ABSTRACT
Male sexual behavior is innate and rewarding. Despite its centrality to reproduction, a molecularly specified neural circuit governing innate male sexual behavior and reward remains to be characterized. We have discovered a developmentally wired neural circuit necessary and sufficient for male mating. This circuit connects chemosensory input to BNSTprTac1 neurons, which innervate POATacr1 neurons that project to centers regulating motor output and reward. Epistasis studies demonstrate that BNSTprTac1 neurons are upstream of POATacr1 neurons, and BNSTprTac1-released substance P following mate recognition potentiates activation of POATacr1 neurons through Tacr1 to initiate mating. Experimental activation of POATacr1 neurons triggers mating, even in sexually satiated males, and it is rewarding, eliciting dopamine release and self-stimulation of these cells. Together, we have uncovered a neural circuit that governs the key aspects of innate male sexual behavior: motor displays, drive, and reward.
Subject(s)
Neural Pathways , Sexual Behavior, Animal , Animals , Male , Neurons/physiology , Reward , Sexual Behavior, Animal/physiology , MiceABSTRACT
Exploration of novel environments ensures survival and evolutionary fitness. It is expressed through exploratory bouts and arrests that change dynamically based on experience. Neural circuits mediating exploratory behavior should therefore integrate experience and use it to select the proper behavioral output. Using a spatial exploration assay, we uncovered an experience-dependent increase in momentary arrests in locations where animals arrested previously. Calcium imaging in freely exploring mice revealed a genetically and projection-defined neuronal ensemble in the basolateral amygdala that is active during self-paced behavioral arrests. This ensemble was recruited in an experience-dependent manner, and closed-loop optogenetic manipulation of these neurons revealed that they are sufficient and necessary to drive experience-dependent arrests during exploration. Projection-specific imaging and optogenetic experiments revealed that these arrests are effected by basolateral amygdala neurons projecting to the central amygdala, uncovering an amygdala circuit that mediates momentary arrests in familiar places but not avoidance or anxiety/fear-like behaviors.
Subject(s)
Basolateral Nuclear Complex/physiology , Central Amygdaloid Nucleus/physiology , Exploratory Behavior/physiology , Nerve Net/physiology , Animals , Basolateral Nuclear Complex/diagnostic imaging , Behavior, Animal/physiology , Central Amygdaloid Nucleus/diagnostic imaging , Female , Locomotion , Machine Learning , Male , Mice, Inbred C57BL , Neurons/physiology , Optical ImagingABSTRACT
Neuropsychiatric disorders often manifest with abnormal control of motor behavior. Common symptoms include restricted and repetitive patterns of behavior (RRBs). Cortico-basal ganglia circuits have been implicated in the etiology of RBBs. However, there is a vast range of behaviors encompassed in RRBs, from simple explosive motor tics to rather complex ritualized compulsions. In this review, we highlight how recent findings about the function of specific basal ganglia circuits can begin to shed light into defined motor symptoms associated with neuropsychiatric disorders. We discuss recent studies using genetic animal models that advocate that different aspects of motor repetition in neurodevelopmental disorders, like obsessive-compulsive disorder and autism spectrum disorder, emerge from particular dysregulations in distinct cortico-basal ganglia circuits.
