State-dependent brainstem ensemble dynamics and their interactions with hippocampus across sleep states.
P/PGO waves
brain state
brainstem
mouse
neural ensemble dynamics
neural oscillations
neuroscience
sleep
Journal
eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614
Informations de publication
Date de publication:
14 01 2020
14 01 2020
Historique:
received:
26
09
2019
accepted:
14
01
2020
pubmed:
15
1
2020
medline:
15
5
2021
entrez:
15
1
2020
Statut:
epublish
Résumé
The brainstem plays a crucial role in sleep-wake regulation. However, the ensemble dynamics underlying sleep regulation remain poorly understood. Here, we show slow, state-predictive brainstem ensemble dynamics and state-dependent interactions between the brainstem and the hippocampus in mice. On a timescale of seconds to minutes, brainstem populations can predict pupil dilation and vigilance states and exhibit longer prediction power than hippocampal CA1 neurons. On a timescale of sub-seconds, pontine waves (P-waves) are accompanied by synchronous firing of brainstem neurons during both rapid eye movement (REM) and non-REM (NREM) sleep. Crucially, P-waves functionally interact with CA1 activity in a state-dependent manner: during NREM sleep, hippocampal sharp wave-ripples (SWRs) precede P-waves. On the other hand, P-waves during REM sleep are phase-locked with ongoing theta oscillations and are followed by burst firing of CA1 neurons. This state-dependent global coordination between the brainstem and hippocampus implicates distinct functional roles of sleep.
Identifiants
pubmed: 31934862
doi: 10.7554/eLife.52244
pii: 52244
pmc: PMC6996931
doi:
pii:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/M00905X/1
Pays : United Kingdom
Organisme : Leverhulme Trust
ID : RPG-2015-377
Organisme : Alzheimer's Research UK
ID : ARUK-PPG2017B-005
Organisme : RNID
ID : S45
Pays : United Kingdom
Organisme : Engineering and Physical Sciences Research Council
ID : EP/S005692/1
Organisme : Japan Science and Technology Agency
ID : JPMJPR1887
Organisme : Japan Society for the Promotion of Science
ID : 17H06520
Informations de copyright
© 2020, Tsunematsu et al.
Déclaration de conflit d'intérêts
TT, AP, AO, SS No competing interests declared
Références
Neuroscience. 1995 Aug;67(3):703-12
pubmed: 7675196
Nat Rev Neurosci. 2019 Feb;20(2):109-116
pubmed: 30573905
Science. 2016 Nov 25;354(6315):1004-1008
pubmed: 27885006
Proc Natl Acad Sci U S A. 2015 Jan 13;112(2):584-9
pubmed: 25548191
Cell Mol Neurobiol. 1987 Jun;7(2):105-49
pubmed: 3308096
Annu Rev Psychol. 2015 Jan 3;66:143-72
pubmed: 25061767
Arch Ital Biol. 1992 Oct;130(4):263-84
pubmed: 1489248
Hippocampus. 2015 Oct;25(10):1073-188
pubmed: 26135716
Science. 1980 Aug 1;209(4456):615-7
pubmed: 6994229
J Neurophysiol. 2010 Feb;103(2):844-57
pubmed: 20007501
Neuroscience. 2006;137(4):1087-106
pubmed: 16343791
Exp Brain Res. 1984;54(3):463-75
pubmed: 6723865
Trends Ecol Evol. 2016 Aug;31(8):590-599
pubmed: 27262386
Nature. 1999 Oct 21;401(6755):788-91
pubmed: 10548103
Nat Commun. 2018 Jan 24;9(1):354
pubmed: 29367602
Nat Rev Neurosci. 2009 Mar;10(3):199-210
pubmed: 19209176
J Pharmacol Exp Ther. 1984 Feb;228(2):268-74
