Differential Effects of Open- and Closed-Loop Intracortical Microstimulation on Firing Patterns of Neurons in Distant Cortical Areas.


Journal

Cerebral cortex (New York, N.Y. : 1991)
ISSN: 1460-2199
Titre abrégé: Cereb Cortex
Pays: United States
ID NLM: 9110718

Informations de publication

Date de publication:
14 05 2020
Historique:
received: 11 06 2019
revised: 27 08 2019
accepted: 01 10 2019
pubmed: 14 12 2019
medline: 21 10 2021
entrez: 14 12 2019
Statut: ppublish

Résumé

Intracortical microstimulation can be used successfully to modulate neuronal activity. Activity-dependent stimulation (ADS), in which action potentials recorded extracellularly from a single neuron are used to trigger stimulation at another cortical location (closed-loop), is an effective treatment for behavioral recovery after brain lesion, but the related neurophysiological changes are still not clear. Here, we investigated the ability of ADS and random stimulation (RS) to alter firing patterns of distant cortical locations. We recorded 591 neuronal units from 23 Long-Evan healthy anesthetized rats. Stimulation was delivered to either forelimb or barrel field somatosensory cortex, using either RS or ADS triggered from spikes recorded in the rostral forelimb area (RFA). Both RS and ADS stimulation protocols rapidly altered spike firing within RFA compared with no stimulation. We observed increase in firing rates and change of spike patterns. ADS was more effective than RS in increasing evoked spikes during the stimulation periods, by producing a reliable, progressive increase in stimulus-related activity over time and an increased coupling of the trigger channel with the network. These results are critical for understanding the efficacy of closed-loop electrical microstimulation protocols in altering activity patterns in interconnected brain networks, thus modulating cortical state and functional connectivity.

Identifiants

pubmed: 31832642
pii: 5673779
doi: 10.1093/cercor/bhz281
pmc: PMC7197073
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2879-2896

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS030853
Pays : United States
Organisme : NICHD NIH HHS
ID : R03 HD094608
Pays : United States
Organisme : NICHD NIH HHS
ID : T32 HD057850
Pays : United States

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permission@oup.com.

