Recurrent Hippocampo-neocortical sleep-state divergence in humans

• Published in: Proceedings of the National Academy of Sciences - PNAS 2022-11, Vol.119 (44), p.e2123427119-e2123427119
• Main Authors: Jang, Rockelle S, Ciliberti, Davide, Mankin, Emily A, Poe, Gina R
• Format: Article
• Language: English
• Subjects: Animals; Basal forebrain; Biological Sciences; Birds; Brain stem; Cerebral cortex; Electrodes; Electroencephalography - methods; Epilepsy; Forebrain; Hippocampus; Humans; Hypothalamus; Mammals; Marine mammals; Neocortex; Phylogeny; Questions; Scalp; Sleep
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2123427119

Sleep is assumed to be a unitary, global state in humans and most other animals that is coordinated by executive centers in the brain stem, hypothalamus, and basal forebrain. However, the common observation of unihemispheric sleep in birds and marine mammals, as well as the recently discovered nonpathological regional sleep in rodents, calls into question whether the whole human brain might also typically exhibit different states between brain areas at the same time. We analyzed sleep states independently from simultaneously recorded hippocampal depth electrodes and cortical scalp electrodes in eight human subjects who were implanted with depth electrodes for pharmacologically intractable epilepsy evaluation. We found that the neocortex and hippocampus could be in nonsimultaneous states, on average, one-third of the night and that the hippocampus often led in asynchronous state transitions. Nonsimultaneous bout lengths varied from 30 s to over 30 min. These results call into question the conclusions of studies, across phylogeny, that measure only surface cortical state but seek to assess the functions and drivers of sleep states throughout the brain.