We study patterns of partial synchronization in a network of FitzHugh–Nagumo oscillators with empirical structural connectivity measured in human subjects. We report the spontaneous occurrence of synchronization phenomena that closely resemble the ones seen during epileptic seizures in humans. In order to obtain deeper insights into the interplay between dynamics and network topology, we perform long-term simulations of oscillatory dynamics on different paradigmatic network structures: random networks, regular nonlocally coupled ring networks, ring networks with fractal connectivities, and small-world networks with various rewiring probability. Among these networks, a small-world network with intermediate rewiring probability best mimics the findings achieved with the simulations using the empirical structural connectivity. For the other network topologies, either no spontaneously occurring epileptic-seizure-related synchronization phenomena can be observed in the simulated dynamics, or the overall degree of synchronization remains high throughout the simulation. This indicates that a topology with some balance between regularity and randomness favors the self-initiation and self-termination of episodes of seizure-like strong synchronization.

1.
A.
Pikovsky
,
M.
Rosenblum
, and
J.
Kurths
,
Synchronization: A Universal Concept in Nonlinear Sciences
, 1st ed. (
Cambridge University Press
,
Cambridge
,
2001
).
2.
S.
Boccaletti
,
A.
Pisarchik
,
C.
del Genio
, and
A.
Amann
,
Synchronization: From Coupled Systems to Complex Networks
(
Cambridge University Press
,
Cambridge
,
2018
).
3.
W.
Singer
,
Eur. J. Neurosci.
48
,
2389
(
2018
).
4.
K.
Lehnertz
,
S.
Bialonski
,
M.
Horstmann
,
D.
Krug
,
A.
Rothkegel
,
M.
Staniek
, and
T.
Wagner
,
J. Neurosci. Methods
183
,
42
(
2009
).
5.
P.
Jiruska
,
M.
de Curtis
,
J.
Jefferys
,
C.
Schevon
,
S.
Schiff
, and
K.
Schindler
,
J. Physiol.
591
(
4
),
787
(
2013
).
6.
V.
Jirsa
,
W.
Stacey
,
P.
Quilichini
,
A.
Ivanov
, and
C.
Bernard
,
Brain
137
,
2210
(
2014
).
7.
K.
Lehnertz
,
G.
Ansmann
,
S.
Bialonski
,
H.
Dickten
,
C.
Geier
, and
S.
Porz
,
Physica D
267
,
7
(
2014
).
8.
D.
Bassett
,
P.
Zurn
, and
J.
Gold
,
Nat. Rev. Neurosci.
19
,
566
(
2018
).
9.
A.
Ngugi
,
S.
Kariuki
,
C.
Bottomley
,
I.
Kleinschmidt
,
J.
Sander
, and
C.
Newton
,
Neurology
77
,
1005
(
2011
).
10.
R.
Fisher
,
W.
van Emde Boas
,
W.
Blume
,
C.
Elger
,
P.
Genton
,
P.
Lee
, and
J.
Engel
, Jr.,
Epilepsia
46
,
470
(
2005
).
13.
M.
Richardson
,
J. Neurol. Neurosurg. Psychiatry
83
,
1238
(
2012
).
14.
L.
Kuhlmann
,
K.
Lehnertz
,
M.
Richardson
,
B.
Schelter
, and
H. P.
Zaveri
,
Nat. Rev. Neurol.
14
,
618
(
2018
).
15.
S.
Boccaletti
,
V.
Latora
,
Y.
Moreno
,
M.
Chavez
, and
D.
Hwang
,
Phys. Rep.
424
,
175
(
2006
).
16.
E.
Schöll
,
S.
Klapp
, and
P.
Hövel
, Control of Self-Organizing Nonlinear Systems, edited by E. Schöll, S. Klapp, and P. Hövel (Springer, Berlin, 2016).
17.
C.
Bick
,
M.
Goodfellow
,
C.
Laing
, and
E.
