Unleashing the Potential of4He OPM-MEG: A Comparison with SQUID-MEG for Detecting Interictal Epileptic Activity

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Abstract

Summary Objectives Conventional magnetoencephalography (MEG) based on superconducting quantum interference devices sensors (SQUIDs), are the only widely used MEG systems in both clinical and research settings. However, they have limitations that hinder their widespread deployment. Optically pumped magnetometers (OPMs) offer several advantages over SQUIDs, particularly for epilepsy studies: lightweight and flexible, OPMs can be integrated into adaptable motion-tolerant headsets, enabling recordings during seizures or natural head movements, and potentially enhancing the detection of interictal epileptiform discharges (IEDs). In the present study, we assess the capabilities of a 5-sensors MEG system with helium OPMs ( 4 He-OPMs) in detecting IEDs. Methods First, we compare the performance of SQUID-MEG and 4 He-OPM-MEG in a routine clinical setup with a group of 7 patients. Second, we perform combined intra-cerebral (SEEG) 4 He-OPM-MEG and SQUID-MEG recordings in a single patient to demonstrate the ability of both systems to detect IEDs originating from deep brain structures. Results The key finding is that, even with a very limited number of sensors, the 4 He-OPM-MEG prototype successfully captured interictal epileptic activity in most patients. This activity was clearly detectable and exhibited the characteristic morphology with strikingly similar time courses between 4 He-OPM-MEG and SQUID-MEG signals. Using combined SEEG and OPM-MEG recordings, we obtained the first direct validation of the ability of 4 He OPM sensors to record epileptic activities originating from deep structures. Significance These results strongly support the clinical adoption of a lightweight, high-sensitivity, whole-head 4 He OPMs-MEG system, offering new perspectives for epilepsy diagnostics and beyond, and enabling the democratization and spread of MEG in clinical and research settings. Plain language summary Magnetoencephalography is a non-invasive neuroimaging technique that has been shown to improve surgical outcomes in epileptic patients. However, its use remains limited due to several constraints, which could be overcome by a new generation of sensors: the optically pumped magnetometers (OPMs). Here, we validate the ability of OPM sensors to record epileptic brain activity in a regular clinical setup and thanks to simultaneous intracerebral recordings. These sensors open new venues for the widespread application of magnetoencephalography in the management of epilepsy and other neurological diseases, as well as for fundamental neuroscience. Key points Epileptic abnormalities are detected by 4 He OPMs as well as with classical magnetoencephalography. Hippocampal interictal activity can be detected by 4 He OPMs as shown by simultaeous SEEG-OPM recordings. This results represents significant step towards the validation of OPM-MEG for epilepsy diagnosis and neuroscience research.
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Objectives

Conventional magnetoencephalography (MEG) based on superconducting quantum interference devices sensors (SQUIDs), are the only widely used MEG systems in both clinical and research settings. However, they have limitations that hinder their widespread deployment. Optically pumped magnetometers (OPMs) offer several advantages over SQUIDs, particularly for epilepsy studies: lightweight and flexible, OPMs can be integrated into adaptable motion-tolerant headsets, enabling recordings during seizures or natural head movements, and potentially enhancing the detection of interictal epileptiform discharges (IEDs). In the present study, we assess the capabilities of a 5-sensors MEG system with helium OPMs (4He-OPMs) in detecting IEDs.

Methods

First, we compare the performance of SQUID-MEG and 4He-OPM-MEG in a routine clinical setup with a group of 7 patients. Second, we perform combined intra-cerebral (SEEG) 4He-OPM-MEG and SQUID-MEG recordings in a single patient to demonstrate the ability of both systems to detect IEDs originating from deep brain structures.

Results

The key finding is that, even with a very limited number of sensors, the 4He-OPM-MEG prototype successfully captured interictal epileptic activity in most patients. This activity was clearly detectable and exhibited the characteristic morphology with strikingly similar time courses between 4He-OPM-MEG and SQUID-MEG signals. Using combined SEEG and OPM-MEG recordings, we obtained the first direct validation of the ability of 4He OPM sensors to record epileptic activities originating from deep structures. Significance These results strongly support the clinical adoption of a lightweight, high-sensitivity, whole-head 4He OPMs-MEG system, offering new perspectives for epilepsy diagnostics and beyond, and enabling the democratization and spread of MEG in clinical and research settings. Plain language summary Magnetoencephalography is a non-invasive neuroimaging technique that has been shown to improve surgical outcomes in epileptic patients. However, its use remains limited due to several constraints, which could be overcome by a new generation of sensors: the optically pumped magnetometers (OPMs). Here, we validate the ability of OPM sensors to record epileptic brain activity in a regular clinical setup and thanks to simultaneous intracerebral recordings. These sensors open new venues for the widespread application of magnetoencephalography in the management of epilepsy and other neurological diseases, as well as for fundamental neuroscience. Key points Epileptic abnormalities are detected by 4He OPMs as well as with classical magnetoencephalography. Hippocampal interictal activity can be detected by 4He OPMs as shown by simultaeous SEEG-OPM recordings. This results represents significant step towards the validation of OPM-MEG for epilepsy diagnosis and neuroscience research. Competing Interest Statement The authors declare the following competing interests: E.L. hold founding equity in Mag4Health SAS, a French start-up company that is developing and commercializing MEG systems based on He-OPM technology. Mag4Health SAS provided technical support to the data acquisition. For the recordings performed until 1 February 2022, S. was still employee of CEA LETI. The remaining authors have no conflicts of interest. Clinical Trial NCT04615637 Funding Statement This study was supported by Agence Nationale de la Recherche Grants ANR-22-CE19-0012-01, Grant ANR-11-INBS-0006 to France Life Imaging network, and ANR-16-CONV-0002 to Institute of Language, Communication,and the Brain, and grant from Region Auvergne-Rhone-Alpes (Pack Ambition project: NEW_MEG). TG is supported by the Labex Cortex (ANR-11-LABX-0042). Author Declarations I confirm all relevant ethical guidelines have been followed, and any necessary IRB and/or ethics committee approvals have been obtained. Yes The details of the IRB/oversight body that provided approval or exemption for the research described are given below: The study was approved by the regulatory and ethics national administration in France under number 2020-A01830-39 and 2020-A00634-35 by l'Agence National de Securite du Medicament et des Produis de Sante (https://ansm.sante.fr) and le Comite de Protection des Personnes SUD EST IV. Informed Consent Statement: Informed written consent was obtained from all subjects involved in the study. I confirm that all necessary patient/participant consent has been obtained and the appropriate institutional forms have been archived, and that any patient/participant/sample identifiers included were not known to anyone (e.g., hospital staff, patients or participants themselves) outside the research group so cannot be used to identify individuals. Yes I understand that all clinical trials and any other prospective interventional studies must be registered with an ICMJE-approved registry, such as ClinicalTrials.gov. I confirm that any such study reported in the manuscript has been registered and the trial registration ID is provided (note: if posting a prospective study registered retrospectively, please provide a statement in the trial ID field explaining why the study was not registered in advance). Yes I have followed all appropriate research reporting guidelines, such as any relevant EQUATOR Network research reporting checklist(s) and other pertinent material, if applicable. Yes Data Availability Statement Anonymized data supporting the results of this study are available from the corresponding author upon reasonable request and validation by regulatory and ethical bodies and subject consent.

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