Patient-Specific Network Connectivity Combined With a Next Generation Neural Mass Model to Test Clinical Hypothesis of Seizure Propagation.

epileptic seizure-like event neural mass model patient-specific brain network model quadratic integrate-and-fire neuron topological network measure

Journal

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

Informations de publication

Date de publication:
2021
Historique:
received: 02 03 2021
accepted: 07 07 2021
entrez: 20 9 2021
pubmed: 21 9 2021
medline: 21 9 2021
Statut: epublish

Résumé

Dynamics underlying epileptic seizures span multiple scales in space and time, therefore, understanding seizure mechanisms requires identifying the relations between seizure components within and across these scales, together with the analysis of their dynamical repertoire. In this view, mathematical models have been developed, ranging from single neuron to neural population. In this study, we consider a neural mass model able to exactly reproduce the dynamics of heterogeneous spiking neural networks. We combine mathematical modeling with structural information from non invasive brain imaging, thus building large-scale brain network models to explore emergent dynamics and test the clinical hypothesis. We provide a comprehensive study on the effect of external drives on neuronal networks exhibiting multistability, in order to investigate the role played by the neuroanatomical connectivity matrices in shaping the emergent dynamics. In particular, we systematically investigate the conditions under which the network displays a transition from a low activity regime to a high activity state, which we identify with a seizure-like event. This approach allows us to study the biophysical parameters and variables leading to multiple recruitment events at the network level. We further exploit topological network measures in order to explain the differences and the analogies among the subjects and their brain regions, in showing recruitment events at different parameter values. We demonstrate, along with the example of diffusion-weighted magnetic resonance imaging (dMRI) connectomes of 20 healthy subjects and 15 epileptic patients, that individual variations in structural connectivity, when linked with mathematical dynamic models, have the capacity to explain changes in spatiotemporal organization of brain dynamics, as observed in network-based brain disorders. In particular, for epileptic patients, by means of the integration of the clinical hypotheses on the epileptogenic zone (EZ), i.e., the local network where highly synchronous seizures originate, we have identified the sequence of recruitment events and discussed their links with the topological properties of the specific connectomes. The predictions made on the basis of the implemented set of exact mean-field equations turn out to be in line with the clinical pre-surgical evaluation on recruited secondary networks.

Identifiants

pubmed: 34539355
doi: 10.3389/fnsys.2021.675272
pmc: PMC8440880
doi:

Types de publication

Journal Article

Langues

eng

Pagination

675272

Informations de copyright

Copyright © 2021 Gerster, Taher, Škoch, Hlinka, Guye, Bartolomei, Jirsa, Zakharova and Olmi.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Biol Cybern. 1978 Nov 10;31(1):15-26
pubmed: 728488
Prog Brain Res. 1976;45:281-308
pubmed: 1013341
Brain. 1998 Dec;121 ( Pt 12):2301-15
pubmed: 9874481
J Math Neurosci. 2017 Dec;7(1):7
pubmed: 28744735
IEEE Trans Neural Syst Rehabil Eng. 2005 Jun;13(2):236-41
pubmed: 16003905
PLoS Comput Biol. 2008 Oct;4(10):e1000196
pubmed: 18846206
PLoS Comput Biol. 2017 Dec 29;13(12):e1005881
pubmed: 29287081
Chaos. 2008 Sep;18(3):037113
pubmed: 19045487
Curr Opin Biomed Eng. 2017 Dec;4:87-96
pubmed: 29532041
Nat Rev Neurosci. 2011 Jan;12(1):43-56
pubmed: 21170073
Trends Neurosci. 1996 May;19(5):202-8
pubmed: 8723208
Electroencephalogr Clin Neurophysiol. 1987 Aug;67(2):101-19
pubmed: 2439287
Front Comput Neurosci. 2013 May 28;7:57
pubmed: 23755005
PLoS Comput Biol. 2015 Dec 10;11(12):e1004642
pubmed: 26657566
Neural Comput. 2007 Feb;19(2):478-512
pubmed: 17206872
Front Comput Neurosci. 2019 Apr 26;13:25
pubmed: 31105545
Neuroimage. 2014 Oct 15;100:135-44
pubmed: 24814212
J Comput Neurosci. 2009 Apr;26(2):159-70
pubmed: 19169801
eNeuro. 2020 Mar 24;7(2):
pubmed: 32066612
J Neurosci. 1991 Aug;11(8):2281-7
pubmed: 1869914
AJNR Am J Neuroradiol. 2009 Oct;30(9):1740-7
pubmed: 19509072
Cell. 2008 Oct 31;135(3):422-35
pubmed: 18984155
PLoS Comput Biol. 2018 May 31;14(5):e1006186
pubmed: 29851959
Neuroimage. 2016 Nov 15;142:135-149
pubmed: 27480624
Brain. 1998 Dec;121 ( Pt 12):2271-99
pubmed: 9874480
Neuroimage. 2015 May 1;111:385-430
pubmed: 25592995
Epilepsia. 2001 Feb;42(2):153-70
pubmed: 11240585
Brain. 2001 Sep;124(Pt 9):1683-700
pubmed: 11522572
Front Hum Neurosci. 2013 Oct 01;7:624
pubmed: 24098281
J Neurophysiol. 2020 Feb 1;123(2):726-742
pubmed: 31774370
IEEE Trans Med Imaging. 2002 May;21(5):493-504
pubmed: 12071620
Psychol Rev. 2014 Jul;121(3):302-36
pubmed: 25090422
Neurosurgery. 2007 Apr;60(4 Suppl 2):260-70; discussion 270-1
pubmed: 17415162
PLoS One. 2018 Mar 27;13(3):e0192842
pubmed: 29584728
J Neurophysiol. 1997 Sep;78(3):1199-211
pubmed: 9310412
Brain. 2017 May 1;140(5):e30
pubmed: 28334981
J Neurol Neurosurg Psychiatry. 2012 Dec;83(12):1238-48
pubmed: 22917671
Sci Rep. 2016 Jul 07;6:29215
pubmed: 27384316
Front Comput Neurosci. 2016 Sep 12;10:97
pubmed: 27672364
Epilepsia. 2013 Feb;54(2):370-6
pubmed: 23106394
Epilepsia. 2012 Sep;53(9):e166-9
pubmed: 22709380
IEEE Trans Med Imaging. 1999 Aug;18(8):712-21
pubmed: 10534053
Neuroimage. 2000 May;11(5 Pt 1):359-69
pubmed: 10806021
Quant Imaging Med Surg. 2015 Apr;5(2):247-63
pubmed: 25853083
Phys Rev Lett. 2016 Jun 10;116(23):238101
pubmed: 27341262
J Clin Neurophysiol. 1986 Apr;3(2):113-30
pubmed: 3084558
Clin Neurophysiol. 2001 Apr;112(4):565-82
pubmed: 11275528
Brain. 2005 Jul;128(Pt 7):1556-70
pubmed: 15817517
Neural Comput. 2011 Dec;23(12):3232-86
pubmed: 21919787
Epilepsia. 2017 Jul;58(7):1131-1147
pubmed: 28543030
J Neurosci Methods. 2016 Feb 15;260:233-51
pubmed: 25843066
Epilepsy Behav. 2010 Mar;17(3):310-23
pubmed: 20163993
PLoS Comput Biol. 2013 Oct;9(10):e1003301
pubmed: 24204236
Neuroimage. 2002 Jan;15(1):273-89
pubmed: 11771995
Drug Discov Today Dis Models. 2008;5(1):45-57
pubmed: 19190736
Epilepsia. 2013 May;54(5):772-82
pubmed: 23586531
Neurosurg Rev. 2019 Sep;42(3):639-647
pubmed: 30006663
J Neurophysiol. 1988 Oct;60(4):1481-96
pubmed: 3193167
Front Comput Neurosci. 2020 May 28;14:47
pubmed: 32547379
Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):6179-84
pubmed: 18375756
Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9515-9
pubmed: 7568165
Neuroimage. 2011 Apr 1;55(3):920-32
pubmed: 21195779
Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3747-52
pubmed: 15007165
PLoS Comput Biol. 2019 Feb 25;15(2):e1006805
pubmed: 30802239
Neuron. 2016 Sep 7;91(5):1170-1182
pubmed: 27568515
Hum Brain Mapp. 2009 May;30(5):1580-91
pubmed: 18661506
Nat Methods. 2020 Mar;17(3):261-272
pubmed: 32015543
Epilepsia. 2009 Jul;50(7):1793-803
pubmed: 19453705
Hum Brain Mapp. 2002 Nov;17(3):143-55
pubmed: 12391568
J Theor Biol. 2009 Apr 21;257(4):527-32
pubmed: 19150365
Eur J Neurosci. 2002 May;15(9):1499-508
pubmed: 12028360
Brain. 2004 Jul;127(Pt 7):1496-506
pubmed: 15155522
Brain. 2017 Oct 1;140(10):2639-2652
pubmed: 28969369
Brain. 2002 Aug;125(Pt 8):1709-18
pubmed: 12135963
Clin Neurophysiol. 1999 Mar;110(3):524-37
pubmed: 10363776
Phys Rev Lett. 2021 Jul 16;127(3):038301
pubmed: 34328756
PLoS Comput Biol. 2014 Sep 25;10(9):e1003823
pubmed: 25255443
Epilepsia. 2010 Apr;51(4):573-82