Martens
,
J. Math. Neurosci.
10
,
9
(
2020
).
18.
P.
Wolf
and
S.
Beniczky
,
Expert Rev. Neurother.
14
,
787
(
2014
).
19.
F.
Lopes Da Silva
,
W.
Blanes
,
S.
Kalitzin
,
J.
Parra
,
P.
Suffczynski
, and
D.
Velis
,
Epilepsia
44
,
72
(
2003
).
20.
E.
Ferlazzo
,
B.
Zifkin
,
E.
Andermann
, and
F.
Andermann
,
Brain
128
,
700
(
2005
).
21.
S.
Ponten
,
L.
Douw
,
F.
Bartolomei
,
J.
Reijneveld
, and
C.
Stam
,
Exp. Neurol.
217
,
197
(
2009
).
22.
M.
Chavez
,
M.
Valencia
,
V.
Navarro
,
V.
Latora
, and
J.
Martinerie
,
Phys. Rev. Lett.
104
,
118701
(
2010
).
23.
G.
Baier
,
M.
Goodfellow
,
P.
Taylor
,
Y.
Wang
, and
D.
Garry
,
Front. Physiol.
3
,
281
(
2012
).
24.
O.
Benjamin
,
T. H.
Fitzgerald
,
P.
Ashwin
,
K.
Tsaneva-Atanasova
,
F.
Chowdhury
,
M.
Richardson
, and
J.
Terry
,
J. Math. Neurosci.
2
,
1
(
2012
).
25.
J.
Terry
,
O.
Benjamin
, and
M.
Richardson
,
Epilepsia
53
,
e166
(
2012
).
26.
G.
Petkov
,
M.
Goodfellow
,
M.
Richardson
, and
J.
Terry
,
Front. Neurol.
5
,
261
(
2014
).
27.
M.
Goodfellow
,
K.
Schindler
, and
G.
Baier
,
Neuroimage
55
,
920
(
2011
).
28.
M.
Goodfellow
and
P.
Glendinning
,
J. Math. Neurosci.
3
,
17
(
2013
).
29.
M.
Lopes
,
M.
Richardson
,
E.
Abela
,
C.
Rummel
,
K.
Schindler
,
M.
Goodfellow
, and
J.
Terry
,
PLoS Comput. Biol.
13
,
e1005637
(
2017
).
30.
T.
Chouzouris
,
I.
Omelchenko
,
A.
Zakharova
,
J.
Hlinka
,
P.
Jiruska
, and
E.
Schöll
,
Chaos
28
,
045112
(
2018
).
31.
A.
Rothkegel
and
K.
Lehnertz
,
Europhys. Lett.
105
,
30003
(
2014
).
32.
W.
Poel
,
A.
Zakharova
, and
E.
Schöll
,
Phys. Rev. E
91
,
022915
(
2015
).
33.
J.
Sawicki
, “Delay controlled partial synchronization in complex networks,” Springer theses (Springer, Heidelberg, 2019).
34.
E.
Schöll
,
A.
Zakharova
, and
R.
Andrzejak
, “
Chimera states in complex networks
,”
Front. Appl. Math. Stat.
29
,
62
(
2020
).
35.
A.
Zakharova
, Chimera Patterns in Networks: Interplay between Dynamics, Structure, Noise, and Delay, Understanding Complex Systems (Springer, 2020).
36.
R.
Andrzejak
,
C.
Rummel
,
F.
Mormann
, and
K.
Schindler
,
Sci. Rep.
6
,
23000
(
2016
).
37.
A.
Rothkegel
and
K.
Lehnertz
,
New J. Phys.
16
,
055006
(
2014
).
39.
J.
Nagumo
,
S.
Arimoto
, and
S.
Yoshizawa
,
Proc. IRE
50
,
2061
(
1962
).
40.
A.
Chernihovskyi
,
F.
Mormann
,
M.
Müller
,
C.
Elger
,
G.
Baier
, and
K.
