دورية أكاديمية

Information flow between motor cortex and striatum reverses during skill learning.

التفاصيل البيبلوغرافية
العنوان: Information flow between motor cortex and striatum reverses during skill learning.
المؤلفون: Lemke SM; Center for Neuroscience and Cognitive Systems, Istituto Italiano di Tecnologia, Corso Bettini 31, 38068 Rovereto, Italy; Neurology Service, San Francisco Veterans Affairs Medical Center, 4150 Clement Street, San Francisco, CA 94121, USA; Department of Neurology, University of California, San Francisco, 1700 Owens Street, San Francisco, CA 94158, USA; Neuroscience Center, University of North Carolina, Chapel Hill, 116 Manning Drive, Chapel Hill, NC 27599, USA. Electronic address: stefan.lemke@unc.edu., Celotto M; Center for Neuroscience and Cognitive Systems, Istituto Italiano di Tecnologia, Corso Bettini 31, 38068 Rovereto, Italy; Department of Pharmacy and Biotechnology, University of Bologna, Via Irnerio 48, 40126 Bologna, Italy; Institute of Neural Information Processing, Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf (UKE), Falkenried 94, 20251 Hamburg, Germany., Maffulli R; Center for Neuroscience and Cognitive Systems, Istituto Italiano di Tecnologia, Corso Bettini 31, 38068 Rovereto, Italy., Ganguly K; Neurology Service, San Francisco Veterans Affairs Medical Center, 4150 Clement Street, San Francisco, CA 94121, USA; Department of Neurology, University of California, San Francisco, 1700 Owens Street, San Francisco, CA 94158, USA., Panzeri S; Institute of Neural Information Processing, Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf (UKE), Falkenried 94, 20251 Hamburg, Germany. Electronic address: s.panzeri@uke.de.
المصدر: Current biology : CB [Curr Biol] 2024 May 06; Vol. 34 (9), pp. 1831-1843.e7. Date of Electronic Publication: 2024 Apr 10.
نوع المنشور: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Cell Press Country of Publication: England NLM ID: 9107782 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1879-0445 (Electronic) Linking ISSN: 09609822 NLM ISO Abbreviation: Curr Biol Subsets: MEDLINE
أسماء مطبوعة: Publication: Cambridge, MA : Cell Press
Original Publication: London, UK : Current Biology Ltd., c1991-
مواضيع طبية MeSH: Motor Cortex*/physiology , Learning*/physiology , Corpus Striatum*/physiology , Rats, Long-Evans* , Motor Skills*/physiology, Animals ; Rats ; Male
مستخلص: The coordination of neural activity across brain areas during a specific behavior is often interpreted as neural communication involved in controlling the behavior. However, whether information relevant to the behavior is actually transferred between areas is often untested. Here, we used information-theoretic tools to quantify how motor cortex and striatum encode and exchange behaviorally relevant information about specific reach-to-grasp movement features during skill learning in rats. We found a temporal shift in the encoding of behaviorally relevant information during skill learning, as well as a reversal in the primary direction of behaviorally relevant information flow, from cortex-to-striatum during naive movements to striatum-to-cortex during skilled movements. Standard analytical methods that quantify the evolution of overall neural activity during learning-such as changes in neural signal amplitude or the overall exchange of information between areas-failed to capture these behaviorally relevant information dynamics. Using these standard methods, we instead found a consistent coactivation of overall neural signals during movement production and a bidirectional increase in overall information propagation between areas during learning. Our results show that skill learning is achieved through a transformation in how behaviorally relevant information is routed across cortical and subcortical brain areas and that isolating the components of neural activity relevant to and informative about behavior is critical to uncover directional interactions within a coactive and coordinated network.
Competing Interests: Declaration of interests The authors declare no competing interests.
(Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.)
References: Curr Opin Behav Sci. 2018 Apr;20:196-201. (PMID: 30944847)
PLoS Biol. 2015 Sep 22;13(9):e1002257. (PMID: 26394205)
Neuroimage. 2022 Sep;258:119347. (PMID: 35660460)
J Neurosci Methods. 2007 Aug 15;164(1):177-90. (PMID: 17517438)
J Neurophysiol. 2020 Dec 1;124(6):1578-1587. (PMID: 32965150)
Elife. 2020 Nov 27;9:. (PMID: 33245045)
