Basolateral amygdala dopamine transmits a nonassociative emotional salience signal

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Abstract

Adaptive decision making relies on proper discrimination and prediction of positive and negative events. The basolateral amygdala (BLA) is central to this valence encoding, assigning emotional value to stimuli to drive appropriate behavioral responses. The ventral tegmental area (VTA), which is classically known to regulate associative learning and incentive motivation via dopamine projections to the striatum, also contains strong dopamine projections to the BLA, but this system has received much less attention. Here, we investigated how in vivo BLA dopamine signaling is engaged durning learning. We show that reward cues evoke BLA dopamine signals that diminish, rather than grow, with training. As the complexity of the learning context was increased, where rats actively differentiated between various cue types signaling threat, reward, safety, and neutral associations, the magnitude of cue-evoked BLA dopamine responses was largest early in training and reported the level of perceived emotional saliency. Fear and safety cues prompted larger, sustained dopamine signals compared to reward and neutral cues, an effect that was more apparent in female rats, compared to males. Together, our findings broaden the theoretical landscape of dopamine heterogeneity, showing that BLA dopamine supports dynamic disambiguation of relative stimulus importance by non-associatively encoding sensory state transitions, independent of value. These signals reflect a scalar readout of emotional salience to prime, rather than track, learning.

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