pubmed: 6694111
Cell Mol Neurobiol. 1997 Jun;17(3):341-65
pubmed: 9187490
Physiol Rev. 2013 Apr;93(2):681-766
pubmed: 23589831
J Neurosci. 1990 Aug;10(8):2560-79
pubmed: 2201752
Curr Opin Neurobiol. 2017 Jun;44:167-177
pubmed: 28544929
Eur J Neurosci. 2011 Dec;34(12):1887-94
pubmed: 22082031
PLoS Comput Biol. 2016 Nov 4;12(11):e1005189
pubmed: 27814363
Nature. 2015 Oct 15;526(7573):435-8
pubmed: 26444238
Brain Res. 1980 Aug 4;194(2):500-5
pubmed: 7388627
Nature. 2005 Oct 27;437(7063):1264-71
pubmed: 16251951
Front Neural Circuits. 2018 Mar 09;12:21
pubmed: 29593504
Neurosci Res. 2017 May;118:30-47
pubmed: 28506629
Sleep Med Rev. 2017 Apr;32:85-94
pubmed: 27083772
Front Aging Neurosci. 2019 Feb 26;11:29
pubmed: 30863301
Elife. 2020 Jan 14;9:
pubmed: 31934862
Neuron. 2002 Jan 31;33(3):325-40
pubmed: 11832222
Front Neural Circuits. 2017 Sep 14;11:64
pubmed: 28959191
Neuron. 2017 Apr 5;94(1):19-36
pubmed: 28384471
Brain Res. 2005 Jul 27;1051(1-2):50-6
pubmed: 15982642
Curr Biol. 2017 Nov 20;27(22):R1237-R1248
pubmed: 29161567
Neurosci Res. 2019 Mar;140:77-92
pubmed: 30118737
Nat Rev Neurosci. 2002 Aug;3(8):591-605
pubmed: 12154361
J Neurophysiol. 1983 Oct;50(4):784-97
pubmed: 6631463
J Neurosci. 2017 Jan 18;37(3):457-463
pubmed: 28100730
Neuron. 2014 Jan 8;81(1):12-34
pubmed: 24411729
J Neurosci. 2008 Jun 25;28(26):6731-41
pubmed: 18579747
Harvey Lect. 1963;58:233-97
pubmed: 14272578
Curr Biol. 2018 Feb 5;28(3):392-400.e3
pubmed: 29358069
Synapse. 1998 Dec;30(4):409-23
pubmed: 9826233
J Neurosci. 1989 Jul;9(7):2215-29
pubmed: 2746326
Brain Res. 2002 Dec 27;958(2):347-58
pubmed: 12470871
Science. 1971 Dec 17;174(4015):1250-2
pubmed: 5133450
Science. 2001 Nov 2;294(5544):1052-7
pubmed: 11691983
Physiol Rev. 2012 Jul;92(3):1087-187
pubmed: 22811426
Neurosci Res. 2004 Nov;50(3):283-9
pubmed: 15488291
Neuron. 2010 Dec 22;68(6):1023-42
pubmed: 21172606
Arch Ital Biol. 1963 Oct 5;101:666-80
pubmed: 14163921
Nat Neurosci. 2018 Sep;21(9):1281-1289
pubmed: 30127430
Science. 1978 Jul 21;201(4352):269-72
pubmed: 663656
Science. 1975 Jul 4;189(4196):55-8
pubmed: 1094539
Science. 1993 Oct 29;262(5134):679-85
pubmed: 8235588
Cell. 2019 May 16;177(5):1293-1307.e16
pubmed: 31031008
J Neurosci. 1997 Mar 1;17(5):1869-79
pubmed: 9030645
Nature. 2007 Nov 15;450(7168):420-4
pubmed: 17943086
Nature. 2016 Oct 05;538(7623):51-59
pubmed: 27708309
J Neurosci. 1993 Aug;13(8):3252-65
pubmed: 8340806
Neuron. 2015 Sep 23;87(6):1143-1161
pubmed: 26402600
Nat Commun. 2018 Dec 18;9(1):5364
pubmed: 30560939
Electroencephalogr Clin Neurophysiol. 1973 May;34(5):547-9
pubmed: 4121327
J Neurosci. 2014 May 14;34(20):6896-909
pubmed: 24828644
Annu Rev Neurosci. 2005;28:403-50
pubmed: 16022602
Pflugers Arch. 2012 Jan;463(1):43-52
pubmed: 22083642
J Physiol (Paris). 1965 Jan-Feb;57:255-6
pubmed: 14309100
Annu Rev Neurosci. 2019 Jul 8;42:27-46
pubmed: 30699051
Behav Brain Res. 2013 Oct 15;255:64-74
pubmed: 23707248
Arch Ital Biol. 1962;100:125-206
pubmed: 14452612
Neuron. 2017 Feb 22;93(4):747-765
pubmed: 28231463
Front Comput Neurosci. 2013 Apr 17;7:35
pubmed: 23616763
Neurosci Biobehav Rev. 2007;31(5):775-824
pubmed: 17445891
Science. 1969 Jan 3;163(3862):32-41
pubmed: 4303225