Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical Circuits

Summary: Natural sounds have rich spectrotemporal dynamics. Spectral information is spatially represented in the auditory cortex (ACX) via large-scale maps. However, the representation of temporal information, e.g., sound offset, is unclear. We perform multiscale imaging of neuronal and thalamic act...

Full description

Bibliographic Details
Main Authors: Ji Liu, Matthew R. Whiteway, Alireza Sheikhattar, Daniel A. Butts, Behtash Babadi, Patrick O. Kanold
Format: Article
Language:English
Published: Elsevier 2019-04-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124719303997
_version_ 1818914629838962688
author Ji Liu
Matthew R. Whiteway
Alireza Sheikhattar
Daniel A. Butts
Behtash Babadi
Patrick O. Kanold
author_facet Ji Liu
Matthew R. Whiteway
Alireza Sheikhattar
Daniel A. Butts
Behtash Babadi
Patrick O. Kanold
author_sort Ji Liu
collection DOAJ
description Summary: Natural sounds have rich spectrotemporal dynamics. Spectral information is spatially represented in the auditory cortex (ACX) via large-scale maps. However, the representation of temporal information, e.g., sound offset, is unclear. We perform multiscale imaging of neuronal and thalamic activity evoked by sound onset and offset in awake mouse ACX. ACX areas differed in onset responses (On-Rs) and offset responses (Off-Rs). Most excitatory L2/3 neurons show either On-Rs or Off-Rs, and ACX areas are characterized by differing fractions of On and Off-R neurons. Somatostatin and parvalbumin interneurons show distinct temporal dynamics, potentially amplifying Off-Rs. Functional network analysis shows that ACX areas contain distinct parallel onset and offset networks. Thalamic (MGB) terminals show either On-Rs or Off-Rs, indicating a thalamic origin of On and Off-R pathways. Thus, ACX areas spatially represent temporal features, and this representation is created by spatial convergence and co-activation of distinct MGB inputs and is refined by specific intracortical connectivity. : Using multiscale imaging of mouse auditory cortices, Liu et al. found that the offset response is tonotopically organized and spatially extensive across auditory fields, while A1 L2/3 pyramidal neurons process tone onset and offset in parallel networks. The offset response is amplified by differential convergence of thalamic input and intracortical processing involving interneurons. Keywords: auditory cortex, mouse, temporal, pattern, MGB, two-photon imaging
first_indexed 2024-12-19T23:49:26Z
format Article
id doaj.art-6be12f8f7eed4603bd42b45222a2620b
institution Directory Open Access Journal
issn 2211-1247
language English
last_indexed 2024-12-19T23:49:26Z
publishDate 2019-04-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj.art-6be12f8f7eed4603bd42b45222a2620b2022-12-21T20:01:12ZengElsevierCell Reports2211-12472019-04-01273872885.e7Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical CircuitsJi Liu0Matthew R. Whiteway1Alireza Sheikhattar2Daniel A. Butts3Behtash Babadi4Patrick O. Kanold5Department of Biology, University of Maryland, College Park, MD 20742, USAApplied Mathematics and Statistics and Scientific Computation Program, University of Maryland, College Park, MD 20742, USADepartment of Electrical & Computer Engineering, University of Maryland, College Park, MD 20742, USADepartment of Biology, University of Maryland, College Park, MD 20742, USA; Applied Mathematics and Statistics and Scientific Computation Program, University of Maryland, College Park, MD 20742, USA; Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD 20742, USADepartment of Electrical & Computer Engineering, University of Maryland, College Park, MD 20742, USADepartment of Biology, University of Maryland, College Park, MD 20742, USA; Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD 20742, USA; Corresponding authorSummary: Natural sounds have rich spectrotemporal dynamics. Spectral information is spatially represented in the auditory cortex (ACX) via large-scale maps. However, the representation of temporal information, e.g., sound offset, is unclear. We perform multiscale imaging of neuronal and thalamic activity evoked by sound onset and offset in awake mouse ACX. ACX areas differed in onset responses (On-Rs) and offset responses (Off-Rs). Most excitatory L2/3 neurons show either On-Rs or Off-Rs, and ACX areas are characterized by differing fractions of On and Off-R neurons. Somatostatin and parvalbumin interneurons show distinct temporal dynamics, potentially amplifying Off-Rs. Functional network analysis shows that ACX areas contain distinct parallel onset and offset networks. Thalamic (MGB) terminals show either On-Rs or Off-Rs, indicating a thalamic origin of On and Off-R pathways. Thus, ACX areas spatially represent temporal features, and this representation is created by spatial convergence and co-activation of distinct MGB inputs and is refined by specific intracortical connectivity. : Using multiscale imaging of mouse auditory cortices, Liu et al. found that the offset response is tonotopically organized and spatially extensive across auditory fields, while A1 L2/3 pyramidal neurons process tone onset and offset in parallel networks. The offset response is amplified by differential convergence of thalamic input and intracortical processing involving interneurons. Keywords: auditory cortex, mouse, temporal, pattern, MGB, two-photon imaginghttp://www.sciencedirect.com/science/article/pii/S2211124719303997
spellingShingle Ji Liu
Matthew R. Whiteway
Alireza Sheikhattar
Daniel A. Butts
Behtash Babadi
Patrick O. Kanold
Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical Circuits
Cell Reports
title Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical Circuits
title_full Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical Circuits
title_fullStr Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical Circuits
title_full_unstemmed Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical Circuits
title_short Parallel Processing of Sound Dynamics across Mouse Auditory Cortex via Spatially Patterned Thalamic Inputs and Distinct Areal Intracortical Circuits
title_sort parallel processing of sound dynamics across mouse auditory cortex via spatially patterned thalamic inputs and distinct areal intracortical circuits
url http://www.sciencedirect.com/science/article/pii/S2211124719303997
work_keys_str_mv AT jiliu parallelprocessingofsounddynamicsacrossmouseauditorycortexviaspatiallypatternedthalamicinputsanddistinctarealintracorticalcircuits
AT matthewrwhiteway parallelprocessingofsounddynamicsacrossmouseauditorycortexviaspatiallypatternedthalamicinputsanddistinctarealintracorticalcircuits
AT alirezasheikhattar parallelprocessingofsounddynamicsacrossmouseauditorycortexviaspatiallypatternedthalamicinputsanddistinctarealintracorticalcircuits
AT danielabutts parallelprocessingofsounddynamicsacrossmouseauditorycortexviaspatiallypatternedthalamicinputsanddistinctarealintracorticalcircuits
AT behtashbabadi parallelprocessingofsounddynamicsacrossmouseauditorycortexviaspatiallypatternedthalamicinputsanddistinctarealintracorticalcircuits
AT patrickokanold parallelprocessingofsounddynamicsacrossmouseauditorycortexviaspatiallypatternedthalamicinputsanddistinctarealintracorticalcircuits