Sleep slow oscillations favour local cortical plasticity underlying the consolidation of reinforced procedural learning in human sleep

• Published in: Journal of sleep research 2020-10, Vol.29 (5), p.e13117-n/a
• Main Authors: Menicucci, Danilo, Piarulli, Andrea, Laurino, Marco, Zaccaro, Andrea, Agrimi, Jacopo, Gemignani, Angelo
• Format: Article
• Language: English
• Subjects: Adult; Cerebral Cortex - physiopathology; electroencephalogram; Electroencephalography - methods; Female; Healthy Volunteers; Humans; implicit learning; Learning - physiology; Male; memory consolidation; Sleep - physiology; slow oscillations; slow waves; structural learning; Young Adult
• ISSN: 0962-1105; 1365-2869
• DOI: 10.1111/jsr.13117

Summary We investigated changes of slow‐wave activity and sleep slow oscillations in the night following procedural learning boosted by reinforcement learning, and how these changes correlate with behavioural output. In the Task session, participants had to reach a visual target adapting cursor's movements to compensate an angular deviation introduced experimentally, while in the Control session no deviation was applied. The task was repeated at 13:00 hours, 17:00 hours and 23:00 hours before sleep, and at 08:00 hours after sleep. The deviation angle was set at 15° (13:00 hours and 17:00 hours) and increased to 45° (reinforcement) at 23:00 hours and 08:00 hours. Both for Task and Control nights, high‐density electroencephalogram sleep recordings were carried out (23:30−19:30 hours). The Task night as compared with the Control night showed increases of: (a) slow‐wave activity (absolute power) over the whole scalp; (b) slow‐wave activity (relative power) in left centro‐parietal areas; (c) sleep slow oscillations rate in sensorimotor and premotor areas; (d) amplitude of pre‐down and up states in premotor regions, left sensorimotor and right parietal regions; (e) sigma crowning the up state in right parietal regions. After Task night, we found an improvement of task performance showing correlations with sleep slow oscillations rate in right premotor, sensorimotor and parietal regions. These findings suggest a key role of sleep slow oscillations in procedural memories consolidation. The diverse components of sleep slow oscillations selectively reflect the network activations related to the reinforced learning of a procedural visuomotor task. Indeed, areas specifically involved in the task stand out as those with a significant association between sleep slow oscillations rate and overnight improvement in task performance.