COALIA: A Computational Model of Human EEG for Consciousness Research.

GABA TMS-EEG brain connectivity computational modeling disinhibition disorders of consciousness (DOC) feedforward inhibition

Journal

Frontiers in systems neuroscience
ISSN: 1662-5137
Titre abrégé: Front Syst Neurosci
Pays: Switzerland
ID NLM: 101477946

Informations de publication

Date de publication:
2019
Historique:
received: 08 03 2019
accepted: 07 10 2019
entrez: 5 12 2019
pubmed: 5 12 2019
medline: 5 12 2019
Statut: epublish

Résumé

Understanding the origin of the main physiological processes involved in consciousness is a major challenge of contemporary neuroscience, with crucial implications for the study of Disorders of Consciousness (DOC). The difficulties in achieving this task include the considerable quantity of experimental data in this field, along with the non-intuitive, nonlinear nature of neuronal dynamics. One possibility of integrating the main results from the experimental literature into a cohesive framework, while accounting for nonlinear brain dynamics, is the use of physiologically-inspired computational models. In this study, we present a physiologically-grounded computational model, attempting to account for the main micro-circuits identified in the human cortex, while including the specificities of each neuronal type. More specifically, the model accounts for thalamo-cortical (vertical) regulation of cortico-cortical (horizontal) connectivity, which is a central mechanism for brain information integration and processing. The distinct neuronal assemblies communicate through feedforward and feedback excitatory and inhibitory synaptic connections implemented in a template brain accounting for long-range connectome. The EEG generated by this physiologically-based simulated brain is validated through comparison with brain rhythms recorded in humans in two states of consciousness (wakefulness, sleep). Using the model, it is possible to reproduce the local disynaptic disinhibition of basket cells (fast GABAergic inhibition) and glutamatergic pyramidal neurons through long-range activation of vasoactive intestinal-peptide (VIP) interneurons that induced inhibition of somatostatin positive (SST) interneurons. The model (COALIA) predicts that the strength and dynamics of the thalamic output on the cortex control the local and long-range cortical processing of information. Furthermore, the model reproduces and explains clinical results regarding the complexity of transcranial magnetic stimulation TMS-evoked EEG responses in DOC patients and healthy volunteers, through a modulation of thalamo-cortical connectivity that governs the level of cortico-cortical communication. This new model provides a quantitative framework to accelerate the study of the physiological mechanisms involved in the emergence, maintenance and disruption (sleep, anesthesia, DOC) of consciousness.

Identifiants

pubmed: 31798421
doi: 10.3389/fnsys.2019.00059
pmc: PMC6863981
doi:

Types de publication

Journal Article

Langues

eng

Pagination

59

Informations de copyright

Copyright © 2019 Bensaid, Modolo, Merlet, Wendling and Benquet.

