Simultaneous stereo-EEG and high-density scalp EEG recordings to study the effects of intracerebral stimulation parameters

Abstract

BackgroundCortico-cortical evoked potentials (CCEPs) recorded by stereo-electroencephalography (SEEG) are a valuable clinical tool to investigate brain reactivity and effective connectivity. However, these invasive recordings are spatially sparse since they depend on clinical needs. This sparsity hampers systematic comparisons across-subjects, the detection of the whole-brain spatiotemporal properties of CCEPs, as well as their relationships with classic sensory evoked potentials.ObjectiveTo demonstrate that CCEPs recorded by high-density electroencephalography (hd-EEG) are sensitive to changes in stimulation parameters and compensate for the limitations typical of invasive recordings.MethodsSEEG and hd-EEG activities were simultaneously recorded during SPES in drug-resistant epileptic patients (N=36). Changes in stimulation parameters encompassed physical (pulse intensity and width), geometrical (angle and position with respect to white/grey matter) and topological (stimulated cortical area) properties. Differences were assessed by measuring the overall responses and the amplitude of N1 and N2 components of the CCEPs, and by their spectral profiles.ResultsWhile invasive and non-invasive CCEPs were generally correlated, differences in pulse duration, angle and stimulated cortical area were better captured by hd-EEG. Further, hd-EEG responses to SPES reproduced basic features of responses to transcranial magnetic stimulation and showed a much larger amplitude as compared to typical sensory evoked potentials.ConclusionsThe present results show that macroscale hd-EEG recordings are exquisitely sensitive to variations in SPES parameters, including local changes in physical and geometrical stimulus properties, while providing valuable information about whole-brain dynamics. Moreover, the common reference space across subjects represented by hd-EEG may facilitate the construction of a perturbational atlas of effective connectivity.HighlightsCCEPs recorded with hd-EEG and SEEG are correlated.hd-EEG recording is highly sensitive to changes in stimulation parameters.hd-EEG responses show higher amplitude responses with respect to non-invasive ones.Simultaneous recordings provide a fixed observation point across subjects.

Local and distant cortical responses to single pulse intracranial stimulation in the human brain are differentially modulated by specific stimulation parameters

“…Further, similar results were demonstrated by a companion study conducted by Parmigiani et al, particularly with a stronger effect of white matter stimulation increasing the N2 peak intracranially as well as both the N1 and N2 peak as recorded on the scalp by high density EEG [83]. Also in keeping with the results from high density EEG data collected by Parmigiani et al [83], we found a stronger effect on responses with the bipolar electrode oriented perpendicular to the closest cortical axis. The results J o u r n a l P r e -p r o o f presented here are interesting in light of recent work involving trains of stimulation.…”

“…We never induced seizures with stimulation using single pulses. While other studies report they can induce epileptiform activity including after discharges with single pulses in other data sets [53,74], we believe we did not because of the fact that we generally used shorter (233 microsec) duration single pulse stimulation at with longer inter-pulse intervals compared to 1 ms duration [83,84].…”

“…We also found, as hypothesized, that increasing duration increased the neural responses both locally and distally, though, as we had only two duration steps, we could not determine if the relationship was linear. Related companion work found there were no differences in responses for intracranial sEEG responses for two larger duration steps (0.5 ms and 1 ms) which could indicate there is a nonlinear saturation effect with changing duration, though, interestingly, there were differences in the response on the scalp as recorded by high density EEG shown by Parmigiani et al [83]. Future work may not only need to include more duration steps, but also to identify if duration and amplitude are independent variables or merely parameters controlling total current which is what really dictates response, particularly if there are regional differences with changing waveform duration.…”

“…While there are exciting conclusions to be made relative to white matter tractography, connectivity, and stimulation [30,61,103], this data set did not have J o u r n a l P r e -p r o o f 45 consistent enough sampling of noninvasive scans mapping white matter (such as diffusion tensor imaging, or DTI). Further, both our approach and a companion study by Parmigiani et al [83] was to start from a naïve geometrically-focused perspective. We performed hypothesis testing and results focused on the geometry to generate independent conclusions from structural or functional connectivity in the brain such that future secondary analyses could allow us to compare these geometrically focused results with connectome studies [30,61].…”

Magnetoencephalography can reveal deep brain network activities linked to memory processes

“…It has been successfully employed in cognitive studies, allowing to track both evoked and oscillatory activities (Barbeau et al, 2017(Barbeau et al, , 2008Despouy et al, 2020;Hagen et al, 2020;Jonas et al, 2016;Lachaux et al, 2005;Nelson et al, 2017;Tallon-Baudry et al, 2005). Because the SEEG signal is recorded locally within the implanted structures, it can be taken as a unique ground truth to which non-invasive measures can be confronted to, although recent studies have suggested that recording EEG or MEG responses to intracranial stimulation may represent a ground truth for source localization algorithms (Mikulan et al, 2020;Parmigiani et al, 2021). Still, in order to optimize the measure of correspondence between MEG and intracranial data, their recordings should be simultaneous (Rampp et al, 2010;Shigeto et al, 2002;Sutherling et al, 2001).…”