Cargando…

Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains

The central nucleus of the inferior colliculus (ICC) integrates information about different features of sound and then distributes this information to thalamocortical circuits. However, the lack of clear definitions of circuit elements in the ICC has limited our understanding of the nature of these...

Descripción completa

Detalles Bibliográficos
Autores principales: Kreeger, Lauren J., Connelly, Catherine J., Mehta, Preeti, Zemelman, Boris V., Golding, Nace L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7958253/
https://www.ncbi.nlm.nih.gov/pubmed/33658359
http://dx.doi.org/10.1073/pnas.2007724118
_version_ 1783664793296568320
author Kreeger, Lauren J.
Connelly, Catherine J.
Mehta, Preeti
Zemelman, Boris V.
Golding, Nace L.
author_facet Kreeger, Lauren J.
Connelly, Catherine J.
Mehta, Preeti
Zemelman, Boris V.
Golding, Nace L.
author_sort Kreeger, Lauren J.
collection PubMed
description The central nucleus of the inferior colliculus (ICC) integrates information about different features of sound and then distributes this information to thalamocortical circuits. However, the lack of clear definitions of circuit elements in the ICC has limited our understanding of the nature of these circuit transformations. Here, we combine virus-based genetic access with electrophysiological and optogenetic approaches to identify a large family of excitatory, cholecystokinin-expressing thalamic projection neurons in the ICC of the Mongolian gerbil. We show that these neurons form a distinct cell type, displaying uniform morphology and intrinsic firing features, and provide powerful, spatially restricted excitation exclusively to the ventral auditory thalamus. In vivo, these neurons consistently exhibit V-shaped receptive field properties but strikingly diverse temporal responses to sound. Our results indicate that temporal response diversity is maintained within this population of otherwise uniform cells in the ICC and then relayed to cortex through spatially restricted thalamic subdomains.
format Online
Article
Text
id pubmed-7958253
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-79582532021-03-19 Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains Kreeger, Lauren J. Connelly, Catherine J. Mehta, Preeti Zemelman, Boris V. Golding, Nace L. Proc Natl Acad Sci U S A Biological Sciences The central nucleus of the inferior colliculus (ICC) integrates information about different features of sound and then distributes this information to thalamocortical circuits. However, the lack of clear definitions of circuit elements in the ICC has limited our understanding of the nature of these circuit transformations. Here, we combine virus-based genetic access with electrophysiological and optogenetic approaches to identify a large family of excitatory, cholecystokinin-expressing thalamic projection neurons in the ICC of the Mongolian gerbil. We show that these neurons form a distinct cell type, displaying uniform morphology and intrinsic firing features, and provide powerful, spatially restricted excitation exclusively to the ventral auditory thalamus. In vivo, these neurons consistently exhibit V-shaped receptive field properties but strikingly diverse temporal responses to sound. Our results indicate that temporal response diversity is maintained within this population of otherwise uniform cells in the ICC and then relayed to cortex through spatially restricted thalamic subdomains. National Academy of Sciences 2021-03-09 2021-03-03 /pmc/articles/PMC7958253/ /pubmed/33658359 http://dx.doi.org/10.1073/pnas.2007724118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Kreeger, Lauren J.
Connelly, Catherine J.
Mehta, Preeti
Zemelman, Boris V.
Golding, Nace L.
Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains
title Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains
title_full Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains
title_fullStr Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains
title_full_unstemmed Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains
title_short Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains
title_sort excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7958253/
https://www.ncbi.nlm.nih.gov/pubmed/33658359
http://dx.doi.org/10.1073/pnas.2007724118
work_keys_str_mv AT kreegerlaurenj excitatorycholecystokininneuronsofthemidbrainintegratediversetemporalresponsesanddriveauditorythalamicsubdomains
AT connellycatherinej excitatorycholecystokininneuronsofthemidbrainintegratediversetemporalresponsesanddriveauditorythalamicsubdomains
AT mehtapreeti excitatorycholecystokininneuronsofthemidbrainintegratediversetemporalresponsesanddriveauditorythalamicsubdomains
AT zemelmanborisv excitatorycholecystokininneuronsofthemidbrainintegratediversetemporalresponsesanddriveauditorythalamicsubdomains
AT goldingnacel excitatorycholecystokininneuronsofthemidbrainintegratediversetemporalresponsesanddriveauditorythalamicsubdomains