Références

Arch Ital Biol. 2012 Jun-Sep;150(2-3):56-90
pubmed: 23165867
J Neurosci Methods. 2016 Feb 15;260:233-51
pubmed: 25843066
Dev Neurobiol. 2011 Jan 1;71(1):45-61
pubmed: 21154909
Curr Opin Neurobiol. 2017 Jun;44:127-131
pubmed: 28486176
Neuroimage. 2015 Apr 15;110:101-9
pubmed: 25620493
IEEE Trans Biomed Eng. 2003 Sep;50(9):1074-85
pubmed: 12943275
PLoS One. 2013 Aug 19;8(8):e71370
pubmed: 23977030
Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14529-34
pubmed: 9826734
Front Comput Neurosci. 2013 Jul 16;7:94
pubmed: 23882212
Prog Brain Res. 1976;45:281-308
pubmed: 1013341
Neuron. 2017 Dec 20;96(6):1403-1418.e6
pubmed: 29268099
Science. 1998 Dec 4;282(5395):1846-51
pubmed: 9836628
Trends Cogn Sci. 2005 Oct;9(10):474-80
pubmed: 16150631
Neural Comput. 2007 Feb;19(2):478-512
pubmed: 17206872
Neural Netw. 2017 Apr;88:65-73
pubmed: 28192762
Clin Neurophysiol. 2014 Jan;125(1):63-8
pubmed: 23927942
J Neurosci. 1996 Oct 15;16(20):6402-13
pubmed: 8815919
Nature. 2013 Nov 7;503(7474):51-8
pubmed: 24201278
Front Neural Circuits. 2016 Jan 14;9:88
pubmed: 26834569
Electroencephalogr Clin Neurophysiol Suppl. 1978;(34):9-18
pubmed: 285858
Nat Neurosci. 2012 Feb 26;15(4):607-12
pubmed: 22366760
Curr Opin Neurobiol. 2014 Jun;26:96-102
pubmed: 24440415
Neuron. 2011 Apr 28;70(2):200-27
pubmed: 21521609
Science. 2018 May 4;360(6388):537-542
pubmed: 29567809
Nat Neurosci. 2007 Jun;10(6):743-53
pubmed: 17515899
Nat Neurosci. 2001 Jul;4(7):752-8
pubmed: 11426233
J Clin Invest. 2006 Jul;116(7):1823-5
pubmed: 16823480
Cogn Neurosci. 2010 Sep;1(3):176-183
pubmed: 20823938
IEEE Trans Biomed Eng. 2003 Jun;50(6):754-67
pubmed: 12814242
Comput Intell Neurosci. 2011;2011:879716
pubmed: 21584256
Elife. 2014 Nov 06;3:
pubmed: 25375253
BMC Neurosci. 2003 Dec 02;4:31
pubmed: 14641936
Phys Rev E Stat Nonlin Soft Matter Phys. 2012 Jan;85(1 Pt 1):011910
pubmed: 22400594
J Neurophysiol. 2008 Oct;100(4):2348-60
pubmed: 18632882
Neuron. 2018 May 2;98(3):602-615.e8
pubmed: 29656873
Neuroimage. 1999 Apr;9(4):377-82
pubmed: 10191166
Nat Commun. 2016 Sep 20;7:12815
pubmed: 27649374
J Neurosci. 2010 Oct 27;30(43):14371-9
pubmed: 20980594
Nat Neurosci. 2007 Apr;10(4):462-8
pubmed: 17334362
Annu Rev Neurosci. 2015 Jul 8;38:171-94
pubmed: 25897876
J Neurosci. 2013 Oct 30;33(44):17373-84
pubmed: 24174670
J Neurosci. 2017 Sep 20;37(38):9132-9148
pubmed: 28821651
J Neurosci. 2016 Nov 9;36(45):11498-11509
pubmed: 27911754
Neuron. 2011 Mar 24;69(6):1188-203
pubmed: 21435562
Curr Opin Neurobiol. 2015 Apr;31:72-80
pubmed: 25233254
PLoS Biol. 2008 Jul 1;6(7):e159
pubmed: 18597554
Hum Brain Mapp. 2015 Nov;36(11):4714-29
pubmed: 26309062
NeuroRehabilitation. 2004;19(4):335-41
pubmed: 15671588
Biol Cybern. 1995 Sep;73(4):357-66
pubmed: 7578475
Eur J Neurosci. 2002 May;15(9):1499-508
pubmed: 12028360
Nature. 2012 Oct 11;490(7419):226-31
pubmed: 23060193
Nat Neurosci. 2014 Aug;17(8):1031-9
pubmed: 25065440
BMC Neurosci. 2004 Nov 02;5:42
pubmed: 15522121
Chaos. 2016 Dec;26(12):123113
pubmed: 28039987
Front Neural Circuits. 2013 Feb 13;7:18
pubmed: 23407686
J Physiol. 2016 May 15;594(10):2719-28
pubmed: 26940751
Kybernetik. 1973 Sep;13(2):55-80
pubmed: 4767470
Neuroimage. 1999 Feb;9(2):179-94
pubmed: 9931268
Neurosci Conscious. 2017 Oct 12;2017(1):nix019
pubmed: 30042851
J Neurophysiol. 2005 Apr;93(4):2194-232
pubmed: 15525801
Neuroreport. 2012 Mar 28;23(5):294-8
pubmed: 22327567
J Neurophysiol. 2009 Oct;102(4):2096-111
