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Interictal epileptic spikes (IES) represent a signature of the transient synchronous and excessive discharge of a large ensemble of cortical heterogeneous neurons. Epilepsy cannot be reduced to a hypersynchronous activation of neurons whose functioning is impaired, resulting on electroencephalogram (EEG) in epileptic seizures or IES. The complex pathophysiological mechanisms require a global approach to the interactions between neural synaptic and nonsynaptic, vascular, and metabolic systems. In the present study, we focused on the interaction between synaptic and nonsynaptic mechanisms through the simultaneous noninvasive multimodal multiscale recording of high-density EEG (HD-EEG; synaptic) and fast optical signal (FOS; nonsynaptic), which evaluate rapid changes in light scattering related to changes in membrane configuration occurring during neuronal activation of IES.

To evaluate changes in light scattering occurring around IES, three children with frontal IES were simultaneously recorded with HD-EEG and FOS. To evaluate change in synchronization, time–frequency representation analysis of the HD-EEG was performed simultaneously around the IES. To independently evaluate our multimodal method, a control experiment with somatosensory stimuli was designed and applied to five healthy volunteers.

Alternating increase–decrease–increase in optical signals occurred 200 ms before to 180 ms after the IES peak. These changes started before any changes in EEG signal. In addition, time–frequency domain EEG analysis revealed alternating decrease–increase–decrease in the EEG spectral power concomitantly with changes in the optical signal during IES. These results suggest a relationship between (de)synchronization and neuronal volume changes in frontal lobe epilepsy during IES.

These changes in the neuronal environment around IES in frontal lobe epilepsy observed in children, as they have been in rats, raise new questions about the synaptic/nonsynaptic mechanisms that propel the neurons to hypersynchronization, as occurs during IES. We further demonstrate that this noninvasive multiscale multimodal approach is suitable for studying the pathophysiology of the IES in patients.