A neuronal mechanism for motivational control of behavior

Description The amygdala and goal-directed actions Almost everything we do in our daily lives is goal directed. The brain can maintain a motivational state to direct actions to achieve desired outcomes. Using deep-brain calcium imaging, electrophysiology, and optogenetics in mice, Courtin et al. observed that at the time of goal-directed action, basolateral amygdala principal neurons integrate and encode pursued outcome identity, pursued outcome value, and action-outcome contingency information. At the time of consumption, basolateral amygdala neuronal firing represents current outcome identity and value. Together, action- and consumption-associated activity integrate behaviorally relevant information at distinct time points along goal-directed action-consumption sequences. —PRS Basolateral amygdala principal neurons encode and maintain outcome-specific and updatable motivational states to direct mouse behavior. INTRODUCTION Acting to achieve goals underlies animals’ behavioral flexibility and depends on the ability to motivate specific behaviors. Formal studies of goal-directed behavior are based on paradigms such as instrumental conditioning, in which subjects learn that specific actions result in a particular outcome. By definition, instrumental goal-directed actions are oriented toward specific outcomes and are sensitive to variations in outcome value and action-outcome contingency. However, the neuronal mechanisms that encode and maintain specific motivational control of self-paced behavior are poorly understood. RATIONALE Animal motivation to engage in goal-directed behavior is governed by a multitude of factors, ranging from the animal’s general metabolic state to specific task parameters including outcome identity, outcome value, and action-outcome contingency. Using Ca2+ imaging, electrophysiology, and optogenetic manipulations, we examined the relationship between noncued, self-paced goal-directed actions and neuronal responses in the amygdala. Although the amygdala is a brain structure well known for encoding associative learning in the context of cue-triggered outcome-seeking behaviors, here, we specifically focused on neuronal correlates of essential parameters supporting goal-directed actions, both during action execution and reward consumption. RESULTS Mice were trained in a self-paced, instrumental goal-directed task in which one action led to the delivery of a sucrose reward and another action to the delivery of a milk reward, with no explicit stimuli signaling trial start or reward availability. Based on an automatically derived description of mouse behavior, we showed that after 5 days of training, mice exhibited stereotypical self-paced behavioral sequences, alternating between periods of action execution when mice pursued a goal and reward consumption when the goal was attained. Using in vivo deep-brain Ca2+ imaging and electrophysiology, we found distinct outcome-specific ensembles of amygdala neurons activated during action-consumption sequences. These ensembles were spatially intermingled and broadcasted behaviorally relevant information to multiple striatum subregions. At the population level, distinct amygdala neuronal activity patterns tiled the entire action-consumption behavioral sequences. These internally generated action- and consumption-associated patterns maintained outcome-specific information along the session and across days. Optogenetic inhibition of amygdala neurons during either action or consumption caused distinct behavioral phenotypes and indicated that action- and consumption-associated amygdala activity was necessary for the outcome-specific motivational control of goal-directed behavior. Last, in agreement with experimental psychology models, we showed that action and consumption representations learned during training can be retrieved, truncated, or remapped upon manipulations of outcome value, such as after outcome devaluation or extinction or upon degradation of action-outcome contingency. More specifically, whereas outcome devaluation resulted in the immediate emergence of new action and outcome representations, action-outcome contingency degradation resulted in a gradual loss of the action representation with no effect on reward consumption representation. CONCLUSION We show here that the interplay between distinct outcome-specific and updatable neuronal activity patterns encodes and maintains specific motivational states necessary for the execution of adaptive, self-initiated action-consumption sequences. Amygdala neurons segregated behaviorally relevant information along different axes, such as outcome identity, value, and expectancy. Our study thus introduces the concept of specific motivation and extends the classic view that the amygdala controls outcome-seeking behavior by conferring value to outcome-predicting sensory stimuli. A neuronal mechanism for noncued goal-directed behavior. (A) The interplay between distinct neuronal activity patterns encodes and maintains behaviorally relevant information at distinct time points along goal-directed action-consumption behavioral sequences. (B) Outcome-specific action and consumption patterns reflect the maintenance of a specific motivational state. Upon behavioral perturbations, action and consumption patterns differentially adapt. This adaptive code might be key to direct behavior toward a pursued goal. 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 Ca2+ 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.