Recovery of consolidation after sleep following stroke—interaction of slow waves, spindles, and GABA

• Published in: Cell reports (Cambridge) Vol. 38; no. 9; p. 110426
• Main Authors: Kim, Jaekyung, Guo, Ling, Hishinuma, April, Lemke, Stefan, Ramanathan, Dhakshin S., Won, Seok Joon, Ganguly, Karunesh
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.03.2022
• Subjects: Animals; delta waves; Electroencephalography; experimental focal stroke; GABA; gamma-Aminobutyric Acid; Memory Consolidation - physiology; motor recovery; Rats; sleep; Sleep - physiology; slow oscillations; spindles; Stroke - complications; sleep; spindles; motor recovery; GABA; delta waves; slow oscillations; experimental focal stroke
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2022.110426

Sleep is known to promote recovery after stroke. Yet it remains unclear how stroke affects neural processing during sleep. Using an experimental stroke model in rats along with electrophysiological monitoring of neural firing and sleep microarchitecture, here we show that sleep processing is altered by stroke. We find that the precise coupling of spindles to global slow oscillations (SOs), a phenomenon that is known to be important for memory consolidation, is disrupted by a pathological increase in “isolated” local delta waves. The transition from this pathological to a physiological state—with increased spindle coupling to SO—is associated with sustained performance gains during recovery. Interestingly, post-injury sleep could be pushed toward a physiological state via a pharmacological reduction of tonic γ-aminobutyric acid (GABA). Together, our results suggest that sleep processing after stroke is impaired due to an increase in delta waves and that its restoration can be important for recovery. [Display omitted] •SO-spindle coupling is impaired after stroke and recovers with motor training•Isolated local delta waves pathologically increase during sleep after stroke•Post-stroke sleep processing is impaired due to an increase in local delta waves•Reduction of inhibition transitions sleep after stroke to a more physiological state Kim et al. reveal that motor recovery after stroke is associated with both increased coupling of spindle to slow oscillations and decrease of pathologically isolated delta waves. Such changes can be modulated by reduction of tonic GABAergic inhibition. These highlight the potential importance of sleep-associated processing for enhancing motor recovery after stroke.