Transcranial slow oscillation stimulation during NREM sleep enhances acquisition of the radial maze task and modulates cortical network activity in rats

Slow wave sleep, hallmarked by the occurrence of slow oscillations (SO), plays an important role for the consolidation of hippocampus-dependent memories. Transcranial stimulation by weak electric currents oscillating at the endogenous SO frequency (SO-tDCS) during post-learning sleep was previously shown by us to boost SO activity and improve the consolidation of hippocampus-dependent memory in human subjects. Here, we aimed at replicating and extending these results to a rodent model. Rats were trained for 12 days at the beginning of their inactive phase in the reference memory version of the radial arm maze. In a between subjects design, animals received SO-tDCS over prefrontal cortex (PFC) or sham stimulation within a time frame of 1 h during subsequent non-rapid eye movement (NREM) sleep. Applied over multiple daily sessions SO-tDCS impacted cortical network activity as measured by EEG and behavior: at the EEG level, SO-tDCS enhanced post-stimulation upper delta (2–4 Hz) activity whereby the first stimulations of each day were preferentially affected. Furthermore, commencing on day 8, SO-tDCS acutely decreased theta activity indicating long-term effects on cortical networks. Behaviorally, working memory for baited maze arms was enhanced up to day 4, indicating enhanced consolidation of task-inherent rules, while reference memory errors did not differ between groups. Taken together, we could show here for the first time an effect of SO-tDCS during NREM sleep on cognitive functions and on cortical activity in a rodent model.