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Research ArticleResearch Article: Methods/New Tools, Novel Tools and Methods

Helium Optically Pumped Magnetometers Can Detect Epileptic Abnormalities as Well as SQUIDs as Shown by Intracerebral Recordings

Jean-Michel Badier, Denis Schwartz, Christian-George Bénar, Khoubeib Kanzari, Sébastien Daligault, Rudy Romain, Sergey Mitryukovskiy, William Fourcault, Vincent Josselin, Matthieu Le Prado, Julien Jung, Augustin Palacios-Laloy, Carron Romain, Fabrice Bartolomei, Etienne Labyt and Francesca Bonini
eNeuro 6 November 2023, 10 (12) ENEURO.0222-23.2023; https://doi.org/10.1523/ENEURO.0222-23.2023
Jean-Michel Badier
1Institut de Neurosciences des Systèmes, Institut National de la Santé et de la Recherche Médicale, Aix Marseille Université, Marseille 13005, France
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Denis Schwartz
2MEG Departement, CERMEP-Imagerie du Vivant, Lyon 69003, France
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Christian-George Bénar
1Institut de Neurosciences des Systèmes, Institut National de la Santé et de la Recherche Médicale, Aix Marseille Université, Marseille 13005, France
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Khoubeib Kanzari
1Institut de Neurosciences des Systèmes, Institut National de la Santé et de la Recherche Médicale, Aix Marseille Université, Marseille 13005, France
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Sébastien Daligault
2MEG Departement, CERMEP-Imagerie du Vivant, Lyon 69003, France
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Rudy Romain
3CEA-LETI, MINATEC, Université Grenoble Alpes, Grenoble 38054, France
4MAG4Health, Grenoble 38000, France
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Sergey Mitryukovskiy
3CEA-LETI, MINATEC, Université Grenoble Alpes, Grenoble 38054, France
4MAG4Health, Grenoble 38000, France
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William Fourcault
3CEA-LETI, MINATEC, Université Grenoble Alpes, Grenoble 38054, France
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Vincent Josselin
3CEA-LETI, MINATEC, Université Grenoble Alpes, Grenoble 38054, France
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Matthieu Le Prado
3CEA-LETI, MINATEC, Université Grenoble Alpes, Grenoble 38054, France
4MAG4Health, Grenoble 38000, France
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Julien Jung
5Centre de Recherche en Neurosciences de Lyon, Unité Mixte de Recherche S1028, Centre National de la Recherche Scientifique, Hospices Civils de Lyon, Institut National de la Santé et de la Recherche Médicale, Université Lyon 1, Lyon 69002, France
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Augustin Palacios-Laloy
3CEA-LETI, MINATEC, Université Grenoble Alpes, Grenoble 38054, France
4MAG4Health, Grenoble 38000, France
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Carron Romain
1Institut de Neurosciences des Systèmes, Institut National de la Santé et de la Recherche Médicale, Aix Marseille Université, Marseille 13005, France
6Department of Functional and Stereotactic Neurosurgery, Hôpital de la Timone, Assistance Publique–Hôpitaux de Marseille, Marseille 3005, France
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Fabrice Bartolomei
1Institut de Neurosciences des Systèmes, Institut National de la Santé et de la Recherche Médicale, Aix Marseille Université, Marseille 13005, France
7Department of Epileptology and Cerebral Rythmology, Hôpital de la Timone, Assistance Publique–Hôpitaux de Marseille, Marseille 3005, France
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Etienne Labyt
3CEA-LETI, MINATEC, Université Grenoble Alpes, Grenoble 38054, France
4MAG4Health, Grenoble 38000, France
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Francesca Bonini
1Institut de Neurosciences des Systèmes, Institut National de la Santé et de la Recherche Médicale, Aix Marseille Université, Marseille 13005, France
2MEG Departement, CERMEP-Imagerie du Vivant, Lyon 69003, France
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  • Figure 1.
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    Figure 1.

    SQUID-MEG, 4He-OPM-MEG, and SEEG recording setup. a, Simultaneous SQUID-MEG/SEEG. The classic cryogenic MEG system, measuring 120 × 100 cm and weighing ∼300 kg with 265 SQUID sensors in a fixed array requiring subject immobility during data acquisition. b, Simultaneous 4He-OPM-MEG/SEEG: recording configuration composed of four sensors integrated into a wearable helmet placed on the scalp and in contact with the bandage covering the SEEG electrode inserts (the cables and connectors outside the helmet are visible). Insert, A photo of the 4He-OPM sensor. c, Three-dimensional reconstruction of the patient's head from MRI, with 4He-OPM (red, named Cant, Cpost, Tant, Tpost), SQUID sensors (blue), and SEEG electrodes entry points (orange). The four SQUID sensors (named A95, A68, A179 and A157) closest to the OPMs are in green. Note the distance between the SQUIDs and the scalp (at least 3 cm), whereas the 4He-OPMs are in contact with it. d, SEEG implantation consists of 14 intracerebral electrodes, 2 in the right hemisphere (not shown) and 12 in the left hemisphere exploring the whole left temporal structures. A’, Amygdala; TB’, rhinal cortex; C’, posterior hippocampus; GPH’, parahippocampal gyrus; T’, anterior insula/lateral T1; H’, thalamus/Heschl gyrus gyrus; Ia’, anterior insula/F2; FCA’, lingual gyrus; GC’, posterior cingulate/T1; OR’, orbitofrontal cortex/middle frontal sulcus.

  • Figure 2.
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    Figure 2.

    Individual spike results. a, b, The signal collected during the SQUID-MEG/SEEG simultaneous session. Bipolar SEEG data (a). The name of the SEEG electrodes and the recording contact label are shown. The labels range from 1 (deeper location) to 11 (more superficial location). The spike (SNR = 14.9) clearly involves both deep and more superficial structures (amygdala, anterior and posterior hippocampus, third anterior temporal gyrus, and temporal pole). Simultaneous SQUID-MEG data collected on the four sensors closest to the 4He-OPM channels (b); an interictal epileptic spike appears at ∼82.5 s, with a peak-to-peak amplitude of 1.1 pT. c, d, The signal collected during the 4He-OPM-MEG/SEEG simultaneous session. Bipolar SEEG data (c). Note the similarity between two intracerebral spikes disclosing the same anatomic location and time course (SNR = 24.8). Simultaneous 4He-OPM-MEG data collected on four sensors (d). t, Tangential magnetic field (red lines); r, radial magnetic field (blue lines). A spike appears at 342.5 s with a peak-to-peak amplitude of 2,5 pT. The vertical scale is identical to that of the SQUID data in a, b.

  • Figure 3.
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    Figure 3.

    Averaged Type I spikes (n = 10). a, b, The averaged signal collected during the SQUID-MEG/SEEG simultaneous session. c, d, The averaged signal collected during the 4He-OPM-MEG/SEEG simultaneous session. The names of the SEEG electrodes and recording contacts are shown. Contacts range from 1 (deeper location) to 9 (most surface location). Bipolar averaged SEEG data for the SQUID session (a). The averaged spike involves only the bipolar TP’3–TP’4 recording. Simultaneous SQUID-MEG averaged data on the four sensors closest to the 4HeOPM sensors (b); a small interictal spike appears ∼25 ms with a peak-to-peak amplitude of 8 pT. Bipolar averaged SEEG data for the OPM session (c). Note the similarity between the intracerebral spikes of the two sessions, disclosing the same anatomic location and time course. 4He-OPM-MEG averaged data collected on four sensors, Tpos, Cant, Cpost, and Tant (d). pos, Posterior; ant, anterior. The subscript indicates the orientation. T, Tangential magnetic field (dashed lines); R, radial magnetic field (solid lines). A spike appears at 35 ms with a maximum peak-to-peak amplitude of 15 pT. The vertical scale is identical to that of the SQUID data in a, b. Extended Data Figures 1-1 and 2-1 show more details on spikes involving medial temporal structures.

  • Figure 4.
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    Figure 4.

