Depth/Surface Relationships: Confronting noninvasive measures to intracerebral EEG Christian G Bénar Institut de Neurosciences des Systèmes; INSERM, Aix-Marseille Université christian.benar@univ-amu.fr OHBM2015 - Electromagnetical Neuroimaging and Multimodal Integration
EEG and MEG are surface recordings MEG EEG - M/EEG are mainly sensitive to the synchronous activity of pyramidal cells in neocortex - Little influence of skull conductivity on MEG - Purely radial sources not visible in MEG
Some open questions Extent of cortex that is necessary for recording activity on MEG/EEG? What is the influence of depth and architectony on detectability? (e.g. hippocampus, amygdala) hippocampus To what extent can EEG/MEG record high frequency activity (gamma, ripples, fast ripples) Yuval-Greenberg et al 2008
How accurate is the inverse problem? The inverse problem is ill posed It requires mathematical hypotheses that may not have physiological grounding There are model imprecisions (skull conductivity, anisotropy ) Baillet et al 2001
Intracranial EEG Used during presurgical evaluation of epilepsy, as a second step after non-invasive methods Allow defining the extent of cortex to be resected surgically Provides a formidable opportunity for validating noninvasive methods
INTRACRANIAL RECORDINGS
Subdural grids Grid placed at the surface of the cortex (Tao et al 2005)
Stereotaxic EEG (SEEG) Electrodes placed directly within the brain (Bancaud and Talairach 1962) Trebuchon da Fonseca et al 2009
DETECTABILITY AS A FUNCTION OF SOURCE EXTENT
Cooper et al 1965 wet skull polythene V 6cm2 (1 inch 2 ) are necessary to measure a potential at the surface
Cooper revisited Tao et al 2005: 10 cm2 for detectability in EEG Oishi et al 2002: 3 cm2 in MEG NB: raw signals; averaging increases signal to noise ratio by a factor of ~sqrt(n)
Effect of source configuration Sleep spindle visible in: MEG +EEG EEG only MEG only Manshanden et al 2002 MEG and EEG are complementary!
VALIDATION OF SOURCE LOCALIZATION IN EPILEPSY
Merlet and Gotman 1999 28 scalp EEG (separate recordings) ; during SEEG: 8 scalp EEG for matching epileptic spikes; Spikes modelled by 1 to 3 dipoles Distance between main dipole and main SEEG contact: 11 ± 4 mm Propagation patterns were confirmed Activity from focal sources not visible (at least 8 intracerebral contacts)
Gavaret et al 2004: temporal epilepsy 64 channel EEG medial lateral - Patients with purely mesial activity : not visible at surface - Lateral activity can be localized with good precision
Gavaret et al 2006: frontal epilepsy 64 channel EEG SEEG SEEG Anterior cingulate is well localized Only lateral part of orbito frontal -> architectony seems more important than depth
Gavaret et al BTOP 2014 Case study: Bilateral occipital sources SEEG MEG reveals bilateral sources Sources are confirmed by SEEG
Mégevand et al 2013: comparison with spiking and seizure onset zone 38 patients with subdural grids; 64-128 EEG channels Median distance EEG source with grid point : 15 mm No difference in accuracy between patients with temporal or extra-temporal epilepsy Good prediction of the seizure onset zone
MEG ICA networks (1) Extraction of epileptic components from surface recordings Malinowska et al Hum Brain Mapp 2013 See also Kobayashi et al 1999, Ossadtchi et al 2004, 2005
MEG MEG ICA networks (2) L SEEG -> very good match between surface and depth recordings Malinowska et al, Hum Brain Mapp 2013
MEG ICA networks (3) MEG L SEEG L Malinowska et al, Hum Brain Mapp 2013 -> surface recording only sees part of the network
Limitations of separate recordings Do not warrant recording the exact same activity Fluctuations can be due to state of vigilance, medication Do not permit using inter-event fluctuations as a source of information on the relations between modalities See EEG-fMRI single-trial evoked potentials studies (Debener et al 2005 etc )
SIMULTANEOUS RECORDINGS
Alarcon et al 1994 Simultaneous scalp EEG foramen ovale Surface recordings are sensitive only to the propagated activity
Lantz et al 2001 22 scalp EEG recorded simultaneously with subdural electrodes Lantz et al 1996, 1997 Epifocus source localization Sources can be localized with sublobar accuracy: medial vs lateral subtemporal; anterior vs posterior lateral temporal
Santiuste 2008 Simultaneous MEG / 1 SEEG electrode Detection of 95 % of neocortical spikes, but only 25 to 60 % of spikes from mesial structures
Simultaneous EEG-MEG-SEEG of Evoked activity Dubarry et al, NIMG 2014 Evoked activity (checkerboard) can be captured simultaneously on the three modalities
Single trial analysis Dubarry et al, NIMG 2014 Single-trial activity can be captured thanks to independant component analysis -> this opens the way to investigate trial-to-trial coupling between surface and depth recordings POSTER 2239: SEEG in language
Application : ICA versus beamformer In a focal case of epilepsy, beamformer and ICA give very similar results for recovering the spikes seen in simultaneously recorded SEEG M. Woodman in prep POSTERS 2271T, 3327 Th
CHALLENGING SITUATIONS: DEEP ACTIVITY HIGH FREQUENCIES
Deep Structures Dalal et al 2013, reading task, zero lag correlation between hippocampus and MEG signals Sylvain Baillet: Comparison of virtual electrode in hippocampus and SEEG recording
Averaging based on hippocampus activity Wennberg et al 2011 Spikes in hippocampus; N=43; low amplitude on scalp (5-10 µv) Koessler et al N=368, amplitude 7µV (snr=-2.1db on raw data) See also Merlet et al 1998
Biophysical/computational modelling Attal and Schwartz 2013 Biophysical model of hippocampus and amygdala Attal et al 2012: computational modelling for estimating hidden variables
High frequency oscillations Rampp et al 2010 simultaneous subdural/meg : high gamma (~80Hz) can be seen on MEG Zelmann et al 2014 simultaneous ECoG/EEG: Ripples fast ripples (100-300Hz) can be seen on surface EEG Recent reports of even higher frequencies Xiang et al 2010: 900 Hz Usui et al 2015 >1000 Hz (!)
CONCLUSIONS
«Take home» message Intracerebral recordings confirm surface recordings in a large proportion of cases Neocortical sources with sufficient extent (signal to noise increase with averaging) In some favorable cases deep structures can be observed Intracerebral EEG keeps a higher sensitivity (MEG/EEG see the «tip of the iceberg») This can be improved by signal processing and modelling Simultaneous recording and computational/biophysical modelling could improve the understanding of signals and strategies to be used
Thank you!