The dominance of global phase dynamics in human cortex, from delta to gamma

Abstract

The organization of the phase of electrical activity in the cortex is critical to inter-site communication, but the balance of this communication across large-scale (>8cm), macroscopic (>1cm) and mesoscopic (1cm to 1mm) ranges is an open question. Traveling waves in the cortex are spatial phase gradients, such that phase values change smoothly through the cortical sheet over time. Large-scale cortical traveling waves have been understudied compared to micro- or mesoscopic waves. The spatial frequencies (i.e., the spatial scales) of cortical waves have been characterized in the grey-matter for micro- and mesoscopic scales of cortex and show decreasing spatial power with increasing spatial frequency. This research, however, has been limited by the size of the measurement array, thus excluding large-scale traveling waves. Obversely, poor spatial resolution of extra-cranial measurements prevents incontrovertible large-scale estimates of spatial power via electroencephalogram and magnetoencephalogram. These limitations mean that the relative importance of large-scale traveling waves is unknown, and recent research has suggested waves measured extra-cranially are artefactual. We apply a novel method to estimate the spatial frequency spectrum of phase dynamics in order to quantify the uncertain large-scale range. Stereotactic electroencephalogram (sEEG) is utilized to leverage measurements of local-field potentials within the grey matter, while also taking advantage of the sometimes large extent of spatial coverage. Irregular sampling of the cortical sheet is offset by use of linear algebra techniques to empirically estimate the spatial frequency spectrum. We find the spatial power of the phase is highest at the lowest spatial frequencies (longest wavelengths), consistent with the power spectra ranges for micro- and meso-scale dynamics, but here shown up to the size of the measurement array (up to 8-16cm), i.e., approaching the entire extent of cortex. Low spatial frequencies dominate the cortical phase dynamics. This has important functional implications as it means that the phase measured for a single contact in the grey matter is more strongly a function of large-scale phase organization than local--within the same frequency band at least. This result arises across a wide range of temporal frequencies, from the delta band (1-3Hz) through to the high gamma range (60-100Hz).