pubmed: 19657080
Sci Rep. 2017 May 12;7(1):1843
pubmed: 28500299
Sci Transl Med. 2013 Aug 14;5(198):198ra105
pubmed: 23946194
Nat Neurosci. 2012 Jan 15;15(3):423-30, S1-3
pubmed: 22246433
Exp Neurobiol. 2012 Sep;21(3):113-22
pubmed: 23055789
J Neurophysiol. 1996 Dec;76(6):4152-68
pubmed: 8985908
Nat Neurosci. 2013 Nov;16(11):1662-70
pubmed: 24097044
Neuroimage. 2010 Sep;52(3):1109-22
pubmed: 20034581
Neural Netw. 2011 Aug;24(6):631-45
pubmed: 21435838
Nat Rev Neurosci. 2017 Dec 14;19(1):17-33
pubmed: 29238085
Int J Psychophysiol. 2000 Dec 1;38(3):315-36
pubmed: 11102670
Neuroimage. 2006 Jul 1;31(3):968-80
pubmed: 16530430
Brain Connect. 2012;2(6):291-302
pubmed: 23153273
Nat Neurosci. 2017 Feb 23;20(3):340-352
pubmed: 28230845
J Neurophysiol. 2005 Mar;93(3):1671-98
pubmed: 15537811
Conscious Cogn. 2018 Jan;57:41-53
pubmed: 29169033
J Comput Assist Tomogr. 1998 Mar-Apr;22(2):324-33
pubmed: 9530404
Sci Transl Med. 2013 Oct 23;5(208):208ra148
pubmed: 24154602
Cereb Cortex. 2016 Jun;26(6):2612-25
pubmed: 25979090
Neuron. 2019 Jan 2;101(1):91-102.e4
pubmed: 30472077
Neuroimage. 2003 Nov;20(3):1743-55
pubmed: 14642484
Brain Connect. 2011;1(1):13-36
pubmed: 22432952
Neuroimage. 2010 Sep;52(3):1080-94
pubmed: 20045071
Neuroimage. 2016 Jan 15;125:657-667
pubmed: 26499809
Annu Rev Neurosci. 2012;35:203-25
pubmed: 22443509
Biomed Eng Online. 2010 Sep 06;9:45
pubmed: 20819204
Annu Rev Neurosci. 2009;32:209-24
pubmed: 19400723
Neuron. 2007 Mar 1;53(5):735-46
pubmed: 17329212
Eur J Neurosci. 2007 Jun;25(11):3347-58
pubmed: 17553003
Front Neuroanat. 2016 Dec 20;10:124
pubmed: 28066195
Philos Trans R Soc Lond B Biol Sci. 1998 Nov 29;353(1377):1841-9
pubmed: 9854256
Nat Rev Neurosci. 2016 Jul;17(7):401-9
pubmed: 27225074
Wiley Interdiscip Rev Cogn Sci. 2013 Nov;4(6):609-622
pubmed: 26304267
J Neural Eng. 2020 Jul 03;17(3):036034
pubmed: 32470963
Cell. 2014 Mar 13;156(6):1139-1152
pubmed: 24630718
Nat Rev Neurosci. 2016 May;17(5):307-21
pubmed: 27094080
Neuroscience. 2004;126(2):467-84
pubmed: 15207365
Nature. 2013 Nov 28;503(7477):521-4
pubmed: 24097352
Trends Neurosci. 2012 Jan;35(1):57-67
pubmed: 22154068
Proc Natl Acad Sci U S A. 2010 Feb 9;107(6):2681-6
pubmed: 20133802
Nat Commun. 2016 Nov 29;7:13664
pubmed: 27897179
Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2187-92
pubmed: 18245383
Elife. 2015 Oct 13;4:e08760
pubmed: 26460547
Science. 2006 Sep 8;313(5792):1402
pubmed: 16959998
Neuroimage. 1999 Feb;9(2):195-207
pubmed: 9931269
Neuron. 2012 Jul 26;75(2):330-41
pubmed: 22841317
Curr Biol. 2014 Jan 6;24(1):R18-R20
pubmed: 24405670
J Comput Neurosci. 2014 Aug;37(1):125-48
pubmed: 24402459
Neuron. 2016 Jul 20;91(2):260-92
pubmed: 27477017
Front Syst Neurosci. 2014 May 09;8:83
pubmed: 24847225

Auteurs

Siouar Bensaid (S)

INSERM, Laboratoire Traitement du Signal et de l'Image (LTSI)-U1099, University of Rennes, Rennes, France.

Julien Modolo (J)

INSERM, Laboratoire Traitement du Signal et de l'Image (LTSI)-U1099, University of Rennes, Rennes, France.

Isabelle Merlet (I)

INSERM, Laboratoire Traitement du Signal et de l'Image (LTSI)-U1099, University of Rennes, Rennes, France.

Fabrice Wendling (F)

INSERM, Laboratoire Traitement du Signal et de l'Image (LTSI)-U1099, University of Rennes, Rennes, France.

Pascal Benquet (P)

INSERM, Laboratoire Traitement du Signal et de l'Image (LTSI)-U1099, University of Rennes, Rennes, France.

Classifications MeSH