Lehnertz
,
J. Clin. Neurophysiol.
22
,
314
(
2005
).
41.
A.
Chernihovskyi
and
K.
Lehnertz
,
Int. J. Bifurc. Chaos
17
,
3425
(
2007
).
42.
N.
Tzourio-Mazoyer
,
B.
Landeau
,
D.
Papathanassiou
,
F.
Crivello
,
O.
Etard
,
N.
Delcroix
,
B.
Mazoyer
, and
M.
Joliot
,
Neuroimage
15
,
273
(
2002
).
43.
I.
Omelchenko
,
O.
Omel’chenko
,
P.
Hövel
, and
E.
Schöll
,
Phys. Rev. Lett.
110
,
224101
(
2013
).
44.
M.
Kiskowski
,
M.
Alber
,
G.
Thomas
,
J.
Glazier
,
N.
Bronstein
,
J.
Pu
, and
S.
Newman
,
Dev. Biol.
271
,
372
(
2004
).
45.
A.
Pereda
,
Nat. Rev. Neurosci.
15
,
250
(
2014
).
46.
P.
Massobrio
,
L.
de Arcangelis
,
V.
Pasquale
,
H.
Jensen
, and
D.
Plenz
,
Front. Syst. Neurosci.
9
,
22
(
2015
).
47.
O.
Omel’chenko
,
M.
Wolfrum
, and
Y.
Maistrenko
,
Phys. Rev. E
81
,
065201(R)
(
2010
).
48.
T.
Melicher
,
J.
Horacek
,
J.
Hlinka
,
F.
Spaniel
,
J.
Tintera
,
I.
Ibrahim
,
P.
Mikolas
,
T.
Novak
,
P.
Mohr
, and
C.
Hoschl
,
Schizophr. Res.
162
,
22
(
2015
).
49.
L.
Ramlow
,
J.
Sawicki
,
A.
Zakharova
,
J.
Hlinka
,
J.
Claussen
, and
E.
Schöll
,
Europhys. Lett.
126
,
50007
(
2019
).
50.
T.
Bal
,
D.
Debay
, and
A.
Destexhe
,
J. Neurosci.
20
,
7478
(
2000
).
51.
H.
Blumenfeld
and
D.
McCormick
,
J. Neurosci.
20
,
5153
(
2000
).
52.
L.
Sadleir
,
K.
Farrell
,
S.
Smith
,
M.
Connolly
, and
I.
Scheffer
,
Neurology
67
,
413
(
2006
).
53.
F.
Mormann
,
K.
Lehnertz
,
P.
David
, and
C.
Elger
,
Physica D
144
,
358
(
2000
).
54.
F.
Mormann
,
T.
Kreuz
,
R.
Andrzejak
,
P.
David
,
K.
Lehnertz
, and
C.
Elger
,
Epilepsy Res.
53
,
173
(
2003
).
55.
S.
Feldt
,
H.
Osterhage
,
F.
Mormann
,
K.
Lehnertz
, and
M.
Zochowski
,
Phys. Rev. E
76
,
eid021920
(
2007
).
56.
A.
Lüttjohann
,
J.
Schoffelen
, and
G.
van Luijtelaar
,
Exp. Neurol.
239
,
235
(
2013
).
57.
A.
Barrat
,
M.
Barthélemy
,
R.
Pastor-Satorras
, and
A.
Vespignani
,
Proc. Natl. Acad. Sci. U.S.A.
101
,
3747
(
2004
).
58.
S.
Boccaletti
and
J.
Bragard
,
Philos. Trans. R. Soc. Lond. A
364
,
2383
(
2006
).
59.
M.
Enright
and
D.
Leitner
,
Phys. Rev. E
71
,
011912
(
2005
).
60.
H.
Hahn
,
M.
Georg
, and
H.
Peitgen
,
Fractals in Biology and Medicine
(
Springer
,
2005
), Vol.
4
.
61.
