Rate and noise in human amygdala drive increased exploration in aversive learning

Abstract

To cope in uncertain environments, animals must balance their actions between using current resources and searching for new ones¹. This exploration-exploitation dilemma has been studied extensively in paradigms involving positive outcomes, and neural correlates have been identified in frontal cortices and subcortical structures^2-11, including the amygdala¹². Importantly, exploration is just as essential for survival or well-being when trying to avoid negative outcomes, yet we do not know whether the single-neuron mechanisms that drive exploration are shared across positive and negative environments. Here we examined the dynamics of exploration when human participants engaged in a probabilistic learning task with intermixed loss and gain trials, while simultaneously recording single-neuron activity. We show that neurons of the amygdala and temporal cortex modulate their activity before a decision to explore in both loss and gain. Moreover, we find that humans exhibit more exploration when trying to avoid losses, and that an increase in the levels of noise in amygdala neurons contributes to this behaviour. Overall, we report that human exploration is driven by two distinct neural mechanisms, a valence-independent rate signal and a valence-dependent global noise signal. The results suggest a link between the heightened amygdala activity observed in mood disorders^13,14 and higher exploration rates^15-17 that underlie maladaptive and even pathological behaviours.