Microglia enable mature perineuronal nets disassembly upon anesthetic ketamine exposure or 60-Hz light entrainment in the healthy brain.


Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
06 07 2021
Historique:
received: 20 08 2020
revised: 20 11 2020
accepted: 04 06 2021
entrez: 7 7 2021
pubmed: 8 7 2021
medline: 11 2 2022
Statut: ppublish

Résumé

Perineuronal nets (PNNs), components of the extracellular matrix, preferentially coat parvalbumin-positive interneurons and constrain critical-period plasticity in the adult cerebral cortex. Current strategies to remove PNN are long-lasting, invasive, and trigger neuropsychiatric symptoms. Here, we apply repeated anesthetic ketamine as a method with minimal behavioral effect. We find that this paradigm strongly reduces PNN coating in the healthy adult brain and promotes juvenile-like plasticity. Microglia are critically involved in PNN loss because they engage with parvalbumin-positive neurons in their defined cortical layer. We identify external 60-Hz light-flickering entrainment to recapitulate microglia-mediated PNN removal. Importantly, 40-Hz frequency, which is known to remove amyloid plaques, does not induce PNN loss, suggesting microglia might functionally tune to distinct brain frequencies. Thus, our 60-Hz light-entrainment strategy provides an alternative form of PNN intervention in the healthy adult brain.

Identifiants

pubmed: 34233180
pii: S2211-1247(21)00689-6
doi: 10.1016/j.celrep.2021.109313
pmc: PMC8284881
mid: NIHMS1715352
pii:
doi:

Substances chimiques

Anesthetics 0
Parvalbumins 0
Ketamine 690G0D6V8H

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

109313

Subventions

Organisme : European Research Council
ID : 715571
Pays : International
Organisme : NEI NIH HHS
ID : R01 EY023037
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY029245
Pays : United States

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests. A.V. and S.S. disclose an international patent application (PCT/EP2020/079365).

