Macroscale traveling waves evoked by single-pulse stimulation of the human brain.

Abstract

Understanding the spatiotemporal dynamics of neural signal propagation is fundamental to unraveling the complexities of brain function. Emerging evidence suggests that cortico-cortical evoked potentials (CCEPs) resulting from single-pulse electrical stimulation may be used to characterize the patterns of information flow between and within brain networks. At present, the basic spatiotemporal dynamics of CCEP propagation cortically and subcortically are incompletely understood. We hypothesized that single-pulse electrical stimulation evokes neural traveling waves detectable in the three-dimensional space sampled by intracranial stereoelectroencephalography. Across a cohort of 21 adult males and females with intractable epilepsy, we delivered 17,631 stimulation pulses and recorded CCEP responses in 1,019 electrode contacts. The distance between each pair of electrode contacts was approximated using three different metrics (Euclidean distance, path length, and geodesic distance), representing direct, tractographic, and transcortical propagation, respectively. For each robust CCEP, we extracted amplitude-, spectral-, and phase-based features to identify traveling waves emanating from the site of stimulation. Many evoked responses to stimulation appear to propagate as traveling waves (∼14-28%, ∼5-19% with false-discovery rate correction), despite sparse sampling throughout the brain. These stimulation-evoked traveling waves exhibited biologically plausible propagation velocities (range 0.1-9.6 m/s). Our results reveal that direct electrical stimulation elicits neural activity with variable spatiotemporal dynamics that can be modeled as a traveling wave.Significance Statement Using single-pulse stimulation, we identify a subset of intracranial evoked potentials that propagate as neural traveling waves. Our results were robust across a range of distinct but complementary analysis methods. The identification of stimulation-evoked traveling waves may help to better characterize the pathways traversed by spontaneous, pathological, or task-evoked traveling waves and distinguish biologically plausible propagation from volume-conducted signals.