Population coding of valence in the basolateral amygdala

Xian Zhang,Bo Li

doi:10.1038/s41467-018-07679-9

Abstract

The basolateral amygdala (BLA) plays important roles in associative learning, by representing conditioned stimuli (CSs) and unconditioned stimuli (USs), and by forming associations between CSs and USs. However, how such associations are formed and updated remains unclear. Here we show that associative learning driven by reward and punishment profoundly alters BLA population responses, reducing noise correlations and transforming the representations of CSs to resemble the 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 predict the switching in valence-specific behaviors. Our results reveal how signals predictive of opposing valences in the BLA evolve during learning, and how these signals are updated during reversal learning thereby guiding flexible behaviors.

Highlights

The basolateral amygdala (BLA) plays important roles in associative learning, by representing conditioned stimuli (CSs) and unconditioned stimuli (USs), and by forming associations between CSs and USs
This study did not examine the roles of the BLA in learning driven by reward, the novel approaches employed by the study provide an opportunity to determine the relationship between BLA population activities and the establishment of valence-specific behaviors, such as, for example, how population CS responses in the BLA evolve in naïve animals during learning to represent both positive and negative valences, and how these representations are dynamically updated in “real time” in response to changes in CS-–US contingencies and influence ongoing behaviors
We found that the changes in the trajectory of BLA population CS responses were highly correlated with those of the behavioral responses, in both the punishment-to-reward and the reward-to-punishment reversal learning (Fig. 8f, g)

Summary

Introduction

The basolateral amygdala (BLA) plays important roles in associative learning, by representing conditioned stimuli (CSs) and unconditioned stimuli (USs), and by forming associations between CSs and USs. An emerging theme is that during associative learning CSs acquire the ability to activate the hard-wired US circuits, which in turn drives valence-specific behavioral responses[41] Consistent with this idea, CS-evoked spiking activity in individual BLA neurons increases with appetitive or aversive conditioning, correlates with learning and represents the valence of the US23,24,33. This study did not examine the roles of the BLA in learning driven by reward, the novel approaches employed by the study provide an opportunity to determine the relationship between BLA population activities and the establishment of valence-specific behaviors, such as, for example, how population CS responses in the BLA evolve in naïve animals during learning to represent both positive and negative valences, and how these representations are dynamically updated in “real time” in response to changes in CS-–US contingencies and influence ongoing behaviors

Methods

Results

Conclusion