Références

Arch Neurol. 2011 Feb;68(2):165
pubmed: 20937936
Epilepsia. 2004 Apr;45(4):346-54
pubmed: 15030497
Neuron. 2011 Oct 20;72(2):197-8
pubmed: 22017983
Brain Res. 1975 Nov 21;98(3):417-40
pubmed: 1102064
Nat Neurosci. 2015 May;18(5):779-86
pubmed: 25867121
Neuron. 2012 Dec 6;76(5):1030-41
pubmed: 23217750
Neurotherapeutics. 2009 Apr;6(2):238-43
pubmed: 19332315
Neurology. 2011 Sep 27;77(13):1295-304
pubmed: 21917777
J Neurosci. 2007 Oct 24;27(43):11496-500
pubmed: 17959792
Science. 2010 Jan 29;327(5965):587-90
pubmed: 20110507
Mov Disord. 2017 Jun;32(6):810-819
pubmed: 28597557
Somatosens Mot Res. 1990;7(4):463-83
pubmed: 2291378
Front Syst Neurosci. 2010 Aug 23;4:
pubmed: 20838477
Front Neuroinform. 2014 Feb 05;8:5
pubmed: 24550819
Neural Comput. 2004 Aug;16(8):1661-87
pubmed: 15228749
IEEE Trans Neural Syst Rehabil Eng. 2013 May;21(3):500-7
pubmed: 23475375
PLoS One. 2010 Dec 08;5(12):e15209
pubmed: 21165147
Annu Rev Neurosci. 1998;21:149-86
pubmed: 9530495
J Neurophysiol. 2015 Apr 1;113(7):2537-48
pubmed: 25652922
PLoS Comput Biol. 2009 Jul;5(7):e1000433
pubmed: 19593378
N Engl J Med. 2010 Dec 30;363(27):2638-50
pubmed: 21190458
Science. 1995 Jun 9;268(5216):1503-6
pubmed: 7770778
J Neurosci. 2013 May 1;33(18):7912-8
pubmed: 23637182
Prog Neurobiol. 2013 Apr;103:115-30
pubmed: 22307059
Front Neural Circuits. 2013 Apr 11;7:57
pubmed: 23596396
J Neural Eng. 2011 Feb;8(1):016011
pubmed: 21252415
Proc Natl Acad Sci U S A. 2013 Nov 5;110(45):18279-84
pubmed: 24127595
J Comp Neurol. 2016 Oct 15;524(15):3104-23
pubmed: 27037503
Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):E4367-75
pubmed: 25267639
J Neurosci Methods. 2009 Feb 15;177(1):241-9
pubmed: 18957306
Neurosci Biobehav Rev. 2013 Jun;37(5):803-18
pubmed: 23535445
Phys Rev Lett. 1996 Apr 29;76(18):3251-3254
pubmed: 10060920
BMC Neurosci. 2017 Jun 12;18(1):49
pubmed: 28606117
Elife. 2015 Jan 03;4:
pubmed: 25556699
J Neurophysiol. 2006 Aug;96(2):512-21
pubmed: 16835359
J Neurophysiol. 2005 Mar;93(3):1659-70
pubmed: 15342724
PLoS Comput Biol. 2014 Jan;10(1):e1003408
pubmed: 24391485
Nature. 2006 Nov 2;444(7115):56-60
pubmed: 17057705
Nature. 2015 May 28;521(7553):511-515
pubmed: 25849776
Brain. 1996 Apr;119 ( Pt 2):507-22
pubmed: 8800945
Neuron. 2013 Dec 4;80(5):1301-9
pubmed: 24210907
Epilepsy Res. 2011 Oct;96(3):267-75
pubmed: 21795024
Proc Natl Acad Sci U S A. 2013 Mar 19;110(12):4780-5
pubmed: 23471992
J Neural Eng. 2014 Apr;11(2):026004
pubmed: 24503702
Epilepsy Res. 2010 Feb;88(2-3):239-46
pubmed: 20044240
Transl Psychiatry. 2017 Sep 19;7(9):e1237
pubmed: 28926001
N Engl J Med. 2006 Aug 31;355(9):896-908
pubmed: 16943402
J Neural Eng. 2015 Dec;12(6):066018
pubmed: 26479701
Proc Natl Acad Sci U S A. 2013 Dec 24;110(52):21177-82
pubmed: 24324155
Acta Neurochir Suppl. 2006;99:87-91
pubmed: 17370771
J Physiol. 1974 Dec;243(2):553-76
pubmed: 4449074
Nat Commun. 2013;4:1482
pubmed: 23403583
J Neural Eng. 2011 Jun;8(3):035001
pubmed: 21593550
J Neural Eng. 2012 Dec;9(6):065003
pubmed: 23186948
Neurol Res. 2003 Dec;25(8):789-93
pubmed: 14669520
Ann Neurol. 2013 Sep;74(3):449-57
pubmed: 23852650
Sci Rep. 2017 Apr 21;7(1):1033
pubmed: 28432303
Front Neurosci. 2016 Sep 23;10:438
pubmed: 27721741
Neuroscientist. 2013 Oct;19(5):434-41
pubmed: 22968640
Arch Neurol. 2005 Apr;62(4):554-60
pubmed: 15824252
Neurology. 2012 Jul 3;79(1):55-65
pubmed: 22722632
Annu Rev Neurosci. 2011;34:601-28
pubmed: 21513454
Nat Rev Neurol. 2012 Dec;8(12):690-9
pubmed: 23147846
J Neural Eng. 2013 Dec;10(6):066016
pubmed: 24280531
J Neurosci. 2008 Nov 19;28(47):12284-93
pubmed: 19020022
Behav Brain Res. 2010 Dec 25;214(2):377-85
pubmed: 20558210
Cereb Cortex. 2016 May;26(5):1866-1877
pubmed: 25609241
Epilepsia. 2010 Nov;51(11):2297-304
pubmed: 20973781
Front Neurosci. 2016 Feb 25;10:62
pubmed: 26941602
Curr Opin Neurobiol. 2004 Apr;14(2):169-77
pubmed: 15082321
J Neurophysiol. 1998 Dec;80(6):3321-5
pubmed: 9862925
Cereb Cortex. 2010 Aug;20(8):1926-36
pubmed: 20019146
Epilepsia. 2010 May;51(5):899-908
pubmed: 20331461

Auteurs

Alberto Averna (A)

Rehab Technologies, Istituto Italiano di Tecnologia, 16163 Genova, Italy.
Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal and Child science (DINOGMI), University of Genova, 16145 Genova, Italy.
Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, 16163 Genova, Italy.

Valentina Pasquale (V)

Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, 16163 Genova, Italy.

Maxwell D Murphy (MD)

Department of Physical Medicine and Rehabilitation, University of Kansas Medical Center, Kansas City, KS 66160, USA.

Maria Piera Rogantin (MP)

Department of Mathematics, University of Genova, 16146 Genova, Italy.

Gustaf M Van Acker (GM)

Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, KS 66160, USA.

Randolph J Nudo (RJ)

Department of Physical Medicine and Rehabilitation, University of Kansas Medical Center, Kansas City, KS 66160, USA.
Landon Center on Aging, University of Kansas Medical Center, Kansas City, KS 66160, USA.

Michela Chiappalone (M)

Rehab Technologies, Istituto Italiano di Tecnologia, 16163 Genova, Italy.

David J Guggenmos (DJ)

Department of Physical Medicine and Rehabilitation, University of Kansas Medical Center, Kansas City, KS 66160, USA.
Landon Center on Aging, University of Kansas Medical Center, Kansas City, KS 66160, USA.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH