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

Background: Cortico-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. Objective: To 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. Methods: SEEG 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. Results: While 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. Conclusions: The 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.