Resting-state intracranial high-frequency oscillations and human cognition

In 59 drug-resistant epilepsy patients undergoing stereo-electroencephalography, we evaluated relationships between rates of 80-250 Hz high-frequency oscillations (HFO-Rs) and standardized neuropsychological scores. We also quantified how local HFO-Rs modulate functional connectivity among brain regions showing significant HFO-R-cognitive score associations. We hypothesized that regional variation in cortical HFO-Rs relates to domain-specific neuropsychological performance. We analyzed HFO-Rs in 6048 gray matter channels excluding epileptogenic and lesional cortices. Resting-state HFO-Rs were comparable between left and right hemispheric homologs, except in inferior frontal and supramarginal gyri where HFO-Rs were higher in the right, and in superior frontal gyrus where they were higher on the left side, respectively. Scores on Wechsler's scales positively covaried with HFO-Rs in right medial occipital region except visual spatial, and negatively with HFO-Rs in left insula except processing speed. HFO-Rs in left inferior temporal gyrus negatively related to calculation, passage comprehension, and spelling scores of Woodcock-Johnson tests, whereas positive relationships of these scores were seen in certain right-hemispheric parcels. For Wide-Range Assessments of Memory and Learning, HFO-Rs in left parahippocampal and right medial occipital gyri covaried positively with multiple sub-scores. Hemispheric asymmetry was noted with higher proportion of positive HFO-R-cognitive score relationships in the right hemisphere (81%vs 37%, p < 0.001), and presence of self-connections and interconnections only among right-sided parcels in networks formed by HFO-correlated functional connectivity. Our findings support a broader role of HFOs in human cognition, demonstrate modulation of long-range neural connectivity by HFO-Rs, and provide a framework for research into neurophysiology of individual neuropsychological domains.