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Institut de Neurosciences des Systèmes Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille [email protected] Workshop on Scale-free Dynamics and Networks in Neurosciences, October 21-24, 2013, Montréal
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Page 1: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Interictal epileptic networks in MEG and SEEG

Christian Bénar Institut de Neurosciences des Systèmes, Marseille

[email protected]

Workshop on Scale-free Dynamics and Networks in

Neurosciences, October 21-24, 2013, Montréal

Page 2: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Overview • Context

• Characterization of networks

– Spike versus oscillations – Strategy 1: Source localization – Strategy 2: ICA

• Simultaneous recordings of EEG/MEG/SEEG

Page 3: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Overview • Context

• Characterization of networks

– Spike versus oscillations – Strategy 1: Source localization – Strategy 2: ICA

• Simultaneous recordings of EEG/MEG/SEEG

Page 4: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Presurgical Evaluation • The goal of presurgical evaluation is to remove

the epileptogenic zone « the minimum amount of cortex to be removed in order to render the

patient seizure-free » H. Lüders « the zone of primary organization of seizures » Talairach and Bancaud

MEG/EEG SEEG

(intracerebral EEG)

Semiology

Phase 1 Phase 2 Surgery

Page 5: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Magnetoencephalography

Marseille MEG platform, 248 sensors

1 2 3

4 5 6

L R

EEG

L R 1 2 3

4 5 6

MEG

Gavaret et al Brain Topogr in press

Page 6: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Stereotaxic EEG (SEEG)

Barbeau et al 2008: evoked activity during face recognition

SEEG implantation in deep regions

Page 7: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Objectives

MEG/EEG SEEG (intracerebral EEG)

Phase 1 Phase 2 Surgery

Optimize signal processing strategies by confronting MEEG with SEEG

Guide SEEG implantation

Avoid SEEG in some cases

Page 8: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Seizure start: focus or network ?

Bartolomei et al 2001 Start of seizure mesial + neocortical

Bartolomei et al 2008 Epileptogenicity index

Page 9: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

What about interictal activity? • Non-invasive tools mostly investigate interictal

discharges (i.e., between seizures)

• Simpler propagation patterns than seizures

• Complex relationship with seizure (Gotman 1989)

• Present network dynamic patterns: indication on propagation pathways?

Page 10: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Existence of extended interictal networks in SEEG

Page 11: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

« preictal build up »

Schwartz et al 2011

The interictal networks fluctuate in time

Page 12: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Gavaret et al J Clin Neurophysiol 2006

time (s)

frequ

ency

(Hz)

2 2.05 2.1 2.15 2.2 2.25 2.3 2.35 2.4 2.45 2.510

15

20

25

30

35

40

45

50

55

60

MEG discharge at 30 Hz

Interictal spikes and oscillations Average spike

Interictal activity can manifest as spikes, oscilation or a mixture of both (« moustache ») Transient patterns (not 1/f !!)

Page 13: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Overview • Context

• Characterization of networks

– Spike versus oscillations – Strategy 1: Source localization – Strategy 2: ICA

• Simultaneous recordings of EEG/MEG/SEEG

Page 14: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Rationale • Characterize interictal epileptic networks, leading

region(s) with non-invasive tools

• Investigate differences betwen spikes and oscillations

• Strategies

– Time-frequency /time-scale analysis – Source localization – Independent component analysis (ICA)

Page 15: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Overview • Context

• Characterization of networks

– Spike vs oscillations: methodological points – Strategy 1: Source localization – Strategy 2: ICA

• Simultaneous recordings of EEG/MEG/SEEG

Page 16: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Point 1: frequency overlap

-100

0

100

Original Signalam

plitu

de (u

V)

-50

0

50Filtered Signal (8-12 Hz)

time (s)

freq

uenc

y (H

z)

Time-Frequency Analysis

200 400 600 800 1000 1200 1400248

153058

Transients and oscillations overlap in frequency: difficulty of extracting « pure » oscillatory part

Page 17: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

« False ripples » (1) : transients

Bénar et al 2010

Filtering spikes or artefacts gives « false » oscillations

Page 18: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

« False ripples » (2): harmonics

Filtering signals with harmonics gives also « false » oscillations

Bénar et al 2010

Page 19: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Separation of oscillations and transients Oscillations

