Unconscious Switching of Dorsal and Medial Pathways for Plasticity and Stability During NREM and REM Sleep

While visual perceptual learning improves during non-REM sleep and stabilizes during REM sleep via excitatory-inhibitory neurotransmitter (E/I) balance in early visual areas (EVA), the role of prefrontal regions remains unclear. Here, we show that contributions of the dorsolateral prefrontal cortex (DLPFC) and medial prefrontal cortex (mPFC) differ by sleep stage in human adults. During non-REM sleep, plasticity increased in DLPFC, indexed by elevated E/I balance measured with magnetic resonance spectroscopy and polysomnography, in correlation with performance gains. During REM sleep, stability increased in mPFC, indexed by reduced E/I balance, in correlation with resilience to retrograde interference from new learning. E/I balance changes and their effects on learning paralleled those in EVA. Connectivity weights between EVA and DLPFC, and between EVA and mPFC, switched with sleep stage. These findings suggest the presence of dorsal and medial pathways that unconsciously alternate between non-REM sleep and REM sleep to improve and stabilize learning.