A neural circuit state change underlying skilled movements.
Action Potentials
/ physiology
Animals
Calcium
/ metabolism
Cerebellum
/ physiology
Cortical Synchronization
Forelimb
/ physiology
Interneurons
/ physiology
Learning
Mice, Inbred C57BL
Mice, Transgenic
Models, Neurological
Motor Activity
/ physiology
Movement
/ physiology
Nerve Net
/ physiology
Olivary Nucleus
/ physiology
Optogenetics
Purkinje Cells
/ physiology
Stereotyped Behavior
Task Performance and Analysis
Purkinje cells
calcium imaging
cerebellum
climbing fibers
coupled oscillators
motor learning
neural circuit dynamics
state change
synchronization
two-photon microscopy
Journal
Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066
Informations de publication
Date de publication:
08 07 2021
08 07 2021
Historique:
received:
07
10
2020
revised:
09
05
2021
accepted:
01
06
2021
pubmed:
3
7
2021
medline:
4
1
2022
entrez:
2
7
2021
Statut:
ppublish
Résumé
In motor neuroscience, state changes are hypothesized to time-lock neural assemblies coordinating complex movements, but evidence for this remains slender. We tested whether a discrete change from more autonomous to coherent spiking underlies skilled movement by imaging cerebellar Purkinje neuron complex spikes in mice making targeted forelimb-reaches. As mice learned the task, millimeter-scale spatiotemporally coherent spiking emerged ipsilateral to the reaching forelimb, and consistent neural synchronization became predictive of kinematic stereotypy. Before reach onset, spiking switched from more disordered to internally time-locked concerted spiking and silence. Optogenetic manipulations of cerebellar feedback to the inferior olive bi-directionally modulated neural synchronization and reaching direction. A simple model explained the reorganization of spiking during reaching as reflecting a discrete bifurcation in olivary network dynamics. These findings argue that to prepare learned movements, olivo-cerebellar circuits enter a self-regulated, synchronized state promoting motor coordination. State changes facilitating behavioral transitions may generalize across neural systems.
Identifiants
pubmed: 34214470
pii: S0092-8674(21)00702-9
doi: 10.1016/j.cell.2021.06.001
pmc: PMC8844704
mid: NIHMS1720166
pii:
doi:
Substances chimiques
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
3731-3747.e21Subventions
Organisme : Howard Hughes Medical Institute
Pays : United States
Informations de copyright
Copyright © 2021 Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests O.R., M.J.S., J.L., T.H.K., and J.S. are inventors on a patent, assigned to Stanford, for the two-photon mesoscope. K.D. and C.R. have disclosed all novel opsins to Stanford, which has submitted patent applications to facilitate commercial application and translation; all opsin methods, protocols, clones, and sequences are freely available to nonprofit institutions and investigators.
Références
PLoS Comput Biol. 2012;8(7):e1002580
pubmed: 22792054
J Neurosci. 2009 Aug 26;29(34):10463-73
pubmed: 19710300
PLoS Comput Biol. 2019 May 6;15(5):e1006475
pubmed: 31059498
Neuron. 2013 May 22;78(4):700-13
pubmed: 23643935
Nature. 2012 Jul 5;487(7405):51-6
pubmed: 22722855
J Neurosci. 2005 Oct 26;25(43):9919-31
pubmed: 16251440
Neuron. 2014 Mar 19;81(6):1389-1400
pubmed: 24656256
Nat Rev Neurosci. 2009 Sep;10(9):670-81
pubmed: 19693030
Brain Struct Funct. 2019 May;224(4):1677-1695
pubmed: 30929054
Phys Rev E Stat Nonlin Soft Matter Phys. 2010 Jul;82(1 Pt 1):011903
pubmed: 20866644
Proc Natl Acad Sci U S A. 2002 Feb 19;99(4):2299-302
