Differential unconscious control of the medial prefrontal cortex during non-REM and REM sleep to mitigate anterograde and retrograde interferences in visual perceptual learning

While it is established that visual perceptual learning (VPL) is associated with changes in visual areas, the roles of the prefrontal cortex (PFC) in regulating top-down signals for VPL remain elusive. This study specifically investigates how the PFC unconsciously controls top-down signals during sleep to reduce anterograde and retrograde interferences between VPL of the two distinct visual tasks trained before and after sleep. Before and after a 90-minute sleep session inside an MRI scanner with polysomnography, two interfering texture discrimination tasks (TDT) were trained. We tested whether training of pre-sleep and post-sleep TDTs interfered with each other. As our prior research (Nature Neuroscience, 2020) demonstrated a significant correlation between the concentration of excitatory-to-inhibitory neurotransmitters (E/I ratio) in the visual cortex during REM sleep and resilience to interference, we measured E/I ratios during non-REM and REM sleep in the medial prefrontal cortex (mPFC) and dorsolateral prefrontal cortex (DLPFC) regarding interference. Subjects who exhibited both NREM and REM sleep demonstrated greater resilience to retrograde interference (from post-sleep TDT to pre-sleep TDT) compared to those who showed NREM sleep alone. In mPFC, the E/I ratio significantly reduced from baseline during REM sleep in correlation with resilience to retrograde interference. However, resilience to anterograde interference (from pre-sleep TDT to post-sleep TDT) was correlated with the E/I ratio during NREM sleep. DLPFC exhibited no significant correlations between E/I ratios and resilience to interference anterogradely or retrogradely, while increases in the E/I ratio in DLPFC during NREM sleep from baseline were significantly correlated with offline performance gains in pre-sleep TDT. These findings indicate the involvement of the mPFC in both anterograde and retrograde interferences but during distinct sleep stages. Despite the prevailing belief that consciousness is predominantly involved in prefrontal controls, our findings suggest that prefrontal control mechanisms operate even during unconscious states such as sleep.