Local sleep-like cortical reactivity in the awake brain after focal injury.


Journal

Brain : a journal of neurology
ISSN: 1460-2156
Titre abrégé: Brain
Pays: England
ID NLM: 0372537

Informations de publication

Date de publication:
01 12 2020
Historique:
received: 02 04 2020
revised: 08 07 2020
accepted: 10 08 2020
pubmed: 15 11 2020
medline: 2 3 2021
entrez: 14 11 2020
Statut: ppublish

Résumé

The functional consequences of focal brain injury are thought to be contingent on neuronal alterations extending beyond the area of structural damage. This phenomenon, also known as diaschisis, has clinical and metabolic correlates but lacks a clear electrophysiological counterpart, except for the long-standing evidence of a relative EEG slowing over the injured hemisphere. Here, we aim at testing whether this EEG slowing is linked to the pathological intrusion of sleep-like cortical dynamics within an awake brain. We used a combination of transcranial magnetic stimulation and electroencephalography (TMS/EEG) to study cortical reactivity in a cohort of 30 conscious awake patients with chronic focal and multifocal brain injuries of ischaemic, haemorrhagic and traumatic aetiology. We found that different patterns of cortical reactivity typically associated with different brain states (coma, sleep, wakefulness) can coexist within the same brain. Specifically, we detected the occurrence of prominent sleep-like TMS-evoked slow waves and off-periods-reflecting transient suppressions of neuronal activity-in the area surrounding focal cortical injuries. These perilesional sleep-like responses were associated with a local disruption of signal complexity whereas complex responses typical of the awake brain were present when stimulating the contralesional hemisphere. These results shed light on the electrophysiological properties of the tissue surrounding focal brain injuries in humans. Perilesional sleep-like off-periods can disrupt network activity but are potentially reversible, thus representing a principled read-out for the neurophysiological assessment of stroke patients, as well as an interesting target for rehabilitation.

Identifiants

pubmed: 33188680
pii: 5981995
doi: 10.1093/brain/awaa338
pmc: PMC7805800
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3672-3684

Commentaires et corrections

Type : CommentIn

Informations de copyright

© The Author(s) (2020). Published by Oxford University Press on behalf of the Guarantors of Brain.

Références

Brain Stimul. 2019 Jul - Aug;12(4):1051-1054
pubmed: 30962028
Neuron. 2011 Apr 14;70(1):153-69
pubmed: 21482364
Neurosci Lett. 2016 Apr 8;618:25-30
pubmed: 26940237
Nat Rev Neurosci. 2013 Jun;14(6):443-51
pubmed: 23635871
Arch Gen Psychiatry. 2012 Aug;69(8):766-74
pubmed: 22474071
Arch Ital Biol. 2014 Jun-Sep;152(2-3):169-77
pubmed: 25828688
Electroencephalogr Clin Neurophysiol. 1949 Aug;1(3):265-72
pubmed: 18135418
J Neurosci. 2012 Sep 5;32(36):12506-17
pubmed: 22956841
Ann Neurol. 2016 Nov;80(5):718-729
pubmed: 27717082
Nat Med. 2017 Dec;23(12):1474-1480
pubmed: 29106402
Cereb Cortex. 2007 Feb;17(2):272-83
pubmed: 16495431
Nature. 2011 Apr 28;472(7344):443-7
pubmed: 21525926
Nat Rev Neurosci. 2009 Mar;10(3):199-210
pubmed: 19209176
Elife. 2017 May 16;6:
pubmed: 28509666
PLoS One. 2017 Sep 14;12(9):e0184910
pubmed: 28910407
Neurorehabil Neural Repair. 2017 Jul;31(7):666-676
pubmed: 28604171
Sleep Med Rev. 2019 Feb;43:14-21
pubmed: 30502497
Int J Psychophysiol. 2013 Aug;89(2):151-7
pubmed: 23384886
J Neurosci. 2009 Jun 17;29(24):7679-85
pubmed: 19535579
Brain Topogr. 2013 Apr;26(2):326-37
pubmed: 23053600
Front Hum Neurosci. 2015 May 05;9:250
pubmed: 25999839
Nat Commun. 2018 Oct 24;9(1):4427
pubmed: 30356042
Arch Neurol. 1988 May;45(5):520-4
pubmed: 3358704
Sleep. 2005 Feb;28(2):177-84
pubmed: 16171241
J Neurosci. 2017 Sep 20;37(38):9132-9148
pubmed: 28821651
Nature. 2010 Nov 11;468(7321):305-9
pubmed: 21048709
Neurorehabil Neural Repair. 2019 Sep;33(9):762-774
pubmed: 31328638
Brain Stimul. 2019 May - Jun;12(3):787-790
pubmed: 30738777
Acta Pharmacol Sin. 2013 Jan;34(1):24-32
pubmed: 23123646
J Clin Neurophysiol. 2016 Jun;33(3):203-10
pubmed: 27258443
Hum Brain Mapp. 2015 Nov;36(11):4714-29
pubmed: 26309062
Brain Res. 2004 May 29;1009(1-2):129-36
pubmed: 15120590
Neuroimage. 2019 Jan 15;185:300-312
pubmed: 30347282
Cereb Cortex. 2007 Feb;17(2):400-14
pubmed: 16547348
Neuroimage. 2018 Jul 15;175:365-378
pubmed: 29635028
Stroke. 2012 Feb;43(2):607-15
pubmed: 22207505
Brain. 2020 Jun 1;143(6):1873-1888
pubmed: 32375172
Int J Psychophysiol. 2013 Aug;89(2):252-8
pubmed: 23403325
Science. 2009 May 22;324(5930):1084-7
pubmed: 19461004
Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1924-9
pubmed: 11172052
Neurology. 1987 Jul;37(7):1153-9
pubmed: 3601079
Proc Natl Acad Sci U S A. 2012 Dec 4;109(49):E3377-86
pubmed: 23129622
J Neurosci. 1993 Aug;13(8):3252-65
pubmed: 8340806
J Neurophysiol. 2003 May;89(5):2707-25
pubmed: 12612051
Brain Stimul. 2019 Sep - Oct;12(5):1280-1289
pubmed: 31133480
Stroke. 1989 Jul;20(7):864-70
pubmed: 2749846
Proc Natl Acad Sci U S A. 1989 Oct;86(20):8098-102
pubmed: 2573061
Arch Phys Med Rehabil. 2004 Dec;85(12):2020-9
pubmed: 15605342
Nat Neurosci. 2000 Oct;3(10):1027-34
pubmed: 11017176
J Neurosci Methods. 2019 Feb 1;313:37-43
pubmed: 30571989
Neuroimage. 2015 May 15;112:105-113
pubmed: 25747918
Neurosci Lett. 2004 Jan 23;355(1-2):93-6
pubmed: 14729243
Front Psychol. 2011 Sep 30;2:236
pubmed: 21994498