P.
Katsaloulis
,
D.
Verganelakis
, and
A.
Provata
,
Fractals
17
,
181
(
2009
).
62.
P.
Katsaloulis
,
A.
Ghosh
,
A.
Philippe
,
A.
Provata
, and
R.
Deriche
,
Eur. Phys. J. B
85
,
1
(
2012
).
63.
I.
Omelchenko
,
A.
Provata
,
J.
Hizanidis
,
E.
Schöll
, and
P.
Hövel
,
Phys. Rev. E
91
,
022917
(
2015
).
64.
S.
Plotnikov
,
J.
Lehnert
,
A.
Fradkov
, and
E.
Schöll
,
Phys. Rev. E
94
,
012203
(
2016
).
65.
J.
Sawicki
,
I.
Omelchenko
,
A.
Zakharova
, and
E.
Schöll
,
Eur. Phys. J. B
92
,
54
(
2019
).
66.
D.
Nikitin
,
I.
Omelchenko
,
A.
Zakharova
,
M.
Avetyan
,
A.
Fradkov
, and
E.
Schöll
,
Philos. Trans. R. Soc. A
377
,
20180128
(
2019
).
67.
S.
Krishnagopal
,
J.
Lehnert
,
W.
Poel
,
A.
Zakharova
, and
E.
Schöll
,
Philos. Trans. R. Soc. A
375
,
20160216
(
2017
).
68.
J.
Hizanidis
,
E.
Panagakou
,
I.
Omelchenko
,
E.
Schöll
,
P.
Hövel
, and
A.
Provata
,
Phys. Rev. E
92
,
012915
(
2015
).
69.
S.
Ulonska
,
I.
Omelchenko
,
A.
Zakharova
, and
E.
Schöll
,
Chaos
26
,
094825
(
2016
).
70.
N.
Tsigkri-DeSmedt
,
J.
Hizanidis
,
P.
Hövel
, and
A.
Provata
,
Eur. Phys. J. ST
225
,
1149
(
2016
).
71.
N.
Tsigkri-DeSmedt
,
J.
Hizanidis
,
E.
Schöll
,
P.
Hövel
, and
A.
Provata
,
Eur. Phys. J. B
90
,
139
(
2017
).
72.
J.
Sawicki
,
I.
Omelchenko
,
A.
Zakharova
, and
E.
Schöll
,
Eur. Phys. J. Spec. Top.
226
,
1883
(
2017
).
73.
A.
zur Bonsen
,
I.
Omelchenko
,
A.
Zakharova
, and
E.
Schöll
,
Eur. Phys. J. B
91
,
65
(
2018
).
74.
D.
Watts
and
S.
Strogatz
,
Nature
393
,
440
(
1998
).
75.
P.
Erdös
and
A.
Rényi
,
Publ. Math. Inst. Hung. Acad. Sci.
5
,
17
(
1960
).
76.
R.
Karnatak
,
G.
Ansmann
,
U.
Feudel
, and
K.
Lehnertz
,
Phys. Rev. E
90
,
022917
(
2014
).
77.
G.
Ansmann
,
K.
Lehnertz
, and
U.
Feudel
,
Phys. Rev. X
6
,
011030
(
2016
).
78.
C.
Hilgetag
and
A.
Goulas
,
Brain Struct. Funct.
221
,
2361
(
2016
).
79.
D.
Papo
,
M.
Zanin
,
J.
Martínez
, and
J.
Buldú
,
Front. Hum. Neurosci.
10
,
96
(
2016
).
80.
M.
Gastner
and
G.
Ódor
,
Sci. Rep.
6
,
27249
(
2016
).
81.
S.
Bialonski
,
M.
Horstmann
, and
K.
Lehnertz
,
Chaos
20
,
013134
(
2010
).
82.
J.
Hlinka
,
D.
Hartman
, and
M.
Paluš
,
Chaos
22
,
033107
(
2012
).
83.
J.
