Reinstatement of emotional associations during human sleep: an intracranial EEG study

Abstract The scientific literature suggests that emotional memories benefit from a privileged consolidation over neutral memories. This effect extends to consolidation processes that occur during sleep. Indeed, during sleep, a complex set of oscillations (namely slow-oscillations, theta rhythm and spindles) mediates the communication between brain regions involved in the long-term integration of memories. However, whether sleep oscillations may contribute to the reactivation and consolidation of emotional memories in humans is still unclear. Because non-invasive electroencephalography (EEG) has limited access to deep brain regions implicated in memory and emotion (e.g., hippocampus, amygdala, orbitofrontal cortex), here we recorded EEG signal from these brain regions using intracranial electrodes placed in medically-resistant epileptic patients in the context of presurgical investigation. During wakefulness, we presented the patients with emotional (i.e., humorous) vs emotionally neutral pictures paired with a sound. Then, we tested for the reinstatement of emotional-associations by delivering the sound during a subsequent period of sleep. We found that the reactivation of emotional (compared to neutral) memories during sleep enhanced slow-oscillation and spindle activity in the orbitofrontal cortex, paralleled with an increase in theta connectivity between the hippocampus and the orbitofrontal cortex. In addition, we observed that the theta response to emotional memories reactivated at subsequent wake was different than for neutral memories, suggesting a change in memory traces with targeted memory reactivation. These data suggest that consolidation of emotional events during sleep is due to a larger expression of sleep features (in the slow-oscillation, theta and sigma frequency bands) and that the mechanisms of brain plasticity also take place in emotional brain regions during NREM sleep.