing stream encodes sounds using a one dimensional physical space—frequency. Previous studies in the auditory system have shown SS to manifest as bandwidth tuning a...

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Autores principales: Gilday, Omri David, Praegel, Benedikt, Maor, Ido, Cohen, Tav, Nelken, Israel, Mizrahi, Adi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9888713/
https://www.ncbi.nlm.nih.gov/pubmed/36656876
http://dx.doi.org/10.1371/journal.pcbi.1010861
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author Gilday, Omri David
Praegel, Benedikt
Maor, Ido
Cohen, Tav
Nelken, Israel
Mizrahi, Adi
author_facet Gilday, Omri David
Praegel, Benedikt
Maor, Ido
Cohen, Tav
Nelken, Israel
Mizrahi, Adi
author_sort Gilday, Omri David
collection PubMed
description Surround suppression (SS) is a fundamental property of sensory processing throughout the brain. In the auditory system, the early processing stream encodes sounds using a one dimensional physical space—frequency. Previous studies in the auditory system have shown SS to manifest as bandwidth tuning around the preferred frequency. We asked whether bandwidth tuning can be found around frequencies away from the preferred frequency. We exploited the simplicity of spectral representation of sounds to study SS by manipulating both sound frequency and bandwidth. We recorded single unit spiking activity from the auditory cortex (ACx) of awake mice in response to an array of broadband stimuli with varying central frequencies and bandwidths. Our recordings revealed that a significant portion of neuronal response profiles had a preferred bandwidth that varied in a regular way with the sound’s central frequency. To gain insight into the possible mechanism underlying these responses, we modelled neuronal activity using a variation of the “Mexican hat” function often used to model SS. The model accounted for response properties of single neurons with high accuracy. Our data and model show that these responses in ACx obey simple rules resulting from the presence of lateral inhibitory sidebands, mostly above the excitatory band of the neuron, that result in sensitivity to the location of top frequency edges, invariant to other spectral attributes. Our work offers a simple explanation for auditory edge detection and possibly other computations of spectral content in sounds.
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spelling pubmed-98887132023-02-01 Surround suppression in mouse auditory cortex underlies auditory edge detection Gilday, Omri David Praegel, Benedikt Maor, Ido Cohen, Tav Nelken, Israel Mizrahi, Adi PLoS Comput Biol Research Article Surround suppression (SS) is a fundamental property of sensory processing throughout the brain. In the auditory system, the early processing stream encodes sounds using a one dimensional physical space—frequency. Previous studies in the auditory system have shown SS to manifest as bandwidth tuning around the preferred frequency. We asked whether bandwidth tuning can be found around frequencies away from the preferred frequency. We exploited the simplicity of spectral representation of sounds to study SS by manipulating both sound frequency and bandwidth. We recorded single unit spiking activity from the auditory cortex (ACx) of awake mice in response to an array of broadband stimuli with varying central frequencies and bandwidths. Our recordings revealed that a significant portion of neuronal response profiles had a preferred bandwidth that varied in a regular way with the sound’s central frequency. To gain insight into the possible mechanism underlying these responses, we modelled neuronal activity using a variation of the “Mexican hat” function often used to model SS. The model accounted for response properties of single neurons with high accuracy. Our data and model show that these responses in ACx obey simple rules resulting from the presence of lateral inhibitory sidebands, mostly above the excitatory band of the neuron, that result in sensitivity to the location of top frequency edges, invariant to other spectral attributes. Our work offers a simple explanation for auditory edge detection and possibly other computations of spectral content in sounds. Public Library of Science 2023-01-19 /pmc/articles/PMC9888713/ /pubmed/36656876 http://dx.doi.org/10.1371/journal.pcbi.1010861 Text en © 2023 Gilday et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Gilday, Omri David
Praegel, Benedikt
Maor, Ido
Cohen, Tav
Nelken, Israel
Mizrahi, Adi
Surround suppression in mouse auditory cortex underlies auditory edge detection
title Surround suppression in mouse auditory cortex underlies auditory edge detection
title_full Surround suppression in mouse auditory cortex underlies auditory edge detection
title_fullStr Surround suppression in mouse auditory cortex underlies auditory edge detection
title_full_unstemmed Surround suppression in mouse auditory cortex underlies auditory edge detection
title_short Surround suppression in mouse auditory cortex underlies auditory edge detection
title_sort surround suppression in mouse auditory cortex underlies auditory edge detection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9888713/
https://www.ncbi.nlm.nih.gov/pubmed/36656876
http://dx.doi.org/10.1371/journal.pcbi.1010861
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