The basolateral amygdala (BLA) plays an important role in associative learning, by representing both conditioned stimuli (CSs) and unconditioned stimuli (USs) of positive and negative valences, and by forming associations between CSs and USs. However, how such associations are formed and updated during learning remains unclear. Here we show that associative learning driven by reward and punishment profoundly alters BLA neuronal responses at population levels, reducing noise correlations and transforming the representations of CSs to resemble the distinctive valence-specific representations of USs. This transformation is accompanied by the emergence of prevalent inhibitory CS and US responses, and by the plasticity of CS responses in individual BLA neurons. During reversal learning wherein the expected valences are reversed, BLA population CS representations are remapped onto ensembles representing the opposite valences and track the switching in valence specific behavioral actions. Our results reveal how signals predictive of opposing valences in the BLA evolve during reward and punishment learning, and how these signals might be updated and used to guide flexible behaviors.
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