Auteurs

Simone Sarasso (S)

Dipartimento di Scienze Biomediche e Cliniche "L. Sacco", Università degli Studi di Milano, Milan, Italy.

Sasha D'Ambrosio (S)

Dipartimento di Scienze Biomediche e Cliniche "L. Sacco", Università degli Studi di Milano, Milan, Italy.
Chalfont Centre for Epilepsy, Chalfont St. Peter, UK.
Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.

Matteo Fecchio (M)

Dipartimento di Scienze Biomediche e Cliniche "L. Sacco", Università degli Studi di Milano, Milan, Italy.

Silvia Casarotto (S)

Dipartimento di Scienze Biomediche e Cliniche "L. Sacco", Università degli Studi di Milano, Milan, Italy.

Alessandro Viganò (A)

Istituto Di Ricovero e Cura a Carattere Scientifico, Fondazione Don Carlo Gnocchi, Milan, Italy.

Cristina Landi (C)

Fondazione Europea per la Ricerca Biomedica Onlus, Milan, Italy.

Giulia Mattavelli (G)

NETS, Scuola universitaria superiore IUSS, Pavia, Italy.

Olivia Gosseries (O)

Coma Science Group, University and University Hospital of Liege, GIGA-Consciousness, 4000 Liege, Belgium.

Matteo Quarenghi (M)

Unità Operativa Radiologia, Azienda Ospedaliera Vizzolo P -Risonanza Magnetica- ASST Melegnano e Martesana, Vizzolo Predabissi, Italy.

Steven Laureys (S)

Coma Science Group, University and University Hospital of Liege, GIGA-Consciousness, 4000 Liege, Belgium.

Guya Devalle (G)

Istituto Di Ricovero e Cura a Carattere Scientifico, Fondazione Don Carlo Gnocchi, Milan, Italy.

Mario Rosanova (M)

Dipartimento di Scienze Biomediche e Cliniche "L. Sacco", Università degli Studi di Milano, Milan, Italy.
Fondazione Europea per la Ricerca Biomedica Onlus, Milan, Italy.

Marcello Massimini (M)

Dipartimento di Scienze Biomediche e Cliniche "L. Sacco", Università degli Studi di Milano, Milan, Italy.
Istituto Di Ricovero e Cura a Carattere Scientifico, Fondazione Don Carlo Gnocchi, Milan, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

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

Classifications MeSH