GABAergic interneurons excite neonatal hippocampus in vivo.


Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
06 2020
Historique:
received: 07 11 2019
accepted: 14 04 2020
entrez: 26 6 2020
pubmed: 26 6 2020
medline: 12 4 2022
Statut: epublish

Résumé

GABAergic interneurons are proposed to be critical for early activity and synapse formation by directly exciting, rather than inhibiting, neurons in developing hippocampus and neocortex. However, the role of GABAergic neurons in the generation of neonatal network activity has not been tested in vivo, and recent studies have challenged the excitatory nature of early GABA. By locally manipulating interneuron activity in unanesthetized neonatal mice, we show that GABAergic neurons are excitatory in CA1 hippocampus at postnatal day 3 (P3) and are responsible for most of the spontaneous firing of pyramidal cells at that age. Hippocampal interneurons become inhibitory by P7, whereas visual cortex interneurons are already inhibitory by P3 and remain so throughout development. These regional and age-specific differences are the result of a change in chloride reversal potential, because direct activation of light-gated anion channels in glutamatergic neurons drives CA1 firing at P3, but silences it at P7 in CA1, and at all ages in visual cortex. This study in the intact brain reveals that GABAergic interneuron excitation is essential for network activity in neonatal hippocampus and confirms that visual cortical interneurons are inhibitory throughout early postnatal development.

Identifiants

pubmed: 32582852
doi: 10.1126/sciadv.aba1430
pii: aba1430
pmc: PMC7292633
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

eaba1430

Subventions

Organisme : NEI NIH HHS
ID : R01 EY022730
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS106244
Pays : United States

Informations de copyright

Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

Références

J Neurosci. 2010 Mar 24;30(12):4325-37
pubmed: 20335468
Dev Neurosci. 1999 Nov;21(3-5):310-9
pubmed: 10575254
Nat Commun. 2015 Jul 16;6:7750
pubmed: 26177896
Neuron. 2011 Sep 22;71(6):995-1013
pubmed: 21943598
Nature. 2017 Mar 29;543(7647):719-722
pubmed: 28358077
Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):5163-8
pubmed: 17360345
J Neurophysiol. 2000 Jan;83(1):359-66
pubmed: 10634879
Cell Rep. 2019 Mar 19;26(12):3173-3182.e5
pubmed: 30893591
Cereb Cortex. 2019 Feb 1;29(2):906-920
pubmed: 30535003
J Neurophysiol. 2007 Jan;97(1):692-700
pubmed: 17093125
Nat Med. 2015 Dec;21(12):1436-44
pubmed: 26594844
Neuron. 2009 Sep 10;63(5):657-72
pubmed: 19755108
Clin Neurophysiol. 2012 Aug;123(8):1502-11
pubmed: 22341979
Physiol Rev. 2007 Oct;87(4):1215-84
pubmed: 17928584
Proc Natl Acad Sci U S A. 2017 Dec 12;114(50):E10819-E10828
pubmed: 29183979
Front Cell Neurosci. 2010 Jul 14;4:
pubmed: 20725525
J Neurosci. 2016 Jun 1;36(22):5961-73
pubmed: 27251618
Front Cell Neurosci. 2017 Sep 20;11:289
pubmed: 28979189
Science. 2016 Sep 2;353(6303):1037-1040
pubmed: 27516412
Nat Neurosci. 2000 May;3(5):452-9
pubmed: 10769384
Science. 2011 Oct 14;334(6053):226-9
pubmed: 21998388
Neuron. 2016 Feb 3;89(3):521-35
pubmed: 26844832
Neuron. 2016 Feb 3;89(3):536-49
pubmed: 26844833
Curr Opin Neurobiol. 2018 Oct;52:72-79
pubmed: 29715588
Nat Neurosci. 2014 Aug;17(8):1123-9
pubmed: 24997763
Neuron. 2013 Feb 6;77(3):388-405
pubmed: 23395369
Science. 2014 Feb 7;343(6171):675-9
pubmed: 24503856
Neuron. 2018 Jul 11;99(1):98-116.e7
pubmed: 29937280
J Neurosci. 2010 Mar 3;30(9):3438-49
pubmed: 20203203
Neuron. 2020 Jan 8;105(1):75-92.e5
pubmed: 31780329
J Physiol. 2004 Jun 15;557(Pt 3):829-41
pubmed: 15090604
Science. 2006 Dec 15;314(5806):1788-92
pubmed: 17170309
Elife. 2016 Oct 11;5:
pubmed: 27725086
J Neurosci. 2018 Oct 10;38(41):8772-8786
pubmed: 30150360
Neuron. 2013 Dec 4;80(5):1129-44
pubmed: 24314725
J Clin Invest. 2011 Apr;121(4):1424-8
pubmed: 21364278
Science. 2002 Jun 14;296(5575):2049-52
pubmed: 12065842
J Neurosci. 2014 Jan 8;34(2):446-50
pubmed: 24403144
Trends Neurosci. 2017 May;40(5):276-294
pubmed: 28431741
Nature. 1999 Jan 21;397(6716):251-5
pubmed: 9930699
Nat Commun. 2018 Oct 8;9(1):4125
pubmed: 30297821
J Neurosci. 2002 Aug 1;22(15):6309-14
pubmed: 12151506
Semin Fetal Neonatal Med. 2006 Dec;11(6):471-8
pubmed: 17018268
Brain Res. 2003 Sep 12;984(1-2):149-59
pubmed: 12932849
CNS Neurosci Ther. 2015 Feb;21(2):83-91
pubmed: 25438879
Neuron. 2015 May 20;86(4):936-946
pubmed: 25937170
J Neurosci. 2016 Mar 2;36(9):2646-62
pubmed: 26937006
Cell Rep. 2015 Nov 3;13(5):1003-15
pubmed: 26565913

Auteurs

Yasunobu Murata (Y)

Department of Pharmacology and Physiology, The George Washington University, Washington, DC, USA.

Matthew T Colonnese (MT)

Department of Pharmacology and Physiology, The George Washington University, Washington, DC, USA.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH