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

Abstract

Magnetoencephalography based on superconducting quantum interference devices (SQUIDs) has been shown to improve the diagnosis and surgical treatment decision for presurgical evaluation of drug-resistant epilepsy. Still, its use remains limited because of several constraints such as cost, fixed helmet size, and the obligation of immobility. A new generation of sensors, optically pumped magnetometers (OPMs), could overcome these limitations. In this study, we validate the ability of helium-based OPM (⁴He-OPM) sensors to record epileptic brain activity thanks to simultaneous recordings with intracerebral EEG [stereotactic EEG (SEEG)]. We recorded simultaneous SQUIDs-SEEG and 4He-OPM-SEEG signals in one patient during two sessions. We show that epileptic activities on intracerebral EEG can be recorded by OPMs with a better signal-to noise ratio than classical SQUIDs. The OPM sensors open new venues for the widespread application of magnetoencephalography in the management of epilepsy and other neurologic diseases and fundamental neuroscience.

Keywords: epilepsy; interictal epileptic discharges; magnetoencephalography; optically pumped magnetometers; simultaneous recording; stereotactic-EEG.

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.

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.

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, T_pos, C_ant, C_post, and T_ant (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.

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, T_pos, C_ant, C_post, T_ant. 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.