Different Learning Stabilization Processes between Wakefulness and Sleep

Abstract

Visual perceptual learning (VPL) is initially fragile and must be stabilized after training to enable long-term retention. While sleep-dependent stabilization has been linked to changes in excitation/inhibition (E/I) balance, the neural mechanisms supporting stabilization during wakefulness remain unclear. Here, we investigated whether electrophysiological indices associated with sleep-based stabilization also characterize stabilization during posttraining wakefulness. Humans of both sexes completed visual training tasks with two competing training blocks separated by an awake rest period during which electroencephalography (EEG) was recorded. We conducted two studies targeting different stabilization states: one in which learning was vulnerable to retrograde interference and a control condition in which learning was largely stabilized through extended training and rest. Across studies, we estimated theta-band power and a criticality-based EEG index of E/I balance from posterior cortical sites. When stabilization was incomplete, elevated E/I balance during wakeful rest was associated with greater subsequent interference, whereas reduced E/I balance predicted stronger stabilization, paralleling findings previously reported during REM sleep. In contrast, when learning was fully stabilized, elevated E/I balance was associated with continued performance improvement rather than interference. Theta power showed a distinct, state-dependent pattern, predicting interference during wakefulness but not after stabilization. These findings indicate that wakeful stabilization of VPL shares a common inhibitory-dominant mechanism with REM sleep, while theta power is related to stabilization in different directions depending on whether the brain is wake or in REM sleep. Together, the results suggest that stabilization during wakefulness and REM sleep share partially common but not completely the same processing.