Procedural learning and sleep hippocampal low frequencies in humans

Abstract

Recent evidence suggests that slow EEG rhythms are involved in post-learning plasticity. However, the relationships between memory consolidation and hippocampal EEG features remain unclear. Here, we assessed the effects of both procedural and declarative learning on qualitative and quantitative measures of sleep by recording stereo-EEG (SEEG) directly from the hippocampus and the neocortex in a group of epileptic patients undergoing pre-surgical evaluations. Following a baseline night, sleep was recorded after administration of a declarative (paired-associate word list learning task) and a procedural (sequential finger tapping) task. Patients were tested before going to bed (test) and after sleep in the following morning (retest). At retest, we found that patients recalled correctly more word pairs compared to the pre-sleep test (declarative task), and they were slightly faster in performing the motor task (procedural task). Standard polysomnography showed an increase in the amount of slow-wave sleep (SWS) only after procedural learning, paralleled by an increase of hippocampal SEEG power in the very low frequency range (VLF, 0.5-1 Hz) during the first NREM sleep cycle. Moreover, procedural performance enhancement and SEEG power increase in the hippocampal VLF were significantly correlated, indicating a link between procedural memory consolidation and slow hippocampal SEEG rhythms. These findings are consistent with the hypothesis of synaptic homeostasis occurring during sleep, suggesting that hippocampal slow oscillations are associated with local processes of post-learning synaptic downscaling.