Neural Circuit Mechanisms of Social Behavior

Abstract

We live in a world that is largely socially constructed, and we are constantly involved in and fundamentally influenced by a broad array of complex social interactions. Social behaviors among conspecifics, either conflictive or cooperative, are exhibited by all sexually reproducing animal species and are essential for the health, survival, and reproduction of animals. Conversely, impairment in social function is a prominent feature of several neuropsychiatric disorders, such as autism spectrum disorders and schizophrenia. Despite the importance of social behaviors, many fundamental questions remain unanswered. How is social sensory information processed and integrated in the nervous system? How are different social behavioral decisions selected and modulated in brain circuits? Here we discuss conceptual issues and recent advances in our understanding of brain regions and neural circuit mechanisms underlying the regulation of social behaviors.

Figure 1. Transformation of sensory inputs to social behavioral decisions in social contexts

(A) Schematic depicting social interaction between two individuals. Information from acute sensory inputs detected from the other individual (and the environment) is transformed into a behavioral output. The behavioral output in turn will provide sensory cues to the other individual, forming a reciprocal feedback loop for the duration of social interaction between the two individuals. (B) Examples of sensory inputs, internal states, and behavioral outputs that are involved in the sensory processing to behavioral decision transformation.

Figure 2. Current understanding of circuits and brain regions in males and females implicated in different social behaviors

(A) Overview of key social behavioral circuits and regions. (B) and (C) Circuits involved in male and female aggression. (D) and (E) Circuits involved in male and female mating. (F) Circuits involved in parenting in males and females. MOB: main olfactory bulb; AOB: accessory olfactory bulb; COApl/pm: posterolateral and posteromedial cortical amygdala; MeApd/pv: posterodorsal and posteroventral medial amygdala; BNSTpr: principal nucleus of the bed nucleus of the stria terminalis; PVN: paraventricular hypothalamic nucleus; AVPV: anteroventral periventricular hypothalamic nucleus; MPOA: medial preoptic area; VMHvl/dm: ventrolateral and dorsomedial subregions of the ventromedial hypothalamic nucleus; PMV: ventral premammillary hypothalamic nucleus; PAG: periaqueductal gray. In (B–F), some of the nodes and connections are hypothetical. Colored nodes and connections represent circuits with direct experimental evidence for the corresponding behavior.

Figure 3. Examples of different or similar sensory inputs leading to different behaviors

(A) The same individual experiencing different sensory inputs can lead to different behavioral outputs. (B) Different individuals experiencing the same sensory inputs can lead to different behavioral outputs.

Figure 4. Examples of experience-dependent changes of social behavioral decisions on different time scales

(A) A experience-dependent change in social internal state during a same-sex interaction leads to a change in behavior from investigation to aggression on the scale of minutes. (B) A heightened aggression state (i.e. higher probability for aggression) following an aggressive interaction on the scale of minutes. (C) A heightened aggression state following sexual experience on the scale of hours to days. (D) A change of an infanticidal to parenting state following sexual experience on the scale of weeks.