Amygdalo-cortical dialogue underlies memory enhancement by emotional association

Abstract

Emotional arousal plays a critical role in determining what is remembered from experiences. It is hypothesized that activation of the amygdala by emotional stimuli enhances memory consolidation in its downstream brain regions. However, the physiological basis of the inter-regional interaction and its functions remain unclear. Here, by adding emotional information to a perceptual recognition task that relied on a frontal-sensory cortical circuit in mice, we demonstrated that the amygdala not only associates emotional information with perceptual information but also enhances perceptual memory retention via amygdalo-frontal cortical projections. Furthermore, emotional association increased reactivation of coordinated activity across the amygdalo-cortical circuit during non-rapid eye movement (NREM) sleep but not during rapid eye movement (REM) sleep. Notably, this increased reactivation was associated with amygdala high-frequency oscillations. Silencing of amygdalo-cortical inputs during NREM sleep selectively disrupted perceptual memory enhancement. Our findings indicate that inter-regional reactivation triggered by the amygdala during NREM sleep underlies emotion-induced perceptual memory enhancement.

Keywords: amygdala; amygdala high-frequency oscillations; cortex; emotional memory; memory consolidation; memory enhancement; perceptual memory; reactivation; sleep.