pubmed: 11854526
J Physiol. 1998 Oct 1;512 ( Pt 1):277-93
pubmed: 9729638
Nat Neurosci. 2018 Oct;21(10):1431-1441
pubmed: 30224805
Neuron. 2009 May 28;62(4):555-65
pubmed: 19477156
Trends Neurosci. 2008 Dec;31(12):617-25
pubmed: 18952303
Philos Trans R Soc Lond B Biol Sci. 2012 Apr 5;367(1591):906-18
pubmed: 22371613
Science. 2015 Dec 11;350(6266):1361-6
pubmed: 26586188
J Neurosci Methods. 2006 Sep 30;156(1-2):351-9
pubmed: 16621010
Nature. 2015 Oct 15;526(7573):439-42
pubmed: 26469054
Neuron. 2009 Sep 24;63(6):747-60
pubmed: 19778505
Prog Brain Res. 2000;124:213-20
pubmed: 10943127
Elife. 2019 Sep 11;8:
pubmed: 31509108
Trends Neurosci. 1998 Sep;21(9):391-400
pubmed: 9735947
Nature. 2014 Jun 26;510(7506):529-32
pubmed: 24814344
Elife. 2019 Oct 29;8:
pubmed: 31661073
Cell. 2017 Aug 24;170(5):1013-1027.e14
pubmed: 28823561
Nat Neurosci. 2015 Sep;18(9):1310-7
pubmed: 26237366
Neuron. 2016 Oct 19;92(2):372-382
pubmed: 27720486
J Neurosci. 2009 Jun 24;29(25):8005-15
pubmed: 19553440
Neuron. 2008 May 22;58(4):599-612
pubmed: 18498740
J Neurosci. 2014 Jul 2;34(27):8937-47
pubmed: 24990915
Front Neural Circuits. 2013 Sep 05;7:138
pubmed: 24046731
Curr Biol. 2015 May 4;25(9):1157-65
pubmed: 25843032
Prog Brain Res. 2007;165:13-9
pubmed: 17925237
J Neurosci. 2009 Nov 11;29(45):14352-62
pubmed: 19906982
Nat Neurosci. 2010 Mar;13(3):369-78
pubmed: 20173745
Nat Neurosci. 2006 Nov;9(11):1404-11
pubmed: 17028585
Science. 1997 Dec 12;278(5345):1950-3
pubmed: 9395398
PLoS One. 2012;7(9):e46360
pubmed: 23029495
Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15921-6
pubmed: 19717463
Front Neural Circuits. 2013 Feb 04;7:3
pubmed: 23382711
Cerebellum. 2006;5(1):7-14
pubmed: 16527758
Curr Biol. 2013 Jun 3;23(11):947-55
pubmed: 23684973
Nature. 1998 Apr 2;392(6675):494-7
pubmed: 9548253
J Physiol. 2000 Jan 15;522 Pt 2:297-309
pubmed: 10639105
Cell. 2019 Apr 18;177(3):669-682.e24
pubmed: 30929904
Nature. 2010 Dec 16;468(7326):964-7
pubmed: 21131948
Neurosci Res. 1993 Mar;16(3):195-207
pubmed: 7683779
Front Neural Circuits. 2012 Nov 22;6:91
pubmed: 23189043
J Physiol. 1986 Jul;376:163-82
pubmed: 3795074
Nature. 2006 Apr 20;440(7087):1007-12
pubmed: 16625187
Nat Commun. 2013;4:2521
pubmed: 24088740
Neuron. 2009 May 14;62(3):400-12
pubmed: 19447095
Proc Natl Acad Sci U S A. 1982 Apr;79(8):2554-8
pubmed: 6953413
Nature. 2011 Dec 25;481(7382):502-5
pubmed: 22198670
IEEE Trans Image Process. 1998;7(1):27-41
pubmed: 18267377
J Neurosci. 2012 Jul 18;32(29):9817-23
pubmed: 22815496
Elife. 2016 Jun 14;5:
pubmed: 27300105
FASEB J. 2001 Oct;15(12):2283-5
pubmed: 11511531
Nature. 2020 Apr;580(7801):100-105
pubmed: 32238928
Cell. 2018 Jul 12;174(2):465-480.e22
pubmed: 30007418
Nat Neurosci. 2008 Oct;11(10):1185-92
pubmed: 18806784
Nature. 1995 Mar 30;374(6521):453-7
pubmed: 7700354
J Neurophysiol. 1996 Jul;76(1):255-75
pubmed: 8836223
J Neurosci Methods. 2017 Nov 1;291:83-94
pubmed: 28782629
Proc Natl Acad Sci U S A. 2007 Oct 2;104(40):15911-6
pubmed: 17895389
Nat Rev Neurosci. 2012 Sep;13(9):619-35
pubmed: 22895474
J Neurophysiol. 2000 Nov;84(5):2622-9
pubmed: 11068003
Nature. 2014 Apr 17;508(7496):351-6
pubmed: 24487621
Nat Methods. 2011 Dec 18;9(2):159-72
pubmed: 22179551
J Physiol. 1981 Sep;318:207-21
pubmed: 7320889
Nat Neurosci. 2018 May;21(5):736-743
pubmed: 29662213
J Neurophysiol. 1992 Dec;68(6):2222-36
pubmed: 1491268
Nat Neurosci. 2019 Jun;22(6):950-962
pubmed: 31036947
Neuroreport. 1997 Jan 20;8(2):523-9
pubmed: 9080441
J Neurophysiol. 1997 Apr;77(4):1747-58
pubmed: 9114233