The role of sleep in emotional processing: insights and unknowns from rodent research

Abstract

Sleep is essential for the regulation of neural dynamics and animal behavior. In particular, sleep is crucial for memory consolidation and emotional regulation. In turn, emotions are key to the modulation of learning processes in which sleep also plays a crucial role. Emotional processing triggers coordinated activity between neuronal populations embedded in a network including the hippocampus, amygdala and prefrontal cortex. The optogenetic modulation of these distributed engrams' activity interferes with emotional memory. During non-REM sleep, cross-structure coordinated replay may underpin the consolidation of brain-wide emotional associative engrams. Fear conditioning induces neural synchronization between the amygdala, hippocampus, and medial prefrontal cortex during subsequent REM sleep, the perturbation of which interferes with fear memory consolidation. Future work may focus on the differential mechanisms during REM vs non-REM sleep that underpin emotional regulation and memory consolidation, as well as on distinguishing between these two tightly linked cognitive processes.

Discriminating Sleep From Freezing With Cortical Spindle Oscillations

“…In particular, immobility is also the main feature of freezing behavior (Blanchard and Blanchard, 1969 ), a widely used index of fear typically employed to probe for learning in fear conditioning (Fanselow and Poulos, 2005 ), a very popular paradigm in rodent behavioral research. This presents a problem for studies addressing the role of sleep in emotional regulation and fear memory consolidation, a research focus likely to become more and more popular since sleep neurophysiology is finally crossing paths with the investigation of emotional learning (Trouche et al, 2020 ).…”

Awake ripples enhance emotional memory encoding in the human brain

“…Similarly, the directional influence from amygdala to hippocampus during encoding was predictive of subsequent memory effect in human participants performing emotional memory task 30 . This finding suggests that the coordinated increase in post-encoding stimulus similarity across the amygdala and hippocampus during ripples is responsible for combining emotional and contextual aspects of the memory 24 , 31 .…”

“…Rodent studies have implicated ripples in the retrieval and consolidation of emotional memory. However, it is unclear whether ripples support the memory benefits of emotional experience 24 . Our study reveals an association of higher ripple rate with stimulus-induced arousal and subsequent correct stimulus discrimination, providing direct evidence for ripple-mediated strengthening of emotional memory.…”

Evidence of an active role of dreaming in emotional memory processing shows that we dream to forget

“…Specifically, emotional experiences are more likely to be tagged with stress and arousal related neurotransmitters, such as cortisol and norepinephrine, during wakefulness, signaling greater significance and prioritization for further processing and consolidation during sleep 62 , 63 . The memory component may be strengthened via spindle-mediated reactivation processes during NREM 64 , followed by further reactivation during REM sleep via amygdala activation 65 – 71 . Building on these findings, the affect tagging and consolidation (ATaC) model posits that negative experiences that heighten amygdala activity during waking are preferentially reactivated and processed during REM sleep to create a biased consolidation of negative memories 72 .…”