Weakly Correlated Local Cortical State Switches under Anesthesia Lead to Strongly Correlated Global States.
anesthesia
oscillations
state transitions
synchrony
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:
30 11 2022
30 11 2022
Historique:
received:
17
01
2022
revised:
30
05
2022
accepted:
15
07
2022
pubmed:
27
10
2022
medline:
3
12
2022
entrez:
26
10
2022
Statut:
ppublish
Résumé
During recovery from anesthesia, brain activity switches abruptly between a small set of discrete states. Surprisingly, this switching also occurs under constant doses of anesthesia, even in the absence of stimuli. These metastable states and the transitions between them are thought to form a "scaffold" that ultimately guides the brain back to wakefulness. The processes that constrain cortical activity patterns to these states and govern how states are coordinated between different cortical regions are unknown. If state transitions were driven by subcortical modulation, different cortical sites should exhibit near-synchronous state transitions. Conversely, spatiotemporal heterogeneity would suggest that state transitions are coordinated through corticocortical interactions. To differentiate between these hypotheses, we quantified synchrony of brain states in male rats exposed to a fixed isoflurane concentration. States were defined from spectra of local field potentials recorded across layers of visual and motor cortices. A transition synchrony measure shows that most state transitions are highly localized. Furthermore, while most pairs of cortical sites exhibit statistically significant coupling of both states and state transition times, coupling strength is typically weak. States and state transitions in the thalamic input layer (L4) are particularly decoupled from those in supragranular and infragranular layers. This suggests that state transitions are not imposed on the cortex by broadly projecting modulatory systems. Although each pairwise interaction is typically weak, we show that the multitude of such weak interactions is sufficient to confine global activity to a small number of discrete states.
Identifiants
pubmed: 36288946
pii: JNEUROSCI.0123-22.2022
doi: 10.1523/JNEUROSCI.0123-22.2022
pmc: PMC9732829
doi:
Substances chimiques
Isoflurane
CYS9AKD70P
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
8980-8996Subventions
Organisme : NINDS NIH HHS
ID : F31 NS118808
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM124023
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS113366
Pays : United States
Informations de copyright
Copyright © 2022 Blackwood, Shortal et al.
Références
Front Syst Neurosci. 2010 Aug 10;4:
pubmed: 20802856
J Neurosci. 1995 Jun;15(6):4658-77
pubmed: 7790931
J Neurosci. 2008 Jan 9;28(2):505-18
pubmed: 18184793
J Neurophysiol. 1993 Jun;69(6):2252-7
pubmed: 8350142
Elife. 2020 Aug 28;9:
pubmed: 32857037
PLoS Comput Biol. 2014 Jan;10(1):e1003408
pubmed: 24391485
J Neurophysiol. 2004 Aug;92(2):1133-43
pubmed: 14749320
Neuron. 2011 Dec 8;72(5):847-58
pubmed: 22153379
Brain Res Bull. 1982 Jul-Dec;9(1-6):287-94
