Synaptic strength dynamics at cortical pathways is encoded by vigilance states duration

Abstract

Interactions among brain areas are essential to most cognitive functions. Neuronal interactions between these areas depend on the modulation of synaptic strength. However, this modulation remains poorly understood. We recorded evoked synaptic responses at four hippocampal pathways in freely moving male rats across 24 hours: the Perforant Path to Dentate Gyrus (PP-DG), Fornix to Prefrontal Cortex (Fx-PFC), Fornix to Nucleus Accumbens (Fx-NAc), and the Schaffer Collaterals to CA1 (SC-CA1). We preserved the temporal dynamics of vigilance states and synaptic responses and show for the first time that synaptic strength at these four hippocampal pathways oscillates, with a very slow periodicity. We demonstrate that synaptic strength at the PP-DG, Fx-PFC, Fx-NAc pathways show a positive correlation with the duration of active wakefulness (aWK) and a negative one with the duration of most sleep states (slow wave sleep (SWS) and rapid eye movement sleep (REM)), with a positive peak correlation time-lag of 1 to 10 minutes for aWK and SWS at these 3 pathways. In contrast, no significant correlation peak is found at the SC-CA1 pathway. Finally, a model based on hypnogram data and synaptic strength at the PP-DG pathway was able to predict the evolution of synaptic strength at the PP-DG, Fx-PFC and Fx-NAc pathways, but not at the SC-CA1 pathway. These results reveal that the temporal succession of vigilance states, particularly aWK and SWS, may contribute to memory processes through rapid modulation of synaptic strength at several pathways during the sleep-wakefulness cycle, suggesting that memory processes are not only dependent on sleep amount but also on sleep architecture.