ReviewA personalized history of EEG–fMRI integration
Introduction
Peter Bandettini asked all authors of this Special Issue to make contributions from the “unique perspective of each author”. This is why the following account in parts will be biased toward the European history of EEG–fMRI integration, specifically a “London perspective” (Hamandi et al., 2004), the one which I was most closely involved with. A more balanced view can be obtained by studying review articles on the topic which will show that many more groups contributed greatly to the field, such as those around John Ives, Franz Schmitt, Steven Warach and Donald Schomer in Boston/U.S.A. (Ives et al., 1993, Warach et al., 1996), John Archer, David Abbott and Graeme Jackson in Melbourne/Australia (Archer et al., 2003a, Archer et al., 2003b), Margitta Seeck, Christoph Michel and Theodor Landis in Geneva/Switzerland (Seeck et al., 1998), Jean Gotman and colleagues in Montréal/Canada (Al-Asmi et al., 2003, Benar et al., 2002, Benar et al., 2003), Alexander Hoffmann, Lorenz Jäger and Maximilian Reiser in Munich/Germany (Hoffmann et al., 2000, Jäger et al., 2002) — just to name a few.
On March 2nd, 2002, Louis Lemieux and Robert Turner held the ‘First Workshop on EEG–fMRI’ at Queen Square in London with David Fish (Institute of Neurology, UCL, UK), Georgio Bonmassar (Hardvard, U.S.A.), John Stern (UCLA, USA), Afraim Salek-Haddadi (Institute of Neurology, UK), Walter Freeman (Berkeley, USA), Arno Villringer (Charité, Germany), Jean Gotman (Montreal Neurological Institute, Canada) and Fabio Babiloni (Roma 1, Italy) as the speakers. I had the opportunity to attend this in retrospect historical meeting accompanying Karsten Krakow. He had completed his PhD at UCL as the first medical fellow (under David Fish) acquiring EEG–fMRI at the National Society for Epilepsy (now called The Epilepsy Society, Chalfont St. Peter, UK) from Queen Square (The National Hospital for Neurology and Neurosurgery, UCL, UK) epilepsy patients (Krakow et al., 1999) with Philip Allen's MR-compatible EEG system (Hamandi et al., 2004, Krakow et al., 1999). Karsten Krakow after his PhD had moved to the Department of Neurology at the Goethe University in Frankfurt (Germany), where I met him starting my fellowship in neurology. It was at that symposium that apart from the speakers I had the opportunity to meet in person some of the “London EEG–fMRI pioneers” including Phil Allen, Oliver Josephs and Mark Symms.
At the inception of EEG–fMRI, advances on the technical as well as the analysis side were tremendous and went hand in hand with one another (first part of this review), while later on, when the first major technical hurdles had been taken and good commercial hard- and software were available, scientific applications and analysis strategies could advance independently of the engineering side of matters (second part). In my opinion, the future progress of EEG–fMRI integration again will depend on further technical advances required to extend current boundaries of EEG–fMRI partly posed by physics and safety limitations (part three).
Section snippets
Driven by epileptologists
The idea of EEG–fMRI integration was clinically motivated and its development driven by the desire of epileptologists to localize electrical sources of epileptic discharges. In November of 1992 John Ives, Steve Warach and Franz Schmitt performed the first EEG recording from within the bore of a Siemens 1.5 T magnet at the Beth Israel Hospital in Boston. A technical article on the accomplishment was published in 1993 (Ives et al., 1993) followed by two clinical articles (Patel et al., 1999,
EEG–fMRI applications in epilepsy
After the main technical hurdles had been taken, EEG–fMRI was applied to series of patients with different epilepsy syndromes including children with the main aim to infer the location of the irritative or seizure onset zones (Rosenow and Lüders, 2001), i.e. the brain regions which are thought to be responsible for a patient's epilepsy. There was the hope of providing useful clinical information particularly in patients undergoing pre-surgical evaluation. A detailed discussion of the literature
Technical challenges
Naturally, the future of simultaneous EEG–fMRI is dependent on technical advances of each modality in isolation as well as the progress in the understanding of the signals and their combined analysis. Like at the inception of EEG–fMRI, safety issues will again be crucial when taking the next steps.
