The human K-complex: Insights from combined scalp-intracranial EEG recordings

Sleep spindles and K-complexes (KCs) are a hallmark of N2 sleep. While the functional significance of spindles is comparatively well investigated, there is still ongoing debate about the role of the KC: it is unclear whether it is a cortical response to an arousing stimulus (either external or internal) or whether it has sleep-promoting properties. Invasive intracranial EEG recordings from individuals with drug-resistant epilepsy offer a unique opportunity to study in-situ human brain physiology. To better understand the function of the KC, we aimed to (i) investigate the intracranial correlates of spontaneous scalp KCs, and (ii) compare the intracranial activity of scalp KCs associated or not with arousals. Whole-night recordings from adults with drug-resistant focal epilepsy who underwent combined intracranial-scalp EEG for pre-surgical evaluation at the Montreal Neurological Institute between 2010 and 2018 were selected. KCs were visually marked in the scalp and categorized according to the presence of microarousals: (i) Pre-microarousal KCs; (ii) KCs during an ongoing microarousal; and (iii) KCs without microarousal. Power in different spectral bands was computed to compare physiological intracranial EEG activity at the time of scalp KCs relative to the background, as well as to compare microarousal subcategories. A total of 1198 scalp KCs selected from 40 subjects were analyzed, resulting in 32,504 intracranial KC segments across 992 channels. Forty-seven percent of KCs were without microarousal, 30% were pre-microarousal, and 23% occurred during microarousals. All scalp KCs were accompanied by widespread cortical increases in delta band power (0.3-4 ​Hz) relative to the background: the highest percentages were observed in the parietal (60-65%) and frontal cortices (52-58%). Compared to KCs without microarousal, pre-microarousal KCs were accompanied by increases (66%) in beta band power (16-30 ​Hz) in the motor cortex, which was present before the peak of the KC. In addition, spatial distribution of spectral power changes following each KC without microarousal revealed that certain brain regions were associated with increases in delta power (25-62%) or decreases in alpha/beta power (11-24%), suggesting a sleep-promoting pattern, whereas others were accompanied by increases of higher frequencies (12-27%), suggesting an arousal-related pattern. This study shows that KCs can be generated across widespread cortical areas. Interestingly, the motor cortex shows awake-like EEG activity before the onset of KCs followed by microarousals. Our findings also highlight region-specific sleep- or arousal-promoting responses following KCs, suggesting a dual role for the human KC.