Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex.


Journal

The Journal of neuroscience : the official journal of the Society for Neuroscience
ISSN: 1529-2401
Titre abrégé: J Neurosci
Pays: United States
ID NLM: 8102140

Informations de publication

Date de publication:
24 06 2020
Historique:
received: 06 02 2020
revised: 08 04 2020
accepted: 04 05 2020
pubmed: 28 5 2020
medline: 21 11 2020
entrez: 28 5 2020
Statut: ppublish

Résumé

Parvalbumin-expressing (PV+) interneurons play a key role in the maturation and synchronization of cortical circuitry and alterations in these inhibitory neurons, especially in the medial prefrontal cortex (mPFC), have been found in different psychiatric disorders. The formation of perineuronal nets (PNNs) around many of these interneurons at the end of the critical periods reduces their plasticity and sets their connectivity. Consequently, the presence of PNNs must have an important impact on the synaptic input and the physiology of PV+ cells. In the present study, we have found that in adult male mice, prefrontocortical PV+ cells surrounded by PNNs show higher density of perisomatic excitatory and inhibitory puncta, longer axonal initial segments (AISs), and higher PV expression when compared with PV+ cells lacking PNNs. In order to better understand the impact of PNNs on the connectivity and physiology of PV+ interneurons in the mPFC, we have digested enzymatically these structures and have found a decrease in the density of inhibitory puncta on their perisomatic region but not on the PV+ perisomatic puncta on pyramidal neurons. Moreover, extracellular recordings show that the digestion of PNNs induces a decrease in γ activity, an oscillation dependent on PV+ cells, in the mPFC of anesthetized mice. Our results suggest that the presence of PNNs enwrapping PV+ cells regulates their inhibitory input and has a potent influence on their activity. These results may be relevant for psychiatric research, given the alterations in PNNs, PV+ interneurons and their physiology described in different mental disorders.

Identifiants

pubmed: 32457072
pii: JNEUROSCI.0291-20.2020
doi: 10.1523/JNEUROSCI.0291-20.2020
pmc: PMC7314408
doi:

Substances chimiques

Parvalbumins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5008-5018

Informations de copyright

Copyright © 2020 the authors.

Références

Mol Psychiatry. 2017 May;22(5):680-688
pubmed: 28194008
Neuron. 2013 Oct 2;80(1):51-63
pubmed: 24094102
Biol Psychiatry. 2013 Sep 15;74(6):427-35
pubmed: 23790226
Dev Neurobiol. 2007 Apr;67(5):570-88
pubmed: 17443809
eNeuro. 2017 Jun 7;4(3):
pubmed: 28593193
J Neurosci. 2019 Feb 27;39(9):1605-1620
pubmed: 30651327
Nat Rev Neurosci. 2019 Aug;20(8):451-465
pubmed: 31263252
Nature. 2010 Jun 24;465(7301):1075-8
pubmed: 20543825
Nature. 2009 Jun 4;459(7247):698-702
pubmed: 19396159
Science. 2009 Sep 4;325(5945):1258-61
pubmed: 19729657
J Neurotrauma. 2013 May 1;30(9):741-51
pubmed: 23025758
J Neurosci. 2017 Feb 1;37(5):1269-1283
pubmed: 28039374
Nat Rev Neurosci. 2005 Nov;6(11):877-88
pubmed: 16261181
Neuron. 2015 Feb 18;85(4):770-86
pubmed: 25695271
Neuron. 2007 Oct 4;56(1):33-42
pubmed: 17920013
Epilepsy Res. 2013 Aug;105(3):272-9
pubmed: 23602553
Neurochem Int. 2018 Jan;112:59-70
pubmed: 29126935
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Cell. 2008 Aug 8;134(3):508-20
pubmed: 18692473
Science. 2002 Nov 8;298(5596):1248-51
pubmed: 12424383
Proc Natl Acad Sci U S A. 2019 Dec 16;:
pubmed: 31843881
Heliyon. 2018 Jun 29;4(6):e00669
pubmed: 30003163
Trends Neurosci. 1998 Dec;21(12):510-5
pubmed: 9881847
Curr Opin Neurobiol. 2014 Jun;26:7-14
pubmed: 24650498
J Neurosci Methods. 2009 Jan 30;176(2):57-62
pubmed: 18778735
Cell Rep. 2018 Jan 16;22(3):576-584
pubmed: 29346758
Int J Bipolar Disord. 2019 Nov 15;7(1):24
pubmed: 31728775
Neuron. 2008 Nov 26;60(4):683-97
pubmed: 19038224
Proc Natl Acad Sci U S A. 2014 Feb 18;111(7):2800-5
pubmed: 24550310
Nat Rev Neurosci. 2012 Feb 15;13(3):169-82
pubmed: 22334212
Annu Rev Neurosci. 2012;35:203-25
pubmed: 22443509
J Comp Neurol. 2000 Dec 25;428(4):616-29
pubmed: 11077416
Eur J Pharmacol. 2015 Apr 15;753:66-72
pubmed: 25446562
Neuron. 2005 Apr 7;46(1):141-51
pubmed: 15820700
Front Neuroanat. 2014 Mar 11;8:11
pubmed: 24653680
Neuroscience. 2001;104(2):359-69
pubmed: 11377840
J Neurosci. 2010 Jan 6;30(1):361-71
pubmed: 20053917
Neuropsychopharmacology. 2016 Aug;41(9):2206-14
pubmed: 26868058
J Neurophysiol. 2010 Aug;104(2):1195-210
pubmed: 20463205
Nat Neurosci. 2013 Aug;16(8):1068-76
pubmed: 23817549
Nature. 2013 Dec 12;504(7479):272-6
pubmed: 24336286
Neuron. 2016 Jul 20;91(2):260-92
pubmed: 27477017

Auteurs

Hector Carceller (H)

Department of Cell Biology, Interdisciplinary Research Structure for Biotechnology and Biomedicine (BIOTECMED), University of Valencia, Burjassot, 46100, Spain.

Ramon Guirado (R)

Department of Cell Biology, Interdisciplinary Research Structure for Biotechnology and Biomedicine (BIOTECMED), University of Valencia, Burjassot, 46100, Spain.

Edna Ripolles-Campos (E)

Department of Cell Biology, Interdisciplinary Research Structure for Biotechnology and Biomedicine (BIOTECMED), University of Valencia, Burjassot, 46100, Spain.

Vicent Teruel-Marti (V)

Neuronal Circuits Laboratory, Department of Anatomy and Human Embryology, University of Valencia, Valencia, 46010, Spain.

Juan Nacher (J)

Department of Cell Biology, Interdisciplinary Research Structure for Biotechnology and Biomedicine (BIOTECMED), University of Valencia, Burjassot, 46100, Spain nacher@uv.es.
Spanish National Network for Research in Mental Health, CIBERSAM, Madrid, 28029, Spain.
Fundación Investigación Hospital Clínico de Valencia, INCLIVA, Valencia 46010, Spain.

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Classifications MeSH