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Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention

Neocortical choline acetyltransferase (ChAT)-expressing interneurons are a subclass of vasoactive intestinal peptide (ChAT-VIP) neurons of which circuit and behavioural function are unknown. Here, we show that ChAT-VIP neurons directly excite neighbouring neurons in several layers through fast synap...

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Autores principales: Obermayer, Joshua, Luchicchi, Antonio, Heistek, Tim S., de Kloet, Sybren F., Terra, Huub, Bruinsma, Bastiaan, Mnie-Filali, Ouissame, Kortleven, Christian, Galakhova, Anna A., Khalil, Ayoub J., Kroon, Tim, Jonker, Allert J., de Haan, Roel, van den Berg, Wilma D. J., Goriounova, Natalia A., de Kock, Christiaan P. J., Pattij, Tommy, Mansvelder, Huibert D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6872593/
https://www.ncbi.nlm.nih.gov/pubmed/31754098
http://dx.doi.org/10.1038/s41467-019-13244-9
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author Obermayer, Joshua
Luchicchi, Antonio
Heistek, Tim S.
de Kloet, Sybren F.
Terra, Huub
Bruinsma, Bastiaan
Mnie-Filali, Ouissame
Kortleven, Christian
Galakhova, Anna A.
Khalil, Ayoub J.
Kroon, Tim
Jonker, Allert J.
de Haan, Roel
van den Berg, Wilma D. J.
Goriounova, Natalia A.
de Kock, Christiaan P. J.
Pattij, Tommy
Mansvelder, Huibert D.
author_facet Obermayer, Joshua
Luchicchi, Antonio
Heistek, Tim S.
de Kloet, Sybren F.
Terra, Huub
Bruinsma, Bastiaan
Mnie-Filali, Ouissame
Kortleven, Christian
Galakhova, Anna A.
Khalil, Ayoub J.
Kroon, Tim
Jonker, Allert J.
de Haan, Roel
van den Berg, Wilma D. J.
Goriounova, Natalia A.
de Kock, Christiaan P. J.
Pattij, Tommy
Mansvelder, Huibert D.
author_sort Obermayer, Joshua
collection PubMed
description Neocortical choline acetyltransferase (ChAT)-expressing interneurons are a subclass of vasoactive intestinal peptide (ChAT-VIP) neurons of which circuit and behavioural function are unknown. Here, we show that ChAT-VIP neurons directly excite neighbouring neurons in several layers through fast synaptic transmission of acetylcholine (ACh) in rodent medial prefrontal cortex (mPFC). Both interneurons in layers (L)1–3 as well as pyramidal neurons in L2/3 and L6 receive direct inputs from ChAT-VIP neurons mediated by fast cholinergic transmission. A fraction (10–20%) of postsynaptic neurons that received cholinergic input from ChAT-VIP interneurons also received GABAergic input from these neurons. In contrast to regular VIP interneurons, ChAT-VIP neurons did not disinhibit pyramidal neurons. Finally, we show that activity of these neurons is relevant for behaviour and they control attention behaviour distinctly from basal forebrain ACh inputs. Thus, ChAT-VIP neurons are a local source of cortical ACh that directly excite neurons throughout cortical layers and contribute to attention.
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spelling pubmed-68725932019-11-25 Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention Obermayer, Joshua Luchicchi, Antonio Heistek, Tim S. de Kloet, Sybren F. Terra, Huub Bruinsma, Bastiaan Mnie-Filali, Ouissame Kortleven, Christian Galakhova, Anna A. Khalil, Ayoub J. Kroon, Tim Jonker, Allert J. de Haan, Roel van den Berg, Wilma D. J. Goriounova, Natalia A. de Kock, Christiaan P. J. Pattij, Tommy Mansvelder, Huibert D. Nat Commun Article Neocortical choline acetyltransferase (ChAT)-expressing interneurons are a subclass of vasoactive intestinal peptide (ChAT-VIP) neurons of which circuit and behavioural function are unknown. Here, we show that ChAT-VIP neurons directly excite neighbouring neurons in several layers through fast synaptic transmission of acetylcholine (ACh) in rodent medial prefrontal cortex (mPFC). Both interneurons in layers (L)1–3 as well as pyramidal neurons in L2/3 and L6 receive direct inputs from ChAT-VIP neurons mediated by fast cholinergic transmission. A fraction (10–20%) of postsynaptic neurons that received cholinergic input from ChAT-VIP interneurons also received GABAergic input from these neurons. In contrast to regular VIP interneurons, ChAT-VIP neurons did not disinhibit pyramidal neurons. Finally, we show that activity of these neurons is relevant for behaviour and they control attention behaviour distinctly from basal forebrain ACh inputs. Thus, ChAT-VIP neurons are a local source of cortical ACh that directly excite neurons throughout cortical layers and contribute to attention. Nature Publishing Group UK 2019-11-21 /pmc/articles/PMC6872593/ /pubmed/31754098 http://dx.doi.org/10.1038/s41467-019-13244-9 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Obermayer, Joshua
Luchicchi, Antonio
Heistek, Tim S.
de Kloet, Sybren F.
Terra, Huub
Bruinsma, Bastiaan
Mnie-Filali, Ouissame
Kortleven, Christian
Galakhova, Anna A.
Khalil, Ayoub J.
Kroon, Tim
Jonker, Allert J.
de Haan, Roel
van den Berg, Wilma D. J.
Goriounova, Natalia A.
de Kock, Christiaan P. J.
Pattij, Tommy
Mansvelder, Huibert D.
Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention
title Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention
title_full Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention
title_fullStr Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention
title_full_unstemmed Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention
title_short Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention
title_sort prefrontal cortical chat-vip interneurons provide local excitation by cholinergic synaptic transmission and control attention
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6872593/
https://www.ncbi.nlm.nih.gov/pubmed/31754098
http://dx.doi.org/10.1038/s41467-019-13244-9
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