Immediate post learning sleep improves motor memory retention and promotes the fast spindle-SO coupling over the contralateral motor network

AGUSTIN SOLANO; LUIS A RIQUELME; DANIEL PEREZ CHADA; VALERIA DELLA MAGGIORE

San Diego, California

Congreso; NEUROSCIENCE 2022 - SFN ANNUAL MEETING; 2022

Society for Neuroscience

The last decade has seen remarkable progress in the identification of neural markers of sleep-dependent memory consolidation. Yet, most advances have emerged from the field of declarative memory. Recently, however, we have shown that the level of coupling between fast spindles and slow oscillations (SO), a mechanism involved in the consolidation of declarative memories (Muehlroth et al., 2019), is modulated by visuomotor adaptation (VMA), a type of procedural learning. Specifically, VMA increases the spindle-SO coupling, over the contralateral hemisphere to the trained hand, and this increment predicts overnight memory retention (Solano et al., 2021, 2022). Here, we deepen on the mechanisms involved in sleep-dependent consolidation of motor memories by manipulating the time interval elapsed between training and sleep, a procedure that has been effective in unveiling the benefit of sleep in declarative tasks (Backhaus et al., 2008; Talamini et al., 2008; Payne et al., 2012; Sawangjit et al., 2018). Two groups of subjects were trained ~14 hours (T-14h; n=23) or ~10 minutes before sleep (T-10min; n=23), and EEG was recorded overnight. Memory retention was assessed 24 h and 2 weeks after learning. We predicted that if sleep modulates the consolidation of VMA memories, sleep immediately after training should improve overnight memory retention and increase spindle-SO coupling locally. We found that the temporal proximity between training and sleep enhanced memory retention by 30% (main effect of group, p=0.049), a phenomenon that persisted for at least two weeks. In line with the observed gains in performance, the density of fast spindles increased during NREM sleep over the hemisphere contralateral to the trained hand (p=0.002). Critically, the coupling between fast spindles and SO significantly increased in the T-10min group compared to the T-14h group (p=0.019). These results are in line with the Systems Consolidation Hypothesis. The proximity between learning and sleep did not influence the delta band activity early during NREM sleep, suggesting that the Synaptic Homeostasis Hypothesis (SHY) may not explain behavioral gains induced by this manipulation. Our results provide evidence in favor of a common mechanism in the stabilization of declarative and motor memories.Refs: Muehlroth et al.(2019) Sci Rep. 9(1):1940; Solano et al., (2021) Cer.Cortex; Solano et al., (2022) Front.Neurosci. vol. 16; Backhaus et al. (2008) Neurobiol. Learn. Mem. 89(1); Talamini et al.(2008). Learn. and Mem., 15(4); Payne et al. (2012)PLoS ONE, 7(3); Sawangjit et al. (2018) Nature. 564(7734)