Integrity of Corpus Callosum Is Essential for theCross-Hemispheric Propagation of Sleep Slow Waves:A High-Density EEG Study in Split-Brain Patients.
NREM
connectivity
corpus callosum
sleep
slow wave
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:
15 07 2020
15 07 2020
Historique:
received:
29
10
2019
revised:
17
02
2020
accepted:
19
04
2020
pubmed:
17
6
2020
medline:
18
12
2020
entrez:
17
6
2020
Statut:
ppublish
Résumé
The slow waves of non-rapid eye movement (NREM) sleep reflect experience-dependent plasticity and play a direct role in the restorative functions of sleep. Importantly, slow waves behave as traveling waves, and their propagation is assumed to occur through cortico-cortical white matter connections. In this light, the corpus callosum (CC) may represent the main responsible for cross-hemispheric slow-wave propagation. To verify this hypothesis, we performed overnight high-density (hd)-EEG recordings in five patients who underwent total callosotomy due to drug-resistant epilepsy (CPs; two females), in three noncallosotomized neurologic patients (NPs; two females), and in a sample of 24 healthy adult subjects (HSs; 13 females). In all CPs slow waves displayed a significantly reduced probability of cross-hemispheric propagation and a stronger inter-hemispheric asymmetry. In both CPs and HSs, the incidence of large slow waves within individual NREM epochs tended to differ across hemispheres, with a relative overall predominance of the right over the left hemisphere. The absolute magnitude of this asymmetry was greater in CPs relative to HSs. However, the CC resection had no significant effects on the distribution of slow-wave origin probability across hemispheres. The present results indicate that CC integrity is essential for the cross-hemispheric traveling of slow waves in human sleep, which is in line with the assumption of a direct relationship between white matter integrity and slow-wave propagation. Our findings also revealed a residual cross-hemispheric slow-wave propagation that may rely on alternative pathways, including cortico-subcortico-cortical loops. Finally, these data indicate that the lack of the CC does not lead to differences in slow-wave generation across brain hemispheres.
Identifiants
pubmed: 32541070
pii: JNEUROSCI.2571-19.2020
doi: 10.1523/JNEUROSCI.2571-19.2020
pmc: PMC7363462
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5589-5603Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 215267/Z/19/Z
Pays : United Kingdom
Informations de copyright
Copyright © 2020 Avvenuti et al.
Références
Cereb Cortex. 2000 Dec;10(12):1185-99
pubmed: 11073868
Cereb Cortex. 2019 Jan 1;29(1):319-335
pubmed: 29190336
Neuron. 2011 Oct 20;72(2):404-16
pubmed: 22017997
Science. 2013 Oct 18;342(6156):373-7
pubmed: 24136970
J Neurosci. 2014 Dec 10;34(50):16890-901
pubmed: 25505340
Electroencephalogr Clin Neurophysiol. 1987 Jan;66(1):8-14
pubmed: 2431870
Neurosci Biobehav Rev. 2019 Oct;105:231-248
pubmed: 31412269
Nat Hum Behav. 2019 Mar;3(3):274-283
pubmed: 30953006
Sci Rep. 2014 May 28;4:5092
pubmed: 24867667
J Neurosci. 2013 Jan 2;33(1):227-33
pubmed: 23283336
Brain. 2019 Mar 1;142(3):674-687
pubmed: 30698667
Brain Behav Evol. 1994;44(3):156-65
pubmed: 7987664
Front Neurosci. 2019 Jun 05;13:576
pubmed: 31231186
Front Neural Circuits. 2016 Jan 14;9:88
pubmed: 26834569
Nat Commun. 2019 Mar 29;10(1):1417
pubmed: 30926845
Neuroimage. 2018 Sep;178:23-35
pubmed: 29758338
Nat Neurosci. 2018 Jul;21(7):974-984
pubmed: 29892048
PLoS One. 2009 Oct 26;4(10):e7601
pubmed: 19855839
Sleep. 2014 Oct 01;37(10):1621-37
pubmed: 25197810
Clin Neurophysiol. 2006 Feb;117(2):348-68
pubmed: 16356767
Physiol Behav. 1972 May;8(5):811-5
pubmed: 4339962
Front Biosci. 2003 May 01;8:s683-93
pubmed: 12700054
Sleep. 2018 Nov 1;41(11):
pubmed: 30169809
Cereb Cortex. 2003 Aug;13(8):883-93
pubmed: 12853375
Curr Biol. 2016 May 9;26(9):1190-4
pubmed: 27112296
Front Hum Neurosci. 2018 Jun 19;12:248
pubmed: 29970995
Sleep. 2007 Dec;30(12):1631-42
pubmed: 18246973
Schizophr Bull. 2007 Nov;33(6):1307-11
pubmed: 17172634
J Neurosci. 2019 Apr 3;39(14):2686-2697
pubmed: 30737310
Neuron. 2014 Jan 8;81(1):12-34
pubmed: 24411729
J Sleep Res. 2011 Dec;20(4):506-13
pubmed: 21435064
Sleep. 2007 Dec;30(12):1643-57
pubmed: 18246974
J Neurosci. 2014 Apr 16;34(16):5689-703
pubmed: 24741059
J Neurosci. 2002 Dec 15;22(24):10941-7
pubmed: 12486189
Nat Sci Sleep. 2016 Jul 12;8:221-38
pubmed: 27471418
J Neurophysiol. 1996 Dec;76(6):4152-68
pubmed: 8985908
J Biol Rhythms. 1999 Dec;14(6):557-68
pubmed: 10643753
Behav Neurosci. 2002 Dec;116(6):976-81
pubmed: 12492296
J Neurophysiol. 2002 Nov;88(5):2280-6
pubmed: 12424269
Neurosci Biobehav Rev. 2000 Dec;24(8):817-42
pubmed: 11118608
Proc Natl Acad Sci U S A. 2009 Feb 3;106(5):1608-13
pubmed: 19164756
Front Cell Neurosci. 2013 Sep 18;7:154
pubmed: 24065884
J Neurosci. 2018 Oct 24;38(43):9175-9185
pubmed: 30201768
Clin Neurophysiol. 2006 Aug;117(8):1826-35
pubmed: 16807092
Brain Res. 2001 Sep 21;913(2):220-3
pubmed: 11549390
Sci Adv. 2019 Feb 27;5(2):eaav5447
pubmed: 30820460
Clin Neurophysiol. 2000 May;111(5):924-8
pubmed: 10802465
Eur Neurol. 1993;33(2):173-6
pubmed: 8467828
Electroencephalogr Clin Neurophysiol. 1966 Apr;20(4):348-56
pubmed: 4143672
J Neurophysiol. 2001 May;85(5):1969-85
pubmed: 11353014
Sleep. 2017 Sep 1;40(9):
pubmed: 28934529
Nat Neurosci. 2000 Oct;3(10):1027-34
pubmed: 11017176
J Neurosci Methods. 2016 Dec 1;274:1-12
pubmed: 27663980
J Neurophysiol. 2019 Jun 1;121(6):2140-2152
pubmed: 30943100
J Neurosci. 2004 Aug 4;24(31):6862-70
pubmed: 15295020
J Neurosci. 2013 Feb 20;33(8):3323-31
pubmed: 23426660
Clin Electroencephalogr. 1990 Jan;21(1):42-7
pubmed: 2297948
J Neurosci Methods. 2004 Mar 15;134(1):9-21
pubmed: 15102499