Behaviors such as mating, territorial defense, parenting or predator avoidance, despite being instinctive, are modulated by social experience. Because instinctive behaviors can be elicited without any previous social experience, it is believed that the brain circuits mediating the recognition of social information are, at least in part, genetically determined. A fundamental question is to understand how the brain interprets different types of social information.
Classical ethological studies have uncovered distinct sex- and species-specific signals underlying social recognition. For example, songbirds recognize specific spectra of tweets emitted by closely related bird species; domestic chickens show increased alarm when shown bird decoys with shorter necks and longer tails, a common feature in raptors. These findings, in turn, have paved the way for direct mechanistic inquiries on the identity and function of central neural circuits mediating social interactions.
In rodents, the processing of animal cues by the vomeronasal system is essential for proper discrimination of sex-specific social signals and identification of predators. Pheromonal cues emitted during social encounters are detected by vomeronasal receptors expressed by VNO neurons. The specific patterns of neuronal activation in the VNO are further processed in the accessory olfactory bulb (AOB), and next in the medial amygdala (MeA), which in turn connects to hypothalamic regions associated with the control of distinct social behaviors. Previous work from our lab (Bergan et al., 2014) using electrical recording in the MeA of anesthetized mice have revealed differences in the neural responses of males and females to social cues. In this work, we study how social information is represented in awake behaving mice, and how this representation changes according to the animal’s sex, and previous social experience to modulate the animal behavior.
In collaboration with the laboratory of Mark Schnitzer at Stanford, we have used a head-mounted miniature microscope that enables long-term optical imaging in deep brain tissue of awake behaving mice. We have monitored the calcium activity of large neuronal ensembles of the MeA when the mice are engaged in various social interactions over the span of several months. Our data reveal that the representation of social information in the MeA is different in males and females, and relies on information provided by the activity of individual cells as well as the more complex dynamics of large neuronal populations. By performing long-term Ca2+ imaging in animals with different social experiences, we found that mating triggers sex-specific changes in the MeA representation of social information. Intriguingly, these experience-dependent changes preferentially enhance the discrimination of social cues from the opposite sex (both in males and females), and persists for at least a month after the animal is separated from its mating partner. At the mechanistic level, we were able to demonstrate that, in males, some of the changes induced by mating are likely driven by the neuropeptide oxytocin.
Our work unveils how social information is represented in the MeA, a key hub of the sensory-motor transformation from chemosensory detection to instinctive behaviors. This study enables us to better understand the nature of the neural codes by which the brain generates an internal representation of social information.