Understanding and reducing artefacts in simultaneously acquired EEG and fMRI data

Lead Research Organisation: University of Nottingham
Department Name: Sch of Physics & Astronomy

Abstract

In electroencephalography (EEG), brain activity is monitored by measuring weak voltages produced at the surface of the scalp by neurons. EEG measurements can be made on a millisecond timescale and so are useful for understanding the timing of brain responses, but it is not easy to work out from where in the brain the voltages arise. Functional magnetic resonance imaging (fMRI) allows the site of brain activity to be identified with high accuracy, but fMRI does not provide much information about the timing of brain responses because it is based on effects of relatively slow changes in blood flow. The complementary attributes of EEG and fMRI mean that their combination in simultaneous EEG-fMRI is potentially very useful, but combining the two techniques is technically challenging because the voltages due to brain activity are much smaller than the artefacts produced by the large time-varying magnetic fields that occur inside an MR scanner. The largest source of artefact is the rapid switching of magnetic field gradients, needed to form MR images. The resulting gradient artefact (GA) can be 10,000 times larger than the brain signals. Since the gradient waveforms are periodic, it is possible to form an average artefact template that can be subtracted from each artefact occurrence to clean up the EEG recording. However, this average artefact subtraction (AAS) fails if the subject moves during the scanning and an EEG system with a very large dynamic range is needed to record the GA. The second artefact, which is typically 10-100 times larger than brain signals, is linked to the cardiac cycle. Several possible sources of this pulse artefact (PA) have been proposed, including head rotation and scalp expansion driven by cardiac pulsation, and Hall voltages due to pulsatile flow of blood in the magnetic field. The periodic nature of the PA means that it can also be corrected using AAS, but the PA often varies significantly across heartbeats making it difficult to completely eliminate this artefact using AAS.

The presence of residual GA and PA in EEG recordings made during simultaneous fMRI limits the application of combined EEG-fMRI, particularly in studying brain activity that produces weak or high frequency signals. The aim of the work proposed here is therefore to develop equipment and techniques which will improve the quality of EEG data acquired with concurrent fMRI, thus allowing the full potential of combined EEG-fMRI to be realised. Focusing on the GA, we will identify and reduce the contributions of different components of the EEG system to the artefact and then identify the orientation and position of the subject's head in the scanner that reduces the effect of the GA to its lowest level. We will develop and test new correction methods for counteracting the effects of changes in the GA that happen when the subject moves during a scan. Computer modelling and experiments will be used to optimise the lay-out of the wires linking to the EEG electrodes so as to reduce the GA. The benefits of adding a reference layer which experiences similar artefact voltages to those produced at the scalp will also be investigated. On the PA, we will identify the relative contributions of the different sources of the artefact and then use this information to optimise the lay-out of the EEG wires and to test the benefits of using a reference layer and information from movement sensors attached to the head in reducing the PA. The findings of the work on the GA and PA will be applied to improving methods for eliminating both artefacts in post-processing and will be brought together to identify an optimal experimental set-up which will be tested in experiments carried out in conjunction with neuroscientists.

The proposed developments will provide immediate benefit to the many researchers who use combined EEG-fMRI in studying the normal brain and changes in brain function in neurological disorders, including epilepsy and schizophrenia.

Planned Impact

Looking outside the academic community, the research that we propose will potentially benefit: (i) members of society suffering from neurological disorders, such as epilepsy and schizophrenia; (ii) clinicians involved in the diagnosis and treatment of neurological disorders; (iii) manufacturers of magnetic resonance compatible electroencephalography systems; (iv) manufacturers of magnetic resonance imaging scanners.

These benefits will arise from the proposed development of better methods and hardware for making EEG recordings during concurrent fMRI which will improve the quality of EEG/fMRI data available to researchers and clinicians. Particular outcomes of the proposed work which will generate this impact include: (I) identification of the best way of positioning the subject and EEG cabling in the scanner so as to limit the magnitude of artefacts; (II) provision of EEG cap designs which reduce the magnitude of the gradient and pulse artefacts at source; (III) provision of new artefact correction methods that can cope with the effect of subject movement; (IV) availability of improved post-processing methods for analysing EEG data recorded during concurrent fMRI. Outcomes I, III & IV would be disseminated to EEG/fMRI users through journal publications and conference presentations and by making available any software developments through standard means (download from SPMMRC website as a plug-in to EEGLAB). Outcome II would be implemented via the manufacturers of MR-compatible EEG systems. Best practice recommendation by MR scanner and EEG system manufacturers would also facilitate dissemination of the other outcomes.

Availability of better quality EEG recordings made during concurrent fMRI data will increase the range of potential uses of simultaneous EEG-fMRI, thus benefiting the manufacturers of MR-compatible EEG systems, and to a lesser extent, MR scanner providers. More importantly, our proposed research should lead to increased opportunities for employing EEG-fMRI in research and clinical studies of patients with neurological disorders. This should not only provide benefits to patients through better diagnosis and treatment, but may also save costs for health organisations around the world.

Publications

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Description We are developing ways of improving the quality of electroencephalography (EEG) data that is acquired during simultaneous functional magnetic resonance imaging (fMRI). In particular we have developed a novel reference layer artefact subtraction (RLAS) approach which uses a modified EEG cap design to eliminate at source the artefacts generated in EEG recordings made simultaneously with fMRI measurements. The modified EEG cap incorporates an additional set of electrodes attached to a conducting layer. These pick up similar artefact voltages to those recorded on the electrodes attached to the scalp, but do not sense the signals from the brain. Taking the difference of the voltages recorded on the scalp and reference-layer electrodes consequently greatly attenuates the artefacts, but does not affect the signals from the brain that we are interested in measuring.

We have also developed two new post-processing methods that help to remove the artefacts that remain in EEG recordings corrected using standard methods when the subject moves their head (which is quite a common occurrence in experiments)
Exploitation Route We are currently working towards commercialising the RLAS system. This work has been supported by a small amount of funding from the University of Nottingham's EPSRC Impact Acceleration Award and from the HEIF-funded University of Nottingham Hermes Fellowship scheme.

The knowledge we gained from the funded work has also resulted in the successful use of EEG-fMRI at 7T to study brain responses at the laminar level. This was supported by a Leverhulme Grant (RPG-2014-369) focusing on study of the origin of alpha oscillations which has resulted in two publications to date. In addition, we have applied the EEG-fMRI developments made during this grant to the study of basic neurophysiology, resulting in other high impact papers.
Sectors Healthcare

 
Description Our work on establishing the optimal set-up for EEG-fMRI recordings was the subject of a JoVe video publication. This was used and promoted by Brain Products GmbH, who manufacture MRI-compatible EEG systems, to help new users of EEG-fMRI in carrying out measurements. As a result of this video and our other publications from the research carried out for this grant we have become established as one of the major academic sites which understand the technical challenges involved in the implementation of EEG-fMRI, and methods for best overcoming these challenges. Consequently, we have been approached by a number of sites for advice on the best EEG-fMRI set-up for use in their research. Examples of this include using EEG-fMRI for the study of: neonates at KCL (UK); sleep at the University of Boston (USA); the effect of drug administration at the University of Auckland (NZ); adult cognition at the Basque Center on Cognition, Brain and Language (Spain) and basic physiology University of Sherbrooke (Canada). These enquiries have resulted in visits to or from these research centres. As we continue to develop and improve the reference layer artefact subtraction (RLAS) approach, we are actively exploring the possibility of licensing or IP protection for the findings on the grant with the Technology Transfer Office at the University of Nottingham and potential commercial partners. The work carried out on this grant fed into a number of outreach events including an exhibit at the Royal Society Summer Exhibition in 2018, which showcased the possibilities for measuring neuronal activity with different neuroimaging methods. In addition, on a local level we have been involved in Mayfest and Wonder at the University of Nottingham which are public open days. At these we have explained the interactions between magnetism and electricity which are the basic physical principles which challenge EEG-fMRI to study brain function. The interest and attendance of these events was high.
First Year Of Impact 2013
Sector Healthcare,Pharmaceuticals and Medical Biotechnology
Impact Types Societal,Economic

 
Description Anne McLaren Fellowship
Amount £85,700 (GBP)
Organisation University of Nottingham 
Sector Academic/University
Country United Kingdom
Start 02/2013 
End 02/2018
 
Description Nottingham Birmingham Strategic Collaboration Fund
Amount £39,840 (GBP)
Organisation University of Nottingham 
Sector Academic/University
Country United Kingdom
Start 03/2013 
End 09/2014
 
Description University of Nottingham EPSRC Impact Acceleration Award EP/K503800/1.503800/
Amount £6,944 (GBP)
Organisation Engineering and Physical Sciences Research Council (EPSRC) 
Sector Public
Country United Kingdom
Start 08/2015 
End 10/2015
 
Description University of Nottingham Hermes Fellowship Scheme
Amount £24,030 (GBP)
Organisation University of Nottingham 
Sector Academic/University
Country United Kingdom
Start 11/2015 
End 03/2016
 
Title Jove Video on Best current practice for obtaining high quality EEG data during simultaneous FMRI. 
Description We collaborated with Brain Products GmbH to produce a JoVE video publication describing the best way of safely and efficiently acquiring EEG data during simultaneous fMRI. 
Type Of Material Physiological assessment or outcome measure 
Year Produced 2013 
Provided To Others? Yes  
Impact Brain Products and others have used this video in training new EEG-fMRI users. 
URL https://www.jove.com/video/50283/best-current-practice-for-obtaining-high-quality-eeg-data-during
 
Description UK7T Network 
Organisation King's College London
Department Institute of Pharmaceutical Science
Country United Kingdom 
Sector Academic/University 
PI Contribution The UK7T Network brought the KCL group, who recently funding from Wellcome to purchase a 7T scanner, into the UK7T Network. We are now working together in implementing the UK7T Network plans.
Collaborator Contribution We are now working together in implementing the UK7T Network plans.
Impact N/A
Start Year 2016
 
Description School visit (tonbridge) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact This was an invited talk to tell A level students about the research which goes on in Nottingham with regards to magnetic resonance imaging and how it works

This talk was well received and feedback given said that the students found it interesting to see how science can be applied.
Year(s) Of Engagement Activity 2012
 
Description Simultaneous EEG-fMRI: from acquisition to application 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Participants in your research and patient groups
Results and Impact This was an invited seminar to dissemnate the methodolgical knowledge we have gained through our research to researchers at the EPFL, Lausanne. I also presented some of the applications work to better understand brain function which we have conducted.

Collaboration with EPFL
Year(s) Of Engagement Activity 2012