Hlinka
,
D.
Hartman
,
N.
Jajcay
,
D.
Tomeček
,
J.
Tintěra
, and
M.
Paluš
,
Chaos
27
,
035812
(
2017
).
84.
M.
Horstmann
,
S.
Bialonski
,
N.
Noennig
,
H.
Mai
,
J.
Prusseit
,
J.
Wellmer
,
H.
Hinrichs
, and
K.
Lehnertz
,
Clin. Neurophysiol.
121
,
172
(
2010
).
85.
G.
Ansmann
and
K.
Lehnertz
,
J. Neurosci. Methods
208
,
165
(
2012
).
86.
M.
Xia
,
J.
Wang
, and
Y.
He
,
PLoS One
8
,
e68910
(
2013
).
87.
F.
Sharbrough
,
J. Clin. Neurophysiol.
8
,
200
(
1991
).
88.
M.
Okamoto
,
H.
Dan
,
K.
Sakamoto
,
K.
Takeo
,
H.
Shimizu
,
S.
Kohno
,
I.
Oda
,
S.
Isobe
,
T.
Suzuki
,
K.
Kohyama
, and
I.
Dan
,
Neuroimage
21
,
99
(
2004
).
89.
M.
Hoke
,
K.
Lehnertz
,
C.
Pantev
, and
B.
Lütkenhöner
, in Brain Dynamics (Springer, 1989), pp. 84–105.
90.
A.
Chernihovskyi
,
C.
Elger
, and
K.
Lehnertz
,
EURASIP J. Adv. Signal Process.
2009
,
582412
.
91.
D.
Kasatkin
,
S.
Yanchuk
,
E.
Schöll
, and
V.
Nekorkin
,
Phys. Rev. E
96
,
062211
(
2017
).
92.
J.
Guo
,
R.
Kim
,
Y.
Chen
,
M.
Negishi
,
S.
Jhun
,
S.
Weiss
,
J.
Ryu
,
X.
Bai
,
W.
Xiao
,
E.
Feeney
,
J.
Rodriguez-Fernandez
,
H.
Mistry
,
V.
Crunelli
,
M.
Crowley
,
L.
Mayes
,
R.
Constable
, and
H.
Blumenfeld
,
Lancet Neurol.
15
,
1336
(
2016
).
93.
C. J.
Kilpatrick
,
S. M.
Davis
,
B. M.
Tress
,
S. C.
Rossiter
,
J. L.
Hopper
, and
M. L.
Vandendriesen
,
Arch. Neurol.
47
,
157
(
1990
).
94.
M.
Goodfellow
,
C.
Rummel
,
E.
Abela
,
M.
Richardson
,
K.
Schindler
, and
J.
Terry
,
Sci. Rep.
6
,
29215
(
2016
).
95.
N.
Sinha
,
J.
Dauwels
,
M.
Kaiser
,
S.
Cash
,
M.
Brandon Westover
,
Y.
Wang
, and
P.
Taylor
,
Brain
140
,
319
(
2016
).
96.
S.
Olmi
,
S.
Petkoski
,
M.
Guye
,
F.
Bartolomei
, and
V.
Jirsa
,
PLoS Comput. Biol.
15
,
e1006805
(
2019
).
97.
J.
Cabral
,
H.
Fernandes
,
T.
Van Hartevelt
,
A.
James
, and
M.
Kringelbach
,
Chaos
23
,
046111
(
2013
).
98.
K. G.
Schilling
,
A.
Daducci
,
K.
Maier-Hein
,
C.
Poupon
,
J.
Houde
,
V.
Nath
,
A. W.
Anderson
,
B. A.
Landman
, and
M.
Descoteaux
,
Magn. Res. Imaging
57
,
194
(
2019
).
99.
J.
Hlinka
and
S.
Coombes
,
Eur. J. Neurosci.
36
,
2137
(
2012
).

Supplementary Material

You do not currently have access to this content.