    Averaged Type II spikes (n = 3). Arrangement of figure is similar to that of Figure 3. a, Bipolar averaged SEEG data for the SQUID session. The spikes involve a larger network encompassing TP’, TB’ and B’ electrodes (medial and lateral temporal pole, anterior hippocampus, third anterior temporal gyrus). TB’, Rhinal cortex. b, Simultaneous SQUID-MEG averaged data on the four sensors closest to the 4He-OPM sensors; a very faint spike appears at ∼75 ms with a peak-to-peak amplitude of 4 pT. c, Bipolar averaged SEEG data for the OPM session. Note the similarity between the intracerebral spikes of the two sessions, disclosing the same anatomic location and time course. d, 4He-OPM-MEG averaged data collected on four sensors, Tpos, Cant, Cpost, Tant. pos, Posterior; ant, anterior. The subscript indicates the orientation. T, Tangential magnetic field (dashed lines); R, radial magnetic field (solid lines). A spike appears at 75 s with a peak-to-peak amplitude of 9.3 pT maximum. The vertical scale is identical to that of the SQUID data in a, b. Extended Data Figures 1-1 and 2-1 show more details on spikes involving medial temporal structures.

Extended Data

  • Figures
  • Figure 1-1

    Averaged spike III results. A, B, The averaged signal (6 events) collected during the SQUID-MEG/SEEG simultaneous session. Bipolar averaged SEEG data (A). The averaged spikes involve only deep leads of the B’ electrode (left anterior hippocampus). Simultaneous SQUID-MEG averaged data on the four sensors closest to the 4He-OPM channels (B); no spike was clearly identified. C, D, The averaged signal (6 events) collected during the 4He-OPM-MEG/SEEG simultaneous session. Bipolar averaged SEEG data (C). Note the similarity between the two intracerebral spikes disclosing the same anatomical location and time course. Simultaneous 4He-OPM-MEG averaged data collected on four channels (D). t, Tangential magnetic field (dotted lines); r, radial magnetic field (continuous lines), No spike is clearly identified. The vertical scale is identical to SQUID-MEG data in A, B. Neither SQUID-MEG nor 4He-OPM-MEG detected signals linked to the events occurring on B’. Download Figure 1-1, TIF file.

  • Figure 2-1

    Averaged spike IV results. A, B, The averaged signal (10 events) collected during the SQUID-MEG/SEEG simultaneous session. Bipolar averaged SEEG data (A). The averaged spikes involve only deep leads of the GPH’ (left posterior hippocampus) electrode. Simultaneous SQUID-MEG averaged data on the four sensors closest to the 4He-OPM channels (B). No spike is clearly identified. C, D, The averaged signal (10 events) collected during the 4He-OPM-MEG/SEEG simultaneous session. Bipolar averaged SEEG data (B). Note the similarity between the two intracerebral spikes disclosing the same anatomical location and time course. Simultaneous 4He-OPM-MEG averaged data collected on four channels (D). t, Tangential magnetic field (dotted lines); r, radial magnetic field (continuous lines). No spike is clearly identified. The vertical scale is identical to the SQUID data in A, B. Neither SQUID-MEG nor 4He-OPM-MEG detected signals linked to the events occurring on GPH’. Download Figure 2-1, TIF file.

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Helium Optically Pumped Magnetometers Can Detect Epileptic Abnormalities as Well as SQUIDs as Shown by Intracerebral Recordings
Jean-Michel Badier, Denis Schwartz, Christian-George Bénar, Khoubeib Kanzari, Sébastien Daligault, Rudy Romain, Sergey Mitryukovskiy, William Fourcault, Vincent Josselin, Matthieu Le Prado, Julien Jung, Augustin Palacios-Laloy, Carron Romain, Fabrice Bartolomei, Etienne Labyt, Francesca Bonini
eNeuro 6 November 2023, 10 (12) ENEURO.0222-23.2023; DOI: 10.1523/ENEURO.0222-23.2023

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Helium Optically Pumped Magnetometers Can Detect Epileptic Abnormalities as Well as SQUIDs as Shown by Intracerebral Recordings
Jean-Michel Badier, Denis Schwartz, Christian-George Bénar, Khoubeib Kanzari, Sébastien Daligault, Rudy Romain, Sergey Mitryukovskiy, William Fourcault, Vincent Josselin, Matthieu Le Prado, Julien Jung, Augustin Palacios-Laloy, Carron Romain, Fabrice Bartolomei, Etienne Labyt, Francesca Bonini
eNeuro 6 November 2023, 10 (12) ENEURO.0222-23.2023; DOI: 10.1523/ENEURO.0222-23.2023
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Keywords

  • epilepsy
  • interictal epileptic discharges
  • magnetoencephalography
  • optically pumped magnetometers
  • simultaneous recording
  • stereotactic-EEG

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