Neural mechanisms of social homeostasis

Abstract

Social connections are vital to survival throughout the animal kingdom and are dynamic across the life span. There are debilitating consequences of social isolation and loneliness, and social support is increasingly a primary consideration in health care, disease prevention, and recovery. Considering social connection as an "innate need," it is hypothesized that evolutionarily conserved neural systems underlie the maintenance of social connections: alerting the individual to their absence and coordinating effector mechanisms to restore social contact. This is reminiscent of a homeostatic system designed to maintain social connection. Here, we explore the identity of neural systems regulating "social homeostasis." We review findings from rodent studies evaluating the rapid response to social deficit (in the form of acute social isolation) and propose that parallel, overlapping circuits are engaged to adapt to the vulnerabilities of isolation and restore social connection. By considering the neural systems regulating other homeostatic needs, such as energy and fluid balance, we discuss the potential attributes of social homeostatic circuitry. We reason that uncovering the identity of these circuits/mechanisms will facilitate our understanding of how loneliness perpetuates long-term disease states, which we speculate may result from sustained recruitment of social homeostatic circuits.

Keywords: loneliness; motivational state; neural circuits; social homeostasis; social isolation; social rank.

Figure 1.

Proposed model for social homeostasis. Based on Cannon’s classic model for homeostatic regulation we propose that a social homeostatic system consists of a detector to sense a change in overall quantity/quality of social contact, a control center to compare this deviation to the individual’s set-point, and effector systems to correct the change. (a) Detection of social signals (both their quantity and quality) would require social recognition. in order to facilitate recall of previous social encounters and determine the expectation for interaction. Information relevant to the identity of the social agent (recognizing that individual as such) as well as estimation of their relative social rank would be required for appropriate evaluation of a deviation. Integration of this information may occur at the level of the detector (model A) or the control center (model B) stage of processing. Identity and rank information may be represented in an overlapping or nonoverlapping fashion (callout box). For a familiar animal both these variables may be incorporated to set social expectation, but for an unfamiliar animal only rank perception would be available. (b) Deviations from the set-point would be evaluated within the control center by comparing the current social input to the homeostatic set-point for quantity and/or quality of social contact. The social control center may integrate information pertinent to other homeostatic needs (e.g., energy balance, fluid balance, and thermoregulation) in a “hub and spoke” fashion (model A), or the social control center may be subservient to other homeostatic control systems (model B). Alternatively, integration of homeostatic needs may occur in a convergent arrangement onto shared effector systems (model C), with interconnections between control centers (model D). (c) If a deviation from set-point is determined, effector systems may be engaged to correct the change. This process could include activation of “external” effectors to promote behavioral adaptation (e.g., social approach/avoidance) along with “internal” effectors to adjust internal/emotional state (model A). Alternatively, engagement of internal effector systems, and a change in emotional state, may itself promote behavioral adaptation (model B).

Figure 2.

Neural circuit components implicated in the response to social deficit. Pathways, neuromodulators, neuropeptides, and receptors showing modifications following acute social isolation in rodents. Circuit components are colored based on their involvement in hypervigilance, social motivation, and passive coping. Other prominent projections/connections are shown in grey. Coordinated activity across these parallel, overlapping circuits may function to maintain social homeostasis by heightening attention to environmental stimuli, motivating social reconnection, and limiting emotional distress. 5-HT, 5-hydroxytryptamine (serotonin); ACTH, adrenocorticotropic hormone; AT₁, angiotensin II receptor 1; BNST, bed nucleus of the stria terminalis; CeA, central amygdala; CRF, corticotropin-releasing factor; CRFR_1/2, corticotropin-releasing factor receptor; DA, dopamine; D_1/2, dopamine D_1/2 receptor; DRN, dorsal raphe nucleus; Hp, hippocampus; KOR, ĸ-opioid receptor; LC, locus coeruleus; MeA, medial amygdala; MOR, μ-opioid receptor; NAc, nucleus accumbens; NE, norepinephrine; OT, oxytocin; PFC, prefrontal cortex; PVN, paraventricular hypothalamic nucleus; VMH, ventromedial hypothalamus; VTA, ventral tegmental area.

Figure 3.

Long-term integration of social experience within a homeostatic system. (a) Under normal conditions, appropriate functioning of a social homeostatic system would maintain social contact quantity/quantity within an acceptable dynamic range. Experienced social interactions may be assimilated and assessed (compared with set-point) in a sliding window fashion across time (e.g., days/months). Social quality and quantity information might be weighted differently depending on the individual (traits) and current environmental conditions. The set-point could be determined by a combination of factors including age, sex, species-typical behavior, and past history of social encounters. (b) Failure of homeostatic system to correct deviations in social contact quantity/quality might result in a chronic deficit. This deficit (whether perceived or actual) may be associated with chronic engagement of homeostatic effector systems, and experienced as a state of loneliness. (c) Major life or environmental changes, such as moving away from home, switching jobs, and others, might provoke the need for a shift in set-point. A stable shift in set-point, and acceptance of a new expected quantity/quality for social contact, could represent an adaptive change. This shift may prevent social homeostatic effector systems from being chronically recruited and promote continued balance.