Non-overlapping social and sucrose reward representations in the basolateral amygdala

Abstract

Animals must continually evaluate the relative value of social and nonsocial rewards to guide adaptive behavior. While both food and social stimuli engage overlapping reward networks, how these reward types are represented within specific nodes of the circuit remains unresolved. The basolateral amygdala (BLA), a region critical for valence and motivational processing, has been implicated in encoding both shared and distinct representations of social and food stimuli. Using in vivo calcium imaging in freely behaving male and female mice performing a two-choice social-sucrose operant task, we examined how individual BLA neurons encode these two different rewards within the same behavioral framework. We found that largely non-overlapping populations of BLA neurons respond to social and sucrose rewards, revealing distinct representational subspaces for each reward type. Under baseline conditions both sexes robustly encoded social and sucrose rewards, but water deprivation revealed a pronounced sex difference, shifting representations toward sucrose reward in females. Populations of sucrose reward responsive neurons in the BLA were selectively sensitive to reward omission. Specifically, sucrose-excited neurons were more strongly modulated by the absence of expected reward than sucrose-inhibited neurons, suggesting a key role for these neurons in signaling reward prediction violations. Together, these findings demonstrate that the BLA encodes social and sucrose rewards through distinct, state-dependent, and functionally heterogeneous neuronal populations, highlighting region-specific strategies for representing reward identity and internal motivational context. Significance Statement The brain’s capacity to weigh different types of rewards, like sucrose versus social interaction, is fundamental to survival yet remains poorly understood. By imaging neuronal activity in the basolateral amygdala (BLA) as mice freely choose between social and sucrose rewards, we found that largely distinct populations of BLA neurons encode each reward type. Internal state selectively altered the recruitment of reward-responsive BLA neurons in a sex-dependent manner. We further show that individual BLA neurons are differentially sensitive to the omission of expected rewards based on baseline responses. Together, these findings highlight the functional diversity through which the brain assigns value across reward modalities and dynamically adapts to changing motivational states.