Noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake mice

Sound location coding has been extensively studied at the central nucleus of the mammalian inferior colliculus (CNIC), supporting a population code. However, this population code has not been extensively characterized on the single-trial level with simultaneous recordings or at other anatomical regi...

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Main Authors: Juan Carlos Boffi, Brice Bathellier, Hiroki Asari, Robert Prevedel
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-11-01
Series:eLife
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Online Access:https://elifesciences.org/articles/97598
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author Juan Carlos Boffi
Brice Bathellier
Hiroki Asari
Robert Prevedel
author_facet Juan Carlos Boffi
Brice Bathellier
Hiroki Asari
Robert Prevedel
author_sort Juan Carlos Boffi
collection DOAJ
description Sound location coding has been extensively studied at the central nucleus of the mammalian inferior colliculus (CNIC), supporting a population code. However, this population code has not been extensively characterized on the single-trial level with simultaneous recordings or at other anatomical regions like the dorsal cortex of inferior colliculus (DCIC), which is relevant for learning-induced experience dependent plasticity. To address these knowledge gaps, here we made in two complementary ways large-scale recordings of DCIC populations from awake mice in response to sounds delivered from 13 different frontal horizontal locations (azimuths): volumetric two-photon calcium imaging with ~700 cells simultaneously recorded at a relatively low temporal resolution, and high-density single-unit extracellular recordings with ~20 cells simultaneously recorded at a high temporal resolution. Independent of the method, the recorded DCIC population responses revealed substantial trial-to-trial variation (neuronal noise) which was significantly correlated across pairs of neurons (noise correlations) in the passively listening condition. Nevertheless, decoding analysis supported that these noisy response patterns encode sound location on the single-trial basis, reaching errors that match the discrimination ability of mice. The detected noise correlations contributed to minimize the error of the DCIC population code of sound azimuth. Altogether these findings point out that DCIC can encode sound location in a similar format to what has been proposed for CNIC, opening exciting questions about how noise correlations could shape this code in the context of cortico-collicular input and experience-dependent plasticity.
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spelling doaj-art-997e7310e8da4ad2980ecfba38e9196b2024-11-25T16:25:06ZengeLife Sciences Publications LtdeLife2050-084X2024-11-011310.7554/eLife.97598Noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake miceJuan Carlos Boffi0https://orcid.org/0000-0002-0116-6892Brice Bathellier1https://orcid.org/0000-0001-9211-1960Hiroki Asari2https://orcid.org/0000-0003-3396-1935Robert Prevedel3https://orcid.org/0000-0003-3366-4703Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany; Epigenetics and Neurobiology Unit, European Molecular Biology Laboratory, Monterotondo, ItalyUniversité Paris Cité, Institut Pasteur, AP-HP, Inserm, Fondation Pour l'Audition, Institut de l’Audition, IHU reConnect, Paris, FranceEpigenetics and Neurobiology Unit, European Molecular Biology Laboratory, Monterotondo, ItalyCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany; Epigenetics and Neurobiology Unit, European Molecular Biology Laboratory, Monterotondo, Italy; Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany; Molecular Medicine Partnership Unit, European Molecular Biology Laboratory, Heidelberg, Germany; Interdisciplinary Center for Neurosciences, Heidelberg University, Heidelberg, GermanySound location coding has been extensively studied at the central nucleus of the mammalian inferior colliculus (CNIC), supporting a population code. However, this population code has not been extensively characterized on the single-trial level with simultaneous recordings or at other anatomical regions like the dorsal cortex of inferior colliculus (DCIC), which is relevant for learning-induced experience dependent plasticity. To address these knowledge gaps, here we made in two complementary ways large-scale recordings of DCIC populations from awake mice in response to sounds delivered from 13 different frontal horizontal locations (azimuths): volumetric two-photon calcium imaging with ~700 cells simultaneously recorded at a relatively low temporal resolution, and high-density single-unit extracellular recordings with ~20 cells simultaneously recorded at a high temporal resolution. Independent of the method, the recorded DCIC population responses revealed substantial trial-to-trial variation (neuronal noise) which was significantly correlated across pairs of neurons (noise correlations) in the passively listening condition. Nevertheless, decoding analysis supported that these noisy response patterns encode sound location on the single-trial basis, reaching errors that match the discrimination ability of mice. The detected noise correlations contributed to minimize the error of the DCIC population code of sound azimuth. Altogether these findings point out that DCIC can encode sound location in a similar format to what has been proposed for CNIC, opening exciting questions about how noise correlations could shape this code in the context of cortico-collicular input and experience-dependent plasticity.https://elifesciences.org/articles/97598sound localizationinferior colliculuspopulation codenoise correlations
spellingShingle Juan Carlos Boffi
Brice Bathellier
Hiroki Asari
Robert Prevedel
Noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake mice
eLife
sound localization
inferior colliculus
population code
noise correlations
title Noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake mice
title_full Noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake mice
title_fullStr Noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake mice
title_full_unstemmed Noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake mice
title_short Noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake mice
title_sort noisy neuronal populations effectively encode sound localization in the dorsal inferior colliculus of awake mice
topic sound localization
inferior colliculus
population code
noise correlations
url https://elifesciences.org/articles/97598
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AT hirokiasari noisyneuronalpopulationseffectivelyencodesoundlocalizationinthedorsalinferiorcolliculusofawakemice
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