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Memory encoding and retrieval rely on specific interactions across multiple brain areas. Although connections between individual brain areas have been extensively studied, the anatomical and functional specificity of neuronal circuit organization underlying information transfer across multiple brain areas remains unclear. Here, we combine transsynaptic viral tracing, optogenetic manipulations, and calcium dynamics recordings to dissect the multisynaptic functional connectivity of the amygdala. We identify a distinct basolateral amygdala (BLA) subpopulation that connects disynaptically to the periaqueductal gray (PAG) via the central amygdala (CeA). This disynaptic pathway serves as a core circuit element necessary for the learning and expression of conditioned fear and exhibits learning-related plasticity. Together, our findings demonstrate the utility of multisynaptic approaches for functional circuit analysis and indicate that disynaptic specificity may be a general feature of neuronal circuit organization.

Acting to achieve goals depends on the ability to motivate specific behaviors based on their predicted consequences given an individual’s internal state. However, the underlying neuronal mechanisms that encode and maintain such specific motivational control of behavior are poorly understood. Here, we used Ca 2+ imaging and optogenetic manipulations in the basolateral amygdala of freely moving mice performing noncued, self-paced instrumental goal-directed actions to receive and consume rewards. We found that distinct neuronal activity patterns sequentially represent the entire action-consumption behavioral sequence. Whereas action-associated patterns integrated the identity, value, and expectancy of pursued goals, consumption-associated patterns reflected the identity and value of experienced outcomes. Thus, the interplay between these patterns allows the maintenance of specific motivational states necessary to adaptively direct behavior toward prospective rewards.