Sleep restores an optimal computational regime in cortical networks

• Published in: Nature neuroscience Vol. 27; no. 2; pp. 328 - 338
• Main Authors: Xu, Yifan, Schneider, Aidan, Wessel, Ralf, Hengen, Keith B.
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.02.2024; Nature Publishing Group
• Subjects: 631/378/116; 631/378/1385/519; 631/378/2613/1875; Animal Genetics and Genomics; Animals; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Brain - physiology; Circuits; Computational neuroscience; Deviation; Electroencephalography - methods; Homeostasis - physiology; Neurobiology; Neurons; Neurosciences; Rats; Sleep; Sleep - physiology; Sleep and wakefulness; Visual cortex; Wakefulness - physiology
• ISSN: 1097-6256; 1546-1726; 1546-1726
• DOI: 10.1038/s41593-023-01536-9

Sleep is assumed to subserve homeostatic processes in the brain; however, the set point around which sleep tunes circuit computations is unknown. Slow-wave activity (SWA) is commonly used to reflect the homeostatic aspect of sleep; although it can indicate sleep pressure, it does not explain why animals need sleep. This study aimed to assess whether criticality may be the computational set point of sleep. By recording cortical neuron activity continuously for 10–14 d in freely behaving rats, we show that normal waking experience progressively disrupts criticality and that sleep functions to restore critical dynamics. Criticality is perturbed in a context-dependent manner, and waking experience is causal in driving these effects. The degree of deviation from criticality predicts future sleep/wake behavior more accurately than SWA, behavioral history or other neural measures. Our results demonstrate that perturbation and recovery of criticality is a network homeostatic mechanism consistent with the core, restorative function of sleep. Xu et al. show that waking progressively disrupts neural dynamics criticality in the visual cortex and that sleep restores it. Deviations from criticality predict future sleep/wake behavior better than prior behavior and slow-wave activity.