The ability to efficiently switch from one defensive strategy to another maximizes an animals chance of survival. Here, we demonstrate that the selection of active defensive behaviors requires the coordinated activation of dopamine D2 receptor (D2R) signaling within the central extended amygdala (EA) comprising the nucleus accumbens, the oval bed nucleus stria terminals and the central amygdala. We find that discriminative learning between predictive and non-predictive threat auditory stimuli is unaltered in mice carrying a temporally-controlled deletion of D2R within output neurons of the EA. In contrast, intact EA D2R signaling is required for active avoidance learning and innate flight responses triggered by a visual threat stimulus (looming). Consequently, conditional D2R knockout mice biased defensive responses toward passive defensive strategies. Altogether, these findings identify EA D2R signaling as an important mechanism by which DA regulates the switch from passive to active defensive behaviors, regardless whether of learned or innate threat.
In mammals, the ability to optimize and select behavioral strategies is a cardinal and conserved psychophysiological feature for maximizing the chances of survival. However, the neural circuits and underlying mechanisms regulating this flexible feature remain yet unsolved. Here, we demonstrate that such optimization relies on dopamine D2 receptors (D2R) within a subcircuit spanning across the extended amygdala (EA) and the tail of the striatum (TS). Using a mouse model carrying a temporally controlled deletion of D2R within a subcircuit defined by WFS1 neurons, we found that intact EA D2R signaling is necessary to regulate homeostasis-dependent food-seeking behaviors in both male and female mice as well as active avoidance learning and innate escape responses in males. Altogether, these findings identify EA and TS D2R signaling as a novel hub through which dopamine optimizes appetitive behaviors and regulates the switch from passive to active defensive behaviors, regardless of learned or innate threats.
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