Jmail et al 2010

In real data, dependence on fit between atoms and data Current collaboration with S Hitziger, T Papadopoulo, M Clerc (INRIA Sophia Antipolis): definition of atoms from data

Page 20: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Point 2: multi-trial aspects

Benar et al 2009

« consensus matching pursuit » -> Taking into account interevent variability in atomic decomposition

Page 21: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Point 3: Interactions background/activity

Indication of phase resetting in primary visual cortex

Krieg et al 2010

Page 22: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Overview • Context

• Characterization of networks

– Spike versus oscillations – Strategy 1: Source localization – Strategy 2: ICA

• Simultaneous recordings of EEG/MEG/SEEG

Page 23: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Spike networks vs oscillation networks

N. Jmail

Page 24: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Spike networks vs oscillation networks

Nawel Jmail

-non-invasive results concordant with SEEG: 89 % for spikes , 75 % for oscillations). -Only partial overlap between networks (38 % of total number of regions in MEG, 50% in SEEG). -Current directions: automatize extraction of networks, increase number of patients

Page 25: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Overview • Context

• Characterization of networks

– Spike versus oscillations – Strategy 1: Source localization – Strategy 2: ICA

• Simultaneous recordings of EEG/MEG/SEEG

Page 26: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

ICA on continuous MEG

Malinowska et al, Hum Brain Mapp 2013

Page 27: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Co-occurrence testing

Similar principle than Bourien et al 2005

Page 28: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Co-occurrence graphs

• significant direction

• spike co-occurrences (significance with non-parametric technique)

Malinowska et al, Hum Brain Mapp 2013

• leaders: delays or conditional probability

Page 29: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Source localisation on components

ICA1

ICA7

ICA6

ICA1

ICA6

ICA7

Page 30: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Resultats (1): good concordance

L

MEG

SEEG

Malinowska et al, Hum Brain Mapp 2013

Page 31: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

L

MEG

SEEG

L

Results (2): partial concordance

Malinowska et al, Hum Brain Mapp 2013

Page 32: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Comparison with ictal networks Interictal, SEEG Ictal, SEEG

Malinowska et al, Hum Brain Mapp 2013

Page 33: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Networks: discussion • One can reliably extract interictal networks from

non-invasive MEG data

• One must be cautious on possible undetectable leaders: need to investigate depth/surface relationships

• Need to validate clinically on larger population of patients (seizure freedom)

• Future direction: use of virtual brain simulations

Page 34: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Overview • Context

• Characterization of networks

– Spike versus oscillations – Strategy 1: Source localization – Strategy 2: ICA

• Simultaneous recordings of EEG/MEG/SEEG

Page 35: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de Neurosciences des Systèmes

Rationale

• Previous comparison MEEG/SEEG done on separate recordings

• Not guaranteed to visualize exact same activity (temporal fluctuations)

• Cannot use single trial fluctuations as source of information (see simultaneous EEG-fMRI)

• Need to record simultaneous data

Page 36: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Recording and Artefacts

Page 37: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Simultaneous MEG-EEG-SEEG

Dubarry et al, under review

Page 38: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Source localization

Dubarry et al, under review

Page 39: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Single trial analysis

Dubarry et al, under review

Page 40: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Institut de neurosciences des systèmes

Simultaneous recordings: discussion

• We have shown the feasibility of simultaneous EEG/MEG/intracerebral EEG - Average - Single trial analysis

• Issue of artefacts: need further work on denoising

• Future directions: mapping of sensitivity of measures according to location/extent of activity

Page 41: Interictal epileptic networks in MEG and SEEG · 2013-11-14 · Interictal epileptic networks in MEG and SEEG Christian Bénar Institut de Neurosciences des Systèmes, Marseille .

Acknowledgments

Neurologists P Chauvel F Bartolomei M Gavaret A Trébuchon Da Fonseca

Neuropsychology C Liegeois-Chauvel

Engineers JM Badier S Chen B Colombet M Woodman B Giusiano

Students, postdocs U Malinowska N Jmail AS Dubarry

Neurosurgeons J Régis R Caron

Collaborations: T Papadopoulo, M Clerc (INRIA Sophia); X Alario (LNC, Marseille); F Wendling (LTSI, Rennes) M Guye, JP Ranjeva (CEMEREM, Marseille), C Grova, JM Lina (Montreal)

Funding: Agence National de la Recherche (ANR Multimodel) Fondation pour la recherche médical (FRM)


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