On the EEG side, there is a clear trend toward high-density recordings, i.e. recordings with 128 channels or more benefitting source localization. Bringing this into an MRI set-up, user- and
Summary and conclusion
On June 17th, 2003 in his introduction of the HBM (9th Annual Meeting of the Organization for Human Brain Mapping in New York) satellite symposium ‘EEG–fMRI’, Louis Lemieux thought-provokingly suggested to the 99 attendees (the 100th spending the day with U.S. immigration) that every MRI scanner in the future should be shipped with a compatible EEG system. Many of the audience were already or by now are well-known in the EEG or fMRI world, all acting as multipliers within the growing EEG–fMRI
Acknowledgments
The author is funded by the Bundesministerium für Bildung und Forschung (grant 01 EV 0703) and the Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz (LOEWE, Neuronale Koordination Forschungsschwerpunkt Frankfurt). I would like to thank Philip Allen, Khalid Hamandi, John R. Ives, Karsten Krakow, Louis Lemieux, Afraim Salek-Haddadi, Robert Störmer and Alexander Svojanovksy for sharing insight into the history of EEG–fMRI, their memories and for providing photographs and
References (189)
- et al.
A method for removing imaging artifact from continuous EEG recorded during functional MRI
Neuroimage
(2000) - et al.
Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction
Neuroimage
(1998) - et al.
Analysis of the EEG–fMRI response to prolonged bursts of interictal epileptiform activity
Neuroimage
(2005) - et al.
Correspondence between EEG–fMRI and EEG dipole localisation of interictal discharges in focal epilepsy
Neuroimage
(2006) - et al.
Quality of EEG in simultaneous EEG–fMRI for epilepsy
Clin. Neurophysiol.
(2003) - et al.
The BOLD response to interictal epileptiform discharges
Neuroimage
(2002) - et al.
An investigation of the relationship between BOLD and perfusion signal changes during epileptic generalised spike wave activity
Magn. Reson. Imaging
(2008) - et al.
Feasibility of simultaneous intracranial EEG–fMRI in humans: a safety study
Neuroimage
(2010) - et al.
Symmetrical event-related EEG/fMRI information fusion in a variational Bayesian framework
Neuroimage
(2007) - et al.
Bayesian multi-modal model comparison: a case study on the generators of the spike and the wave in generalized spike-wave complexes
Neuroimage
(2010)
Predicting EEG single trial responses with simultaneous fMRI and Relevance Vector Machine regression
Neuroimage
A study of the brain's resting state based on alpha band power, heart rate and fMRI
Neuroimage
The hemodynamic response of the alpha rhythm: an EEG/fMRI study
Neuroimage
Impact of interictal epileptic activity on normal brain function in epileptic encephalopathy: an electroencephalography–functional magnetic resonance imaging study
Epilepsy Behav.
Improved quality of auditory event-related potentials recorded simultaneously with 3-T fMRI: removal of the ballistocardiogram artefact
Neuroimage
Single-trial EEG–fMRI reveals the dynamics of cognitive function
Trends Cogn. Sci.
Ballistocardiogram artifact reduction in the simultaneous acquisition of auditory ERPS and fMRI
Neuroimage
How wrong can we be? The effect of inaccurate mark-up of EEG/fMRI studies in epilepsy
Clin. Neurophysiol.
Overview of artifact reduction and removal in evoked potential and event-related potential recordings
Phys. Med. Rehabil. Clin. N. Am.
Endogenous cortical rhythms determine cerebral specialization for speech perception and production
Neuron
Acquiring simultaneous EEG and functional MRI
Clin. Neurophysiol.
Concordance between distributed EEG source localization and simultaneous EEG-fMRI studies of epileptic spikes
Neuroimage
EEG–fMRI of idiopathic and secondarily generalized epilepsies
Neuroimage
fMRI temporal clustering analysis in patients with frequent interictal epileptiform discharges: comparison with EEG-driven analysis
Neuroimage
BOLD changes occur prior to epileptic spikes seen on scalp EEG
Neuroimage
Simultaneous recording of EEG and BOLD responses: a historical perspective
Int. J. Psychophysiol.
