Sleep-dependent upscaled excitability, saturated neuroplasticity, and modulated cognition in the human brain

• Published in: eLife Vol. 11
• Main Authors: Salehinejad, Mohammad Ali, Ghanavati, Elham, Reinders, Jörg, Hengstler, Jan G, Kuo, Min-Fang, Nitsche, Michael A
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 06-06-2022; eLife Sciences Publications Ltd; eLife Sciences Publications, Ltd
• Subjects: Animal cognition; Behavior; Behavioral plasticity; Brain; Cognition; Cognitive ability; cortical excitability; EEG; Evoked Potentials, Motor - physiology; Excitability; GABA; Glutamate; Homeostasis; Humans; Learning; learning and memory; Long-term depression; Long-term potentiation; Magnetic fields; Memory; Motor Cortex - physiology; Neural plasticity; Neuronal Plasticity - physiology; Neurophysiology; neuroplasticity; Neuroscience; non-invasive brain stimulation; Physiological aspects; Physiology; Short term memory; Sleep; Sleep Deprivation; sleep homeostasis; Synaptic strength; Theta rhythms; Transcranial Direct Current Stimulation - methods; Transcranial Magnetic Stimulation; γ-Aminobutyric acid; Germany; sleep deprivation; learning and memory; neuroscience; sleep homeostasis; transcranial magnetic stimulation; human; non-invasive brain stimulation; transcranial direct current stimulation; cortical excitability; neuroplasticity
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.69308

Sleep strongly affects synaptic strength, making it critical for cognition, especially learning and memory formation. Whether and
sleep deprivation modulates human brain physiology and cognition is not well understood. Here we examined how overnight sleep deprivation vs overnight sufficient sleep affects (a) cortical excitability, measured by transcranial magnetic stimulation, (b) inducibility of long-term potentiation (LTP)- and long-term depression (LTD)-like plasticity via transcranial direct current stimulation (tDCS), and (c) learning, memory, and attention. The results suggest that sleep deprivation upscales cortical excitability due to enhanced glutamate-related cortical facilitation and decreases and/or reverses GABAergic cortical inhibition. Furthermore, tDCS-induced LTP-like plasticity (anodal) abolishes while the inhibitory LTD-like plasticity (cathodal) converts to excitatory LTP-like plasticity under sleep deprivation. This is associated with increased EEG theta oscillations due to sleep pressure. Finally, we show that learning and memory formation, behavioral counterparts of plasticity, and working memory and attention, which rely on cortical excitability, are impaired during sleep deprivation. Our data indicate that upscaled brain excitability and altered plasticity, due to sleep deprivation, are associated with impaired cognitive performance. Besides showing how brain physiology and cognition undergo changes (from neurophysiology to higher-order cognition) under sleep pressure, the findings have implications for
and optimal
of noninvasive brain stimulation.