Cerebellar Purkinje cells can differentially modulate coherence between sensory and motor cortex depending on region and behavior.
LFP
cerebellum
cerebral cortex
laminar model
whisker system
Journal
Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876
Informations de publication
Date de publication:
12 01 2021
12 01 2021
Historique:
entrez:
14
1
2021
pubmed:
15
1
2021
medline:
19
5
2021
Statut:
ppublish
Résumé
Activity of sensory and motor cortices is essential for sensorimotor integration. In particular, coherence between these areas may indicate binding of critical functions like perception, motor planning, action, or sleep. Evidence is accumulating that cerebellar output modulates cortical activity and coherence, but how, when, and where it does so is unclear. We studied activity in and coherence between S1 and M1 cortices during whisker stimulation in the absence and presence of optogenetic Purkinje cell stimulation in crus 1 and 2 of awake mice, eliciting strong simple spike rate modulation. Without Purkinje cell stimulation, whisker stimulation triggers fast responses in S1 and M1 involving transient coherence in a broad spectrum. Simultaneous stimulation of Purkinje cells and whiskers affects amplitude and kinetics of sensory responses in S1 and M1 and alters the estimated S1-M1 coherence in theta and gamma bands, allowing bidirectional control dependent on behavioral context. These effects are absent when Purkinje cell activation is delayed by 20 ms. Focal stimulation of Purkinje cells revealed site specificity, with cells in medial crus 2 showing the most prominent and selective impact on estimated coherence, i.e., a strong suppression in the gamma but not the theta band. Granger causality analyses and computational modeling of the involved networks suggest that Purkinje cells control S1-M1 phase consistency predominantly via ventrolateral thalamus and M1. Our results indicate that activity of sensorimotor cortices can be dynamically and functionally modulated by specific cerebellar inputs, highlighting a widespread role of the cerebellum in coordinating sensorimotor behavior.
Identifiants
pubmed: 33443203
pii: 2015292118
doi: 10.1073/pnas.2015292118
pmc: PMC7812746
pii:
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
Copyright © 2021 the Author(s). Published by PNAS.
Déclaration de conflit d'intérêts
The authors declare no competing interest.
Références
Cell Rep. 2019 Jun 11;27(11):3167-3181.e5
pubmed: 31189103
Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5670-4
pubmed: 1608977
Neuron. 2019 Sep 25;103(6):1150-1163.e5
pubmed: 31327663
Exp Neurol. 2013 Jul;245:15-26
pubmed: 23022918
Nature. 2012 Sep 13;489(7415):299-303
pubmed: 22922646
Neuroscience. 2018 Jan 1;368:229-239
pubmed: 28743454
Proc Natl Acad Sci U S A. 2016 May 3;113(18):5083-8
pubmed: 27091982
Trends Neurosci. 1998 Sep;21(9):370-5
pubmed: 9735944
Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14332-41
pubmed: 25205811
Exp Brain Res. 1995;104(1):41-54
pubmed: 7621940
Neuroscience. 1998 Mar;83(1):15-25
pubmed: 9466396
Clin Neurophysiol. 2018 Feb;129(2):419-430
pubmed: 29304417
Philos Trans R Soc Lond B Biol Sci. 2011 Nov 12;366(1581):2989-95
pubmed: 21969680
Ann Neurol. 2015 Jun;77(6):1027-49
pubmed: 25762286
Nat Neurosci. 2014 Sep;17(9):1233-9
pubmed: 25064850
J Physiol. 2007 May 15;581(Pt 1):139-54
pubmed: 17317752
Cereb Cortex. 2014 Aug;24(8):2237-48
pubmed: 23547136
J Neurosci. 2013 Apr 10;33(15):6552-6
pubmed: 23575852