Références

Neuron. 2003 Jun 19;38(6):977-85
pubmed: 12818182
Biochem Biophys Res Commun. 2001 May 4;283(2):379-83
pubmed: 11327712
Neuroscience. 2017 May 14;350:13-22
pubmed: 28323012
Eur J Neurosci. 2021 Jun;53(12):3988-4004
pubmed: 32510674
Exp Brain Res. 2001 Apr;137(3-4):346-53
pubmed: 11355381
Eur J Neurosci. 1998 May;10(5):1856-77
pubmed: 9751156
Neuron. 2013 Apr 10;78(1):81-93
pubmed: 23583108
Front Cell Neurosci. 2015 Sep 22;9:369
pubmed: 26441540
Cell Mol Life Sci. 2019 Aug;76(16):3207-3228
pubmed: 31172215
Matrix Biol. 2013 Aug 8;32(6):352-63
pubmed: 23597636
Neuroscience. 2017 Jul 4;355:161-174
pubmed: 28495333
Cell. 2020 Jul 23;182(2):388-403.e15
pubmed: 32615087
Science. 2011 Sep 9;333(6048):1456-8
pubmed: 21778362
Nature. 2016 Dec 7;540(7632):230-235
pubmed: 27929004
Adv Exp Med Biol. 2012;970:153-71
pubmed: 22351055
Sci Rep. 2018 Mar 5;8(1):4007
pubmed: 29507385
Nature. 2013 Sep 26;501(7468):543-6
pubmed: 23975100
FEBS J. 2011 Jan;278(1):28-45
pubmed: 21087458
J Neurosci. 1996 May 15;16(10):3274-86
pubmed: 8627365
Annu Rev Physiol. 2017 Feb 10;79:619-643
pubmed: 27959620
Elife. 2017 Sep 06;6:
pubmed: 28875930
Cell. 2013 Dec 19;155(7):1596-609
pubmed: 24360280
Nat Commun. 2018 Nov 9;9(1):4724
pubmed: 30413686
J Neurosci. 2017 Feb 1;37(5):1269-1283
pubmed: 28039374
Proc Natl Acad Sci U S A. 2016 Dec 6;113(49):14139-14144
pubmed: 27856748
J Neuroinflammation. 2015 Aug 01;12:139
pubmed: 26232154
Cereb Cortex. 2012 Mar;22(3):725-34
pubmed: 21685398
Nat Rev Neurosci. 2005 Nov;6(11):877-88
pubmed: 16261181
Neuron. 2004 Dec 16;44(6):917-23
pubmed: 15603735
Nat Commun. 2013;4:1484
pubmed: 23403561
Elife. 2015 Nov 26;5:e11290
pubmed: 26609811
Neuron. 2013 Jan 9;77(1):10-8
pubmed: 23312512
Nat Rev Neurosci. 2010 Nov;11(11):735-46
pubmed: 20944663
J Neurosci. 2008 Apr 16;28(16):4283-92
pubmed: 18417708
Brain Res Brain Res Rev. 1994 Jan;19(1):128-45
pubmed: 8167657
Mol Psychiatry. 2019 Jun;24(6):828-838
pubmed: 30696941
Behav Brain Res. 2020 Jul 15;390:112631
pubmed: 32437885
Behav Brain Res. 2017 Aug 14;332:316-326
pubmed: 28634108
Front Hum Neurosci. 2016 Nov 29;10:612
pubmed: 27965560
IBRO Rep. 2018 Nov 28;6:1-17
pubmed: 30582064
Nat Commun. 2019 Aug 21;10(1):3758
pubmed: 31434879
Front Psychiatry. 2019 Jan 17;9:766
pubmed: 30705645
J Neurosci. 2012 Oct 17;32(42):14538-47
pubmed: 23077039
Elife. 2016 Mar 04;5:
pubmed: 26943618
Biom J. 2008 Jun;50(3):346-63
pubmed: 18481363
Behav Brain Res. 2016 Oct 1;312:305-12
pubmed: 27343934
Physiol Rev. 2011 Apr;91(2):461-553
pubmed: 21527731
EBioMedicine. 2020 Aug;58:102919
pubmed: 32745992
Science. 2002 Nov 8;298(5596):1248-51
pubmed: 12424383
Neuroscience. 2017 Sep 17;359:196-208
pubmed: 28723388
Neuroreport. 1992 Oct;3(10):869-72
pubmed: 1421090
Transl Psychiatry. 2017 Sep 19;7(9):e1237
pubmed: 28926001
Biol Psychiatry. 2008 Apr 15;63(8):730-5
pubmed: 18022604
J Biol Chem. 2008 May 16;283(20):13652-65
pubmed: 18359769
Nature. 1989 Mar 23;338(6213):334-7
pubmed: 2922061
J Neurosci. 2008 Oct 8;28(41):10278-86
pubmed: 18842887
Semin Cell Dev Biol. 2011 Apr;22(2):214-9
pubmed: 21320624
PLoS One. 2018 Sep 19;13(9):e0203559
pubmed: 30231081
Science. 2001 Feb 23;291(5508):1560-3
pubmed: 11222864
Front Cell Neurosci. 2015 Jul 29;9:280
pubmed: 26283917
Trends Neurosci. 2007 Jul;30(7):309-16
pubmed: 17555828
J Pharmacol Exp Ther. 2016 Oct;359(1):11-7
pubmed: 27511819
PLoS Biol. 2010 Nov 02;8(11):e1000527
pubmed: 21072242
Nat Neurosci. 2005 Jun;8(6):752-8
pubmed: 15895084
Neuropharmacology. 2013 Jul;70:27-34
pubmed: 23337256
J Neurosci Res. 1994 Jul 1;38(4):365-75
pubmed: 7932870
Nat Rev Neurosci. 2019 Aug;20(8):451-465
pubmed: 31263252
Nature. 2009 Jun 4;459(7247):663-7
pubmed: 19396156
Nat Commun. 2016 Mar 07;7:10905
pubmed: 26948129
Eur J Biochem. 2003 Oct;270(19):3996-4007
pubmed: 14511382
Front Mol Neurosci. 2018 Aug 03;11:270
pubmed: 30123106
Brain Res. 2018 Nov 1;1698:139-150
pubmed: 30099038
Annu Rev Neurosci. 2011;34:601-28
pubmed: 21513454
Science. 2005 May 27;308(5726):1314-8
pubmed: 15831717
Exp Neurol. 2019 Aug;318:32-41
pubmed: 31029597
Nature. 2009 Jun 4;459(7247):698-702
pubmed: 19396159
Nat Neurosci. 2006 Dec;9(12):1512-9
pubmed: 17115040
Neuron. 2012 May 24;74(4):691-705
pubmed: 22632727
Exp Anim. 2015;64(1):57-64
pubmed: 25312399

Auteurs

Alessandro Venturino (A)

Institute of Science and Technology (IST) Austria, Am Campus 1, 3400 Klosterneuburg, Austria.

Rouven Schulz (R)

Institute of Science and Technology (IST) Austria, Am Campus 1, 3400 Klosterneuburg, Austria.

Héctor De Jesús-Cortés (H)

The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.

Margaret E Maes (ME)

Institute of Science and Technology (IST) Austria, Am Campus 1, 3400 Klosterneuburg, Austria.

Bálint Nagy (B)

Institute of Science and Technology (IST) Austria, Am Campus 1, 3400 Klosterneuburg, Austria.

Francis Reilly-Andújar (F)

The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.

Gloria Colombo (G)

Institute of Science and Technology (IST) Austria, Am Campus 1, 3400 Klosterneuburg, Austria.

Ryan John A Cubero (RJA)

Institute of Science and Technology (IST) Austria, Am Campus 1, 3400 Klosterneuburg, Austria.

Florianne E Schoot Uiterkamp (FE)

Institute of Science and Technology (IST) Austria, Am Campus 1, 3400 Klosterneuburg, Austria.

Mark F Bear (MF)

The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.

Sandra Siegert (S)

Institute of Science and Technology (IST) Austria, Am Campus 1, 3400 Klosterneuburg, Austria. Electronic address: sandra.siegert@ist.ac.at.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH