Neuronal Avalanches in Input and Associative Layers of Auditory Cortex

The primary auditory cortex processes acoustic sequences for the perception of behaviorally meaningful sounds such as speech. Sound information arrives at its input layer four from where activity propagates to associative layer 2/3. It is currently not known whether there is a characteristic organiz...

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Main Authors: Zac Bowen, Daniel E. Winkowski, Saurav Seshadri, Dietmar Plenz, Patrick O. Kanold
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnsys.2019.00045/full
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spelling doaj-b573e28bfa9149eaade773cb32ff9d7c2020-11-25T01:46:44ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372019-09-011310.3389/fnsys.2019.00045477874Neuronal Avalanches in Input and Associative Layers of Auditory CortexZac Bowen0Daniel E. Winkowski1Daniel E. Winkowski2Saurav Seshadri3Dietmar Plenz4Patrick O. Kanold5Patrick O. Kanold6Department of Biology, University of Maryland, College Park, College Park, MD, United StatesDepartment of Biology, University of Maryland, College Park, College Park, MD, United StatesInstitute for Systems Research, University of Maryland, College Park, College Park, MD, United StatesSection on Critical Brain Dynamics, National Institute of Mental Health, Bethesda, MD, United StatesSection on Critical Brain Dynamics, National Institute of Mental Health, Bethesda, MD, United StatesDepartment of Biology, University of Maryland, College Park, College Park, MD, United StatesInstitute for Systems Research, University of Maryland, College Park, College Park, MD, United StatesThe primary auditory cortex processes acoustic sequences for the perception of behaviorally meaningful sounds such as speech. Sound information arrives at its input layer four from where activity propagates to associative layer 2/3. It is currently not known whether there is a characteristic organization of neuronal population activity across layers and sound levels during sound processing. Here, we identify neuronal avalanches, which in theory and experiments have been shown to maximize dynamic range and optimize information transfer within and across networks, in primary auditory cortex. We used in vivo 2-photon imaging of pyramidal neurons in cortical layers L4 and L2/3 of mouse A1 to characterize the populations of neurons that were active spontaneously, i.e., in the absence of a sound stimulus, and those recruited by single-frequency tonal stimuli at different sound levels. Single-frequency sounds recruited neurons of widely ranging frequency selectivity in both layers. We defined neuronal ensembles as neurons being active within or during successive temporal windows at the temporal resolution of our imaging. For both layers, neuronal ensembles were highly variable in size during spontaneous activity as well as during sound presentation. Ensemble sizes distributed according to power laws, the hallmark of neuronal avalanches, and were similar across sound levels. Avalanches activated by sound were composed of neurons with diverse tuning preference, yet with selectivity independent of avalanche size. Our results suggest that optimization principles identified for avalanches guide population activity in L4 and L2/3 of auditory cortex during and in-between stimulus processing.https://www.frontiersin.org/article/10.3389/fnsys.2019.00045/fullauditory cortexmouseavalanchepatternpopulationimaging
collection DOAJ
language English
format Article
sources DOAJ
author Zac Bowen
Daniel E. Winkowski
Daniel E. Winkowski
Saurav Seshadri
Dietmar Plenz
Patrick O. Kanold
Patrick O. Kanold
spellingShingle Zac Bowen
Daniel E. Winkowski
Daniel E. Winkowski
Saurav Seshadri
Dietmar Plenz
Patrick O. Kanold
Patrick O. Kanold
Neuronal Avalanches in Input and Associative Layers of Auditory Cortex
Frontiers in Systems Neuroscience
auditory cortex
mouse
avalanche
pattern
population
imaging
author_facet Zac Bowen
Daniel E. Winkowski
Daniel E. Winkowski
Saurav Seshadri
Dietmar Plenz
Patrick O. Kanold
Patrick O. Kanold
author_sort Zac Bowen
title Neuronal Avalanches in Input and Associative Layers of Auditory Cortex
title_short Neuronal Avalanches in Input and Associative Layers of Auditory Cortex
title_full Neuronal Avalanches in Input and Associative Layers of Auditory Cortex
title_fullStr Neuronal Avalanches in Input and Associative Layers of Auditory Cortex
title_full_unstemmed Neuronal Avalanches in Input and Associative Layers of Auditory Cortex
title_sort neuronal avalanches in input and associative layers of auditory cortex
publisher Frontiers Media S.A.
series Frontiers in Systems Neuroscience
issn 1662-5137
publishDate 2019-09-01
description The primary auditory cortex processes acoustic sequences for the perception of behaviorally meaningful sounds such as speech. Sound information arrives at its input layer four from where activity propagates to associative layer 2/3. It is currently not known whether there is a characteristic organization of neuronal population activity across layers and sound levels during sound processing. Here, we identify neuronal avalanches, which in theory and experiments have been shown to maximize dynamic range and optimize information transfer within and across networks, in primary auditory cortex. We used in vivo 2-photon imaging of pyramidal neurons in cortical layers L4 and L2/3 of mouse A1 to characterize the populations of neurons that were active spontaneously, i.e., in the absence of a sound stimulus, and those recruited by single-frequency tonal stimuli at different sound levels. Single-frequency sounds recruited neurons of widely ranging frequency selectivity in both layers. We defined neuronal ensembles as neurons being active within or during successive temporal windows at the temporal resolution of our imaging. For both layers, neuronal ensembles were highly variable in size during spontaneous activity as well as during sound presentation. Ensemble sizes distributed according to power laws, the hallmark of neuronal avalanches, and were similar across sound levels. Avalanches activated by sound were composed of neurons with diverse tuning preference, yet with selectivity independent of avalanche size. Our results suggest that optimization principles identified for avalanches guide population activity in L4 and L2/3 of auditory cortex during and in-between stimulus processing.
topic auditory cortex
mouse
avalanche
pattern
population
imaging
url https://www.frontiersin.org/article/10.3389/fnsys.2019.00045/full
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