Front Neural Circuits. 2013 Aug 21;7:133
pubmed: 23970855
J Physiol. 2010 Oct 1;588(Pt 19):3757-83
pubmed: 20724365
Clin Neurophysiol. 2019 Jun;130(6):997-1007
pubmed: 31005052
Neuron. 2018 Aug 8;99(3):564-575.e2
pubmed: 30017394
J Physiol. 2018 Aug;596(16):3775-3791
pubmed: 29874406
PLoS Comput Biol. 2019 May 6;15(5):e1006475
pubmed: 31059498
J Neurophysiol. 2016 Sep 1;116(3):1261-74
pubmed: 27334960
Neuron. 2019 Aug 7;103(3):506-519.e4
pubmed: 31201123
PLoS Biol. 2006 May;4(5):e124
pubmed: 16605304
Ann N Y Acad Sci. 2011 Apr;1225:110-8
pubmed: 21534998
J Physiol Paris. 2006 Oct;100(4):182-93
pubmed: 17317118
Cereb Cortex. 2019 Feb 1;29(2):598-614
pubmed: 29300895
Prog Brain Res. 2000;124:141-72
pubmed: 10943123
Science. 2012 Aug 10;337(6095):753-6
pubmed: 22879517
Curr Biol. 2017 Jun 5;27(11):1585-1596.e6
pubmed: 28552362
J Neurosci. 2007 Nov 7;27(45):12407-12
pubmed: 17989305
Front Syst Neurosci. 2016 Jan 08;9:175
pubmed: 26778976
Biol Cybern. 2001 Aug;85(2):145-57
pubmed: 11508777
J Physiol. 2019 May;597(9):2483-2514
pubmed: 30908629
J Neurophysiol. 1996 Dec;76(6):3949-67
pubmed: 8985892
Nat Rev Neurosci. 2011 Jun;12(6):327-44
pubmed: 21544091
Brain Behav Evol. 1978;15(2):94-140
pubmed: 638731
Trends Neurosci. 1992 Jun;15(6):218-26
pubmed: 1378666
Nature. 1993 Nov 11;366(6451):153-6
pubmed: 8232553
Nat Neurosci. 2005 Feb;8(2):202-11
pubmed: 15665875
J Neurophysiol. 1996 Dec;76(6):3968-82
pubmed: 8985893
Neuron. 2007 Dec 6;56(5):907-23
pubmed: 18054865
J Comput Neurosci. 2008 Jun;24(3):291-313
pubmed: 17926125
Neuron. 2013 Jul 24;79(2):375-90
pubmed: 23889937
Front Integr Neurosci. 2011 Oct 04;5:53
pubmed: 22065951
J Neurophysiol. 2002 Apr;87(4):2137-48
pubmed: 11929931
Cell Rep. 2019 May 21;27(8):2328-2334.e3
pubmed: 31116979
Neuron. 2013 Aug 7;79(3):567-78
pubmed: 23850595
Front Neural Circuits. 2015 Oct 26;9:64
pubmed: 26578892
Nature. 2011 Dec 25;481(7382):502-5
pubmed: 22198670
Neuron. 2011 Oct 6;72(1):111-23
pubmed: 21982373
Science. 2007 Jun 15;316(5831):1609-12
pubmed: 17569862
Neuroscience. 2018 Jan 1;368:256-267
pubmed: 28528963
Annu Rev Neurosci. 2012;35:203-25
pubmed: 22443509
Elife. 2014 May 07;3:e02536
pubmed: 24843004
Elife. 2019 Feb 11;8:
pubmed: 30741160
Nat Neurosci. 2017 Jul;20(7):951-959
pubmed: 28481348
Somatosens Mot Res. 2011;28(3-4):63-72
pubmed: 21879990
Eur J Neurosci. 2002 Sep;16(6):999-1014
pubmed: 12383229
Nature. 2009 Jun 4;459(7247):663-7
pubmed: 19396156
J Neurosci. 2014 Aug 13;34(33):10870-83
pubmed: 25122889
Sci Adv. 2019 Jul 10;5(7):eaaw5388
pubmed: 31309153
Science. 2010 Nov 26;330(6008):1240-3
pubmed: 21109671
Cell Rep. 2020 Jul 7;32(1):107867
pubmed: 32640232
J Physiol. 2009 Sep 1;587(Pt 17):4139-46
pubmed: 19581378
Nature. 2018 Nov;563(7729):113-116
pubmed: 30333626
Sci Adv. 2016 Nov 16;2(11):e1601335
pubmed: 28138530
Cell Rep. 2015 Dec 1;13(9):1977-88
pubmed: 26655909
J Neurophysiol. 2004 Sep;92(3):1700-7
pubmed: 15331651
Front Neuroanat. 2015 Apr 08;9:41
pubmed: 25904851
J Comp Neurol. 1977 Oct 15;175(4):455-82
pubmed: 915034
Neuron. 2015 Oct 7;88(1):220-35
pubmed: 26447583
Elife. 2018 Dec 18;7:
pubmed: 30561331
Neuron. 2019 Jan 16;101(2):321-336.e9
pubmed: 30553546
Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):724-8
pubmed: 9012852
J Neurosci. 2010 Feb 3;30(5):1832-8
pubmed: 20130192
J Cogn Neurosci. 1989 Spring;1(2):136-52
pubmed: 23968462
Nat Rev Neurosci. 2009 Sep;10(9):670-81
pubmed: 19693030
Neurosci Res. 1996 Jul;25(3):267-83
pubmed: 8856723
J Neurophysiol. 2011 Jan;105(1):474-86
pubmed: 21068271