Monitoring the patient's EEG during echo planar MRI
Electroencephalogr. Clin. Neurophysiol.
Variability of the hemodynamic response as a function of age and frequency of epileptic discharge in children with epilepsy
Neuroimage
BOLD correlates of continuously fluctuating epileptic activity isolated by independent component analysis
Neuroimage
Using patient-specific hemodynamic response functions in combined EEG–fMRI studies in epilepsy
Neuroimage
Hemodynamic correlates of EEG: a heuristic
Neuroimage
Improved ballistocardiac artifact removal from the electroencephalogram recorded in fMRI
J. Neurosci. Methods
Metabolic correlates of epileptic spikes in cerebral cavernous angiomas
Epilepsy Res.
Removal of imaging artifacts in EEG during simultaneous EEG/fMRI recording: reconstruction of a high-precision artifact template
Neuroimage
Recent advances in recording electrophysiological data simultaneously with magnetic resonance imaging
Neuroimage
Where the BOLD signal goes when alpha EEG leaves
Neuroimage
EEG-correlated fMRI of human alpha activity
Neuroimage
fMRI activation during spike and wave discharges in idiopathic generalized epilepsy
Brain
fMRI activation in continuous and spike-triggered EEG–fMRI studies of epileptic spikes
Epilepsia
Benign epilepsy with centro-temporal spikes: spike triggered fMRI shows somato-sensory cortex activity
Epilepsia
Spike-triggered fMRI in reading epilepsy: involvement of left frontal cortex working memory area
Neurology
Identifying seizure-onset zone and visualizing seizure spread by fMRI: a case report
Epileptic Disord.
Dynamic time course of typical childhood absence seizures: EEG, behavior, and functional magnetic resonance imaging
J. Neurosci.
How ongoing neuronal oscillations account for evoked FMRI variability
J. Neurosci.
Über das Elektrenkephalogramm des Menschen
Arch. Psychiatr. Nervenkr.
Simultaneous EEG, fMRI, and behavior in typical childhood absence seizures
Epilepsia
Interictal functional connectivity of human epileptic networks assessed by intracerebral EEG and BOLD signal fluctuations
PLoS One
EEG/fMRI study of ictal and interictal epileptic activity: methodological issues and future perspectives in clinical practice
Epilepsia
Visual evoked potential (VEP) measured by simultaneous 64-channel EEG and 3T fMRI
Neuroreport
Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients
Brain
Cited by (89)
Ballistocardiogram artifact removal in simultaneous EEG-fMRI using generative adversarial network
2022, Journal of Neuroscience MethodsWeBrain: A web-based brainformatics platform of computational ecosystem for EEG big data analysis
2021, NeuroImageCitation Excerpt :Since the first report was published nearly 90 years ago (Berger, 1929), the scalp EEG has been an excellent technique for uncovering brain functions in a wide range of fields, including clinical neurophysiology (Li et al., 2019a; Xu et al., 2014), cognitive neuroscience studies (Enriquez-Geppert et al., 2017; Li et al., 2019b; Tian et al., 2018) and brain-computer interfaces (He et al., 2013; Zhang et al., 2019; Zhao et al., 2020), due to its high temporal resolution (∼milliseconds), low cost and noninvasive direct measurement of neuronal activity (Cohen, 2017). Furthermore, in view of the complementarity of the spatiotemporal resolution, the scalp EEG is more valuable when combined with other imaging modalities, such as MRI (Dong et al., 2014, 2015a; Friston et al., 2019; Laufs, 2012). Especially, in clinics, the EEG has been a standard test for diagnosing and characterizing brain diseases, such as epilepsy and strokes, and a basic measurement for the detection of sleep stages (Yamada and Meng, 2012).
Advances in multimodal data fusion in neuroimaging: Overview, challenges, and novel orientation
2020, Information FusionMultimodal data analysis of epileptic EEG and rs-fMRI via deep learning and edge computing
2020, Artificial Intelligence in MedicineQuantitative signal quality assessment for large-scale continuous scalp electroencephalography from a big data perspective
2023, Physiological Measurement