pubmed: 7172032
J Physiol. 1952 Aug;117(4):500-44
pubmed: 12991237
Curr Biol. 2013 Nov 4;23(21):2121-9
pubmed: 24139742
Nature. 2006 Jun 1;441(7093):589-94
pubmed: 16688184
Neuron. 2011 Apr 14;70(1):153-69
pubmed: 21482364
Nat Neurosci. 2016 Feb;19(2):290-8
pubmed: 26691833
Nature. 1999 Oct 21;401(6755):788-91
pubmed: 10548103
Anesthesiology. 2017 Feb;126(2):214-222
pubmed: 27984262
Nature. 2011 Apr 28;472(7344):443-7
pubmed: 21525926
Nat Commun. 2019 Jul 1;10(1):2897
pubmed: 31263107
Nature. 2010 Jul 29;466(7306):617-21
pubmed: 20601940
Epilepsy Behav. 2010 Oct;19(2):100-4
pubmed: 20692877
Neuroreport. 1994 Nov 21;5(17):2217-20
pubmed: 7881030
Prog Brain Res. 2004;145:179-96
pubmed: 14650916
Nat Neurosci. 2002 Oct;5(10):979-84
pubmed: 12195434
Proc Natl Acad Sci U S A. 2014 Jun 24;111(25):9283-8
pubmed: 24927558
Front Syst Neurosci. 2014 Oct 07;8:191
pubmed: 25339873
Nat Rev Neurosci. 2013 Nov;14(11):770-85
pubmed: 24135696
N Engl J Med. 2011 Aug 18;365(7):591-600
pubmed: 21848460
Epilepsia. 2009 Dec;50 Suppl 12:38-9
pubmed: 19941521
Nature. 2021 Oct;598(7879):159-166
pubmed: 34616071
Phys Rev E Stat Nonlin Soft Matter Phys. 2013 Oct;88(4):042812
pubmed: 24229230
Neuron. 2009 May 28;62(4):539-54
pubmed: 19477155
Anesthesiology. 2012 Apr;116(4):946-59
pubmed: 22314293
Nat Protoc. 2009;4(8):1128-44
pubmed: 19617885
J Neurosci. 2011 Jun 29;31(26):9574-84
pubmed: 21715622
Neuroscience. 1997 Jan;76(1):25-38
pubmed: 8971756
PLoS One. 2014 Sep 29;9(9):e106291
pubmed: 25264892
J Neurosci. 2004 Dec 8;24(49):11137-47
pubmed: 15590930
Neuron. 2010 Dec 22;68(6):1023-42
pubmed: 21172606
Cereb Cortex. 2008 Dec;18(12):2891-901
pubmed: 18400792
Front Biosci. 2003 May 01;8:s438-51
pubmed: 12700104
Br Med J. 1977 May 21;1(6072):1321
pubmed: 861598
Proc Natl Acad Sci U S A. 2014 Mar 11;111(10):3859-64
pubmed: 24567395
Science. 1993 Oct 29;262(5134):679-85
pubmed: 8235588
Ann N Y Acad Sci. 2008;1129:105-18
pubmed: 18591473
Nature. 2006 Apr 20;440(7087):1007-12
pubmed: 16625187
Front Neuroanat. 2017 Sep 20;11:78
pubmed: 28970785
Elife. 2015 Dec 10;4:e09215
pubmed: 26652162
Electroencephalogr Clin Neurophysiol. 1994 Jan;90(1):1-16
pubmed: 7509269
Front Syst Neurosci. 2012 Apr 13;6:25
pubmed: 22509158
J Neurosci. 1993 Aug;13(8):3252-65
pubmed: 8340806
Trends Neurosci. 2001 Oct;24(10):595-601
pubmed: 11576674
J Neurosci. 2020 Dec 2;40(49):9440-9454
pubmed: 33122389
Cold Spring Harb Protoc. 2012 May 01;2012(5):
pubmed: 22550299
J Sleep Res. 1998;7 Suppl 1:30-5
pubmed: 9682191
Brain. 2020 Mar 1;143(3):833-843
pubmed: 32049333
Nat Neurosci. 2000 Oct;3(10):1027-34
pubmed: 11017176
Acta Neurochir (Wien). 2013 Aug;155(8):1417-24
pubmed: 23812965
Curr Biol. 2012 Nov 6;22(21):2008-16
pubmed: 23103189
Nature. 2008 Aug 14;454(7206):881-5
pubmed: 18633351
Neuron. 2019 Jun 5;102(5):1053-1065.e4
pubmed: 31006556
Cell Rep. 2021 Jun 22;35(12):109270
pubmed: 34161772
J Neurosci. 2016 Jul 20;36(29):7718-26
pubmed: 27445148
J Comp Neurol. 1985 Dec 1;242(1):56-92
pubmed: 2416786
Nature. 2004 Jul 1;430(6995):78-81
pubmed: 15184907
Nat Neurosci. 2015 Apr;18(4):553-561
pubmed: 25706476