Sleep is an active state critical for processing emotional memories encoded during waking in both humans and animals. There is a remarkable overlap between the brain structures and circuits active during sleep, particularly rapid eye-movement (REM) sleep, and the those encoding emotions. Accordingly, disruptions in sleep quality or quantity, including REM sleep, are often associated with, and precede the onset of, nearly all affective psychiatric and mood disorders. In this context, a major biomedical challenge is to better understand the underlying mechanisms of the relationship between (REM) sleep and emotion encoding to improve treatments for mental health. This lecture will summarize our investigation of the cellular and circuit mechanisms underlying sleep architecture, sleep oscillations, and local brain dynamics across sleep-wake states using electrophysiological recordings combined with single-cell calcium imaging or optogenetics. The presentation will detail the discovery of a 'somato-dendritic decoupling'in prefrontal cortex pyramidal neurons underlying REM sleep-dependent stabilization of optimal emotional memory traces. This decoupling reflects a tonic inhibition at the somas of pyramidal cells, occurring simultaneously with a selective disinhibition of their dendritic arbors selectively during REM sleep. Recent findings on REM sleep-dependent subcortical inputs and neuromodulation of this decoupling will be discussed in the context of synaptic plasticity and the optimization of emotional responses in the maintenance of mental health.

Sleep is crucial for the continuity and development of life. Sleep-related problems can alter brain function, and cause potentially severe psychological and behavioral consequences. However, the role of sleep in our mind and behavior is far from clear. In this talk, I will present our research on how sleep may play a role in visual perceptual learning (VPL) by using simultaneous magnetic resonance spectroscopy and polysomnography in human subjects. We measured the concentrations of neurotransmitters in the early visual areas during sleep and obtained the excitation/inhibition (E/I) ratio which represents the amount of plasticity in the visual system. We found that the E/I ratio significantly increased during NREM sleep while it decreased during REM sleep. The E/I ratio during NREM sleep was correlated with offline performance gains by sleep, while the E/I ratio during REM sleep was correlated with the amount of learning stabilization. These suggest that NREM sleep increases plasticity, while REM sleep decreases it to solidify once enhanced learning. NREM and REM sleep may play complementary roles, reflected by significantly different neurochemical processing, in VPL.

The brain is a prediction machine. Yet the world is never entirely predictable, for any animal. Unexpected events are surprising and this typically evokes prediction error signatures in animal brains. In humans such mismatched expectations are often associated with an emotional response as well. Appropriate emotional responses are understood to be important for memory consolidation, suggesting that valence cues more generally constitute an ancient mechanism designed to potently refine and generalize internal models of the world and thereby minimize prediction errors. On the other hand, abolishing error detection and surprise entirely is probably also maladaptive, as this might undermine the very mechanism that brains use to become better prediction machines. This paradoxical view of brain functions as an ongoing tug-of-war between prediction and surprise suggests a compelling new way to study and understand the evolution of consciousness in animals. I will present approaches to studying attention and prediction in the tiny brain of the fruit fly, Drosophila melanogaster. I will discuss how an ‘active’ sleep stage (termed rapid eye movement – REM – sleep in mammals) may have evolved in the first animal brains as a mechanism for optimizing prediction in motile creatures confronted with constantly changing environments. A role for REM sleep in emotional regulation could thus be better understood as an ancient sleep function that evolved alongside selective attention to maintain an adaptive balance between prediction and surprise. This view of active sleep has some interesting implications for the evolution of subjective awareness and consciousness.

The hippocampus and the amygdala are two structures required for emotional memory. While the hippocampus encodes the contextual part of the memory, the amygdala processes its emotional valence. During Non-REM sleep, the hippocampus displays high frequency oscillations called “ripples”. Our early work shows that the suppression of ripples during sleep impairs performance on a spatial task, underlying their crucial role in memory consolidation. We more recently showed that the joint amygdala-hippocampus activity linked to aversive learning is reinstated during the following Non-REM sleep epochs, specifically during ripples. This mechanism potentially sustains the consolidation of aversive associative memories during Non REM sleep. On the other hand, REM sleep is associated with regular 8 Hz theta oscillations, and is believed to play a role in emotional processing. A crucial, initial step in understanding this role is to unravel sleep dynamics related to REM sleep in the hippocampus-amygdala network

Creative thought relies on the reorganisation of existing knowledge. Sleep is known to be important for creative thinking, but there is a debate about which sleep stage is most relevant, and why. I will address this issue by proposing that Rapid Eye Movement sleep, or 'REM', and Non-REM sleep facilitate creativity in different ways. Memory replay mechanisms in Non-REM can abstract rules from corpuses of learned information, while replay in REM may promote novel associations. I propose that the iterative interleaving of REM and Non-REM across a night boosts the formation of complex knowledge frameworks, and allows these frameworks to be restructured - thus facilitating creative thought. My talk will discuss experiments exploring these hypotheses, and the mechanisms for these processes.