Prosocial and Hypersocial Behavior: From Genes to Circuits and Behavior

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Background

Impaired and abnormal social behavior has been extensively studied as it is often associated with anxiety, antisocial personality disorders, and autism. Opposite manifestations of social functioning, such as the excessive need for social contact, emotional dependence on continuous social company, and attention, have also been recognized as potentially abnormal, but are much less well understood.

As with many behaviors, increased sociability exists on a continuum, ranging from prosociability to the more extreme hypersociability. Prosocial personality is considered advantageous in society, while hypersociability is often inappropriate and is frequently associated with neurodevelopmental disorders and child maltreatment. Twin studies suggest that prosocial behavior has a genetic basis. Similarly, pathological hypersociability can be due, at least partly, to variants in one or few genes, exemplified by Williams syndrome for example. Hypersocialbility can also be linked to genetically complex conditions with a polygenic structure often combined with environmental influences. As regards the environmental influence, early adverse care experience in adopted children has been consistently found to increase the likelihood of developing behavior referred to as indiscriminate friendliness, disinhibited social behavior, or disinhibited attachment disorder.

Prosocial and hypersocial behavior is not limited to human sociability; indeed it is observed in various social species suggesting the existence of evolutionary conserved mechanism/s. Domestic dogs, unlike human-socialized grey wolves, exhibit a heightened propensity to initiate social contact that is extended to members of other species. This suggests how selective breeding, presumably via genetic variability, modulates social behavior. Similarly, recombinant murine strains show a wide range of social behaviors from low to high tendency for social contact with non-familiar conspecifics. Animals, including rodents, exhibit more complex social behaviors such as “altruism” behaviors, i.e. increasing other conspecifics’ fitness through helping behaviors, as well as “empathy”.

Although hypersociability has a genetic and epigenetic basis, it is ultimately neuronal circuitry function/dysfunction that leads to behavioral manifestations. Human studies carried out with various imaging techniques, revealed the role of the amygdala in discriminating between fear-inducing and friendly social cues, to produce appropriate social behavior, while the dopaminergic reward/aversion system seems to assess the salience of social situations, modulating approach or avoidance behaviors.

We aim to integrate our current state of knowledge on prosociability and hypersociability encouraging contributions addressing this theme via human and other animals’ behavioral investigations focusing on the genetic, epigenetic, and neuronal circuit features underlying the different behaviors.

Topics of interest include, but are not limited to:

• GWAS studies on social behavior

• Mendelian traits and conditions with strong hypersociability profile

• Neural circuit-level studies focusing on functional imaging in humans

• Circuit mapping in other animals with state-of-the-art opto- and chemogenetic tools

• Current behavioral paradigms and future directions in measuring prosocial behavior, including behavioral models for empathy, altruism, and cooperation in nonhuman animals

• Novel AI tools able to recognize and track nuanced social behaviors that might be not obvious with standard methods

Ultimately, the combination of human and animal studies at the gene, neuron, circuit, and behavioral levels will lead to a better understanding of prosocial and hypersocial behavior.

Keywords: hypersociability, prosociability, social species, neural circuit, genetic variability

Important note: All contributions to this Research Topic must be within the scope of the section and journal to which they are submitted, as defined in their mission statements. Frontiers reserves the right to guide an out-of-scope manuscript to a more suitable section or journal at any stage of peer review.

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