How does the human brain sleep: analysis of scalp-intracerebral correlates to better understand the region-specific neurophysiology of sleep

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Sleep is typically considered a global brain phenomenon. Regional variations in oscillatory activity during sleep remain unknown. Intracranial electroencephalography (iEEG), as used in few tertiary centers during presurgical epilepsy evaluation, offers the unique and only possibility to study in situ the human cortex with high spatio-temporal resolution. This program exploits this method to generate knowledge on the regional variability of sleep neurophysiology in the human brain and to investigate the contribution of deep brain structures to the non-invasive signal of sleep activity. Objective #1: atlas of normative region-specific iEEG activity during sleep. We have pioneered the first human atlas of the normal iEEG during wakefulness by selecting in each patient the few contacts located in healthy brain and accumulating a large number of patients to cover the whole cortex (Frauscher et al., Brain 2018). In a subset, we had access to segments with sleep. First data show that the iEEG has a caudo-rostral frequency gradient across all sleep stages. Moreover, deep-seated structures show spectral peaks differing from the scalp EEG. This approach will be used in a more ambitious project, building an atlas during the different stages and cycles of sleep, in all brain regions. Objective #2: analysis of the intracerebral correlates of sleep microstructure and dynamics. Whereas there is extensive knowledge on sleep spindles and their intracerebral correlates (e.g. Frauscher et al., NeuroImage 2015), knowledge on other sleep-specific transients or changes in sleep dynamics are scarce or non-existing. This is because combined sleep recording is rarely performed in the set-up of iEEG. The large datapool of objective 1 will enable to elucidate regional sleep microstructural and dynamic changes. Objective #3: contribution of deep brain structures to the non-invasive neurophysiological signal of sleep activity. Non-invasive source localization methods suffer from our inability to know in what conditions a source model is correct and can be trusted. We propose a unique approach, which will enable us to validate directly, using non-invasive mapping procedures such as high-density EEG and magnetoencephalography, the detectability of deep sources as recorded with iEEG as ground truth. This will determine which sleep patterns can be studied non-invasively. This program will (i) generate knowledge on the distinct participation of various cortical regions and networks in the local regulation of sleep, (ii) demonstrate which brain regions are specifically involved at the time of sleep oscillations or changes in sleep dynamics, and (iii) establish which type of sleep activity in deep structures is detectable using non-invasive brain mapping techniques. It will increase our knowledge on neurophysiological correlates of sleep and open new avenues for better interpreting the correlates of non-invasive measures of brain activity. The dataset will be open-access.