pubmed: 19845730
Neuroimage. 2015 Aug 15;117:343-57
pubmed: 25837600
Neuroimage. 2012 Aug 15;62(2):782-90
pubmed: 21979382
Chaos. 2020 Dec;30(12):123130
pubmed: 33380049
Hum Brain Mapp. 2009 Sep;30(9):2701-21
pubmed: 19107753
PLoS Comput Biol. 2011 Dec;7(12):e1002298
pubmed: 22215992
Neuroimage. 2006 Jul 15;31(4):1487-505
pubmed: 16624579
Nat Neurosci. 2001 Jan;4(1):52-62
pubmed: 11135645
Brain. 2017 Feb;140(2):319-332
pubmed: 28011454
Neuroimage. 2012 Sep;62(3):1924-38
pubmed: 22705374
Front Neural Circuits. 2018 Feb 06;12:3
pubmed: 29467627
Phys Rev Lett. 2020 Dec 11;125(24):248101
pubmed: 33412049
Biol Cybern. 2013 Feb;107(1):83-94
pubmed: 23132433
Int J Psychophysiol. 2000 Dec 1;38(3):315-36
pubmed: 11102670
Neuroimage. 2006 Jul 1;31(3):968-80
pubmed: 16530430
Epilepsy Behav. 2009 Jul;15(3):278-86
pubmed: 19366638
Front Neurol. 2020 Feb 11;11:74
pubmed: 32117033
PLoS Comput Biol. 2020 Sep 28;16(9):e1008206
pubmed: 32986695
Nat Commun. 2018 Mar 14;9(1):1088
pubmed: 29540685
Chaos. 2020 May;30(5):053121
pubmed: 32491891
Clin Neurophysiol. 1999 Nov;110(11):1842-57
pubmed: 10576479
J Neurosci. 2007 Feb 28;27(9):2424-32
pubmed: 17329441
Neuroimage. 2013 Feb 15;67:298-312
pubmed: 23238430
PLoS Comput Biol. 2020 Dec 15;16(12):e1008533
pubmed: 33320855
J Comput Neurosci. 2010 Jun;28(3):375-87
pubmed: 20135212
Brain. 2017 Mar 1;140(3):641-654
pubmed: 28364550
Neuron. 2000 Feb;25(2):449-57
pubmed: 10719898
Neuroimage. 2004;23 Suppl 1:S208-19
pubmed: 15501092
Biophys J. 1972 Jan;12(1):1-24
pubmed: 4332108
Neuroimage. 2012 Feb 1;59(3):2644-60
pubmed: 21945465
Neurosurgery. 1992 Jul;31(1):59-71; discussion 71-2
pubmed: 1641111
Elife. 2018 Jan 08;7:
pubmed: 29308767
Biosystems. 2001 Nov-Dec;63(1-3):89-99
pubmed: 11595332
Brain. 2011 Oct;134(Pt 10):2898-911
pubmed: 21975587
Confin Neurol. 1966;27(1):91-4
pubmed: 5334025
Rev Neurol (Paris). 2002 May;158(5 Pt 2):4S55-64
pubmed: 11997752
Cogn Neurodyn. 2008 Mar;2(1):29-38
pubmed: 19003471
Magn Reson Med. 2000 Oct;44(4):625-32
pubmed: 11025519
Neuroimage. 2016 Oct 15;140:174-87
pubmed: 26883068
PLoS Comput Biol. 2018 Oct 11;14(10):e1006403
pubmed: 30307937
J R Soc Interface. 2005 Mar 22;2(2):113-27
pubmed: 16849171
J Comput Neurosci. 2007 Feb;22(1):63-80
pubmed: 16998642
Schizophr Res. 2015 Mar;162(1-3):22-8
pubmed: 25660467
J Neurosurg. 1999 Jul;91(1):73-9
pubmed: 10389883
J Neurosurg. 1999 Mar;90(3):478-83
pubmed: 10067916
Arch Ital Biol. 2010 Sep;148(3):189-205
pubmed: 21175008
Clin Neurophysiol. 2018 Apr;129(4):829-841
pubmed: 29482079
J Neurol Neurosurg Psychiatry. 2012 Sep;83(9):903-9
pubmed: 22764263
Prog Neurobiol. 2012 Sep;98(3):302-15
pubmed: 22480752
Epilepsia. 2002 Mar;43(3):219-27
pubmed: 11906505
J Neurophysiol. 2003 May;89(5):2707-25
pubmed: 12612051
J Neurosci. 2014 Nov 5;34(45):15009-21
pubmed: 25378166
Brain. 2014 Aug;137(Pt 8):2210-30
pubmed: 24919973
J Neurosci. 2013 Jul 3;33(27):11100-15
pubmed: 23825415
Lancet Neurol. 2016 Apr;15(4):420-33
pubmed: 26925532
Philos Trans A Math Phys Eng Sci. 2009 Mar 28;367(1891):1145-61
pubmed: 19218156
Proc Natl Acad Sci U S A. 2012 Dec 18;109(51):21116-21
pubmed: 23213262
Proc Natl Acad Sci U S A. 2020 Apr 28;117(17):9566-9576
pubmed: 32284420
Neuroimage. 2007 May 1;35(4):1459-72
pubmed: 17379540
Epilepsia. 1991 Nov-Dec;32(6):822-37
pubmed: 1743154
J Theor Biol. 2006 Sep 7;242(1):171-87
pubmed: 16620870
Lancet. 2011 Oct 15;378(9800):1388-95
pubmed: 22000136
Phys Rev Lett. 2018 Sep 21;121(12):128301
pubmed: 30296134
Chaos. 2018 Apr;28(4):045112
pubmed: 31906648
Epilepsia. 2006 Jan;47(1):98-107
pubmed: 16417537
PLoS One. 2013 Aug 13;8(8):e71369
pubmed: 23967201
J Neurosci. 1998 Nov 1;18(21):9002-9
pubmed: 9787005
Clin Neurophysiol. 2001 Sep;112(9):1746-60
pubmed: 11514258
PLoS Comput Biol. 2017 Aug 17;13(8):e1005637
pubmed: 28817568
Ann Neurol. 2012 Feb;71(2):169-78
pubmed: 22367988
PLoS Comput Biol. 2019 May 9;15(5):e1007019
pubmed: 31071085
Electroencephalogr Clin Neurophysiol. 1992 Feb;82(2):155-9
pubmed: 1370786
Kybernetik. 1974 May 31;15(1):27-37
pubmed: 4853232
Curr Opin Neurol. 2008 Aug;21(4):446-51
pubmed: 18607205
J Neurol Neurosurg Psychiatry. 2003 Apr;74(4):471-8
pubmed: 12640066
Radiology. 2014 Mar;270(3):842-8
pubmed: 24475828
Front Physiol. 2012 Jul 17;3:281
pubmed: 22934035
Elife. 2020 Jul 21;9:
pubmed: 32691734
J Comput Neurosci. 2009 Apr;26(2):171-83
pubmed: 19083088
Phys Rev Lett. 2018 Jun 29;120(26):264101
pubmed: 30004770
Neuroimage. 2012 Aug 15;62(2):774-81
pubmed: 22248573
Chaos. 2013 Dec;23(4):046111
pubmed: 24387590
Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):8128-33
pubmed: 10869419
N Engl J Med. 2000 Feb 3;342(5):314-9
pubmed: 10660394