Neuron. 2011 Nov 3;72(3):469-76. (PMID: 22078506)
Sci Rep. 2017 Nov 17;7(1):15759. (PMID: 29150620)
Nat Rev Neurosci. 2009 Mar;10(3):173-85. (PMID: 19229240)
eNeuro. 2023 Feb 21;10(2):. (PMID: 36750360)
eNeuro. 2016 Aug 30;3(4):. (PMID: 27761519)
Nat Commun. 2022 May 4;13(1):2450. (PMID: 35508447)
Trends Cogn Sci. 2015 Apr;19(4):227-33. (PMID: 25746123)
Neuron. 2021 Oct 20;109(20):3298-3311.e4. (PMID: 34437845)
Neuron. 2015 Oct 21;88(2):345-56. (PMID: 26494279)
Network. 2003 Feb;14(1):35-60. (PMID: 12613551)
Neuron. 2022 Sep 7;110(17):2790-2801.e5. (PMID: 35809573)
Sci Adv. 2022 Feb 25;8(8):eabk0231. (PMID: 35213216)
J Neurosci Methods. 2015 May 15;246:30-7. (PMID: 25769277)
Sci Adv. 2019 Oct 30;5(10):eaay0001. (PMID: 31693007)
Nat Commun. 2021 Nov 8;12(1):6443. (PMID: 34750407)
J Neurosci Methods. 2010 Sep 30;192(1):146-51. (PMID: 20637804)
Eur J Neurosci. 2008 Jul;28(2):311-22. (PMID: 18702702)
Neuron. 2015 May 6;86(3):800-12. (PMID: 25892304)
Nat Neurosci. 2009 Mar;12(3):333-41. (PMID: 19198605)
Nat Neurosci. 2022 Jun;25(6):771-782. (PMID: 35618951)
Elife. 2017 Jun 07;6:. (PMID: 28590903)
Phys Rev Lett. 2000 Jul 10;85(2):461-4. (PMID: 10991308)
Trends Neurosci. 1999 Oct;22(10):464-71. (PMID: 10481194)
Neuron. 2014 Sep 3;83(5):1185-99. (PMID: 25132467)
Nature. 2021 Jan;589(7840):96-102. (PMID: 33208951)
J Neurosci. 2016 Mar 23;36(12):3623-32. (PMID: 27013690)
Nat Neurosci. 2019 Oct;22(10):1677-1686. (PMID: 31551604)
J Neurophysiol. 2007 Sep;98(3):1064-72. (PMID: 17615128)
Nat Commun. 2017 Jun 09;8:15834. (PMID: 28598433)
Behav Brain Res. 2009 Dec 1;204(1):153-61. (PMID: 19520119)
Elife. 2021 Sep 10;10:. (PMID: 34505576)
Trends Neurosci. 2000 Aug;23(8):372-6. (PMID: 10906801)
Neuron. 2017 May 17;94(4):880-890.e8. (PMID: 28521138)
J Neurosci. 2004 Jun 16;24(24):5560-9. (PMID: 15201328)
Nature. 2014 Jun 12;510(7504):263-7. (PMID: 24805237)
Elife. 2015 Dec 02;4:e10774. (PMID: 26633811)
Nat Neurosci. 2019 Jul;22(7):1122-1131. (PMID: 31133689)
Nat Rev Neurosci. 2012 May 18;13(6):407-20. (PMID: 22595786)
Nat Med. 2018 Aug;24(8):1257-1267. (PMID: 29915259)
PLoS One. 2019 Dec 11;14(12):e0226028. (PMID: 31825985)
Elife. 2015 Sep 29;4:e09423. (PMID: 26417950)
J Neurosci. 2015 Feb 25;35(8):3499-514. (PMID: 25716849)
J Neurophysiol. 1998 Jun;79(6):3272-8. (PMID: 9636126)
Elife. 2017 May 03;6:. (PMID: 28467303)
Network. 1996;7(1):87-107. (PMID: 29480146)
Neuropsychopharmacology. 2010 Jan;35(1):48-69. (PMID: 19776734)
Neurobiol Learn Mem. 2011 Sep;96(2):95-120. (PMID: 21704718)
J Neurosci. 2003 Dec 17;23(37):11539-53. (PMID: 14684857)
BMC Neurosci. 2009 Jul 16;10:81. (PMID: 19607698)
Cell Rep. 2022 May 31;39(9):110878. (PMID: 35649366)
Annu Rev Neurosci. 2008;31:359-87. (PMID: 18558860)
Nature. 2020 Jan;577(7790):386-391. (PMID: 31875851)
Cell. 2019 Apr 18;177(3):669-682.e24. (PMID: 30929904)
Neuron. 2016 Feb 3;89(3):472-9. (PMID: 26804995)
Proc Natl Acad Sci U S A. 2015 Oct 13;112(41):12834-9. (PMID: 26417078)
Brain. 1986 Oct;109 ( Pt 5):805-43. (PMID: 3779371)
Nat Neurosci. 2018 Sep;21(9):1281-1289. (PMID: 30127430)
Nature. 2012 Mar 04;483(7389):331-5. (PMID: 22388818)
PLoS Biol. 2006 Apr;4(4):e92. (PMID: 16529529)
Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15254-9. (PMID: 17015831)
Entropy (Basel). 2018 Apr 11;20(4):. (PMID: 33265362)
Cereb Cortex. 2020 Jan 10;30(1):421-437. (PMID: 31711133)
Curr Biol. 2004 Jul 13;14(13):1124-34. (PMID: 15242609)
Proc Natl Acad Sci U S A. 2023 Jan 10;120(2):e2207677120. (PMID: 36603032)
Entropy (Basel). 2018 Apr 23;20(4):. (PMID: 33265398)
Nature. 2010 Jul 22;466(7305):457-62. (PMID: 20651684)
Nat Neurosci. 2021 Sep;24(9):1256-1269. (PMID: 34267392)
Neuron. 2017 May 17;94(4):891-907.e6. (PMID: 28521139)
Nat Commun. 2020 Aug 13;11(1):4057. (PMID: 32792523)
Neuron. 2013 Sep 4;79(5):865-72. (PMID: 23954030)
Neuron. 2017 Feb 8;93(3):491-507. (PMID: 28182905)
Nat Commun. 2019 Oct 23;10(1):4812. (PMID: 31645554)
معلومات مُعتمدة: R01 NS108410 United States NS NINDS NIH HHS; R01 NS109961 United States NS NINDS NIH HHS; U19 NS107464 United States NS NINDS NIH HHS
فهرسة مساهمة: Keywords: information flow; information theory; motor control; motor cortex; partial information decomposition; skill learning; striatum
تواريخ الأحداث: Date Created: 20240411 Date Completed: 20240507 Latest Revision: 20240523
رمز التحديث: 20240524
مُعرف محوري في PubMed: PMC11078609
DOI: 10.1016/j.cub.2024.03.023
PMID: 38604168
قاعدة البيانات: MEDLINE
الوصف
تدمد:1879-0445
DOI:10.1016/j.cub.2024.03.023