Habit learning shapes activity dynamics in the central nucleus of the amygdala

Abstract

A habit develops as a motivated behavior that is strengthened by extended experience and feedback. While the performance component of a habit is relatively well studied, being linked to action-related neural dynamics in the basal ganglia and beyond, neural mechanisms for outcome feedback during habit formation, the reinforcement component, remain unknown. One candidate for this feedback mechanism is in the central nucleus of the amygdala (CeA). Here, we identify CeA neural firing dynamics in male and female rats that serve to promote habit formation. We used a novel maze task with rewards of differing identity and value to show that habits arise with task overtraining. After showing that overtraining engages CeA as shown through elevated cFos expression, we recorded in-vivo CeA activity across learning, and after outcome devaluation when habitual behavior is most identifiable. Neuronal activity changes tracked with habit formation. During learning, a group of recorded cells were significantly responsive at the choice point of maze trials while others encoded outcome consumption. By late training, neural activity exhibited a rapid depression at the choice point of the maze and excitation during reward receipt. In both cases, outcome magnitude, but not identity, was a significant modulator of neural activity. Additionally, a population of neurons tracked instantaneous changes in animal run speed. These speed cells dramatically decreased in number as habits formed. Together, these findings support a role for the CeA in providing reinforcement for habitual behavior, offering a signal that marks successful performance, while identifying speed representations in the CeA. Significance Statement Habits enable efficient behavior but can also become inflexibly maladaptive. Although the neural circuits underlying habitual action execution have been studied extensively, the mechanisms by which outcome feedback reinforces habit formation remain poorly understood. Here, we show that neural activity in the central nucleus of the amygdala evolves with habit development, shifting from representations of choice and reward consumption to reinforcement-related signals during overtraining. Activity reflected outcome magnitude rather than identity, consistent with a role for the central amygdala in reinforcement. We also identify a previously unrecognized population of CeA neurons that track animal running speed. Together, these findings implicate the CeA as a source of reinforcement signals that promote habit formation.