Auteurs

Moritz Gerster (M)

Institut für Theoretische Physik, Technische Universität Berlin, Berlin, Germany.

Halgurd Taher (H)

Inria Sophia Antipolis Méditerranée Research Centre, MathNeuro Team, Valbonne, France.

Antonín Škoch (A)

National Institute of Mental Health, Klecany, Czechia.
MR Unit, Department of Diagnostic and Interventional Radiology, Institute for Clinical and Experimental Medicine, Prague, Czechia.

Jaroslav Hlinka (J)

National Institute of Mental Health, Klecany, Czechia.
Institute of Computer Science of the Czech Academy of Sciences, Prague, Czechia.

Maxime Guye (M)

Faculté de Médecine de la Timone, Centre de Résonance Magnétique et Biologique et Médicale (CRMBM, UMR CNRS-AMU 7339), Medical School of Marseille, Aix-Marseille Université, Marseille, France.
Assistance Publique -Hôpitaux de Marseille, Hôpital de la Timone, Pôle d'Imagerie, Marseille, France.

Fabrice Bartolomei (F)

Assistance Publique - Hôpitaux de Marseille, Hôpital de la Timone, Service de Neurophysiologie Clinique, Marseille, France.

Viktor Jirsa (V)

Aix Marseille Université, Inserm, Institut de Neurosciences des Systèmes, UMRS 1106, Marseille, France.

Anna Zakharova (A)

Institut für Theoretische Physik, Technische Universität Berlin, Berlin, Germany.

Simona Olmi (S)

Inria Sophia Antipolis Méditerranée Research Centre, MathNeuro Team, Valbonne, France.
Consiglio Nazionale delle Ricerche, Istituto dei Sistemi Complessi, Sesto Fiorentino, Italy.

Classifications MeSH