Dopamine Modulation of Reunion Behavior in Short and Long Term Marmoset Pairs

Abstract

One major neurobiological substrate regulating social processes is dopamine (DA). DA is implicated in social behavior in species as diverse as fish and birds, and has an established role in regulating relationships between mates in socially monogamous rodents. Marmoset monkeys display traits associated with social monogamy including high rates of affiliation, biparental care, distress upon separation, and aggression toward strangers; several of these behavioral patterns change throughout the development of relationships. This temporal change may represent changing demands, as pairs are likely to jointly face new experiences (e.g., parenthood) throughout pairing. We investigated the role of DA and pairing length on social behavior during reunion after separation from the mate. Marmosets were removed from their home environment and treated with agonists and antagonists for the D1 and D2 receptor subtypes. They were exposed to a novel environment containing an opposite-sex stranger and their pair mate, and then reunited with their mate in the home enclosure. Marmosets in long term pairs exhibited higher levels of food sharing during reunion than marmosets in short term pairs, with females in long term pairs sharing food more than males; no sex difference was observed in short term pairs. Subjects in short term pairs spent more time grooming their mate than receiving grooming during reunion, while marmosets in long term pairs displayed similar amounts of both initiated and received grooming. DA treatment altered pair-level behavior. When females received either a D2 agonist or antagonist, short term pairs spent less time in proximity, compared to when males received the same treatments. In long term pairs, treatment of females with either a D1 agonist or antagonist resulted in pairs spending less time in social proximity than when males were treated. These findings suggest that the function of the DA system in mate behavior may be similar between rodents and primates, with the D1 system modulating the expression of behavior in long term pairs and the D2 system regulating behavior in short term pairs. Furthermore, these results supplement a large body of work suggestive of deep evolutionary roots of the DA system in regulating social behavior.

Evolution of affiliation: patterns of convergence from genomes to behaviour

“…Siganid rabbitfishes [19]) and allogrooming (e.g. common marmosets [20]). Affiliative behaviours are often reciprocated between partners and provide mutual fitness benefits, including mate and offspring guarding/provisioning and assisted resource defence [21].…”

“…After pair bonds have been established, D1R density in the nucleus accumbens increases, likely inhibiting the formation of new partnerships [44]. Similarly, in common marmosets, D2Rs regulate partner proximity behaviour in new pairs, whereas D1Rs do so in long-term pairs [20]. In zebra finches, dopamine levels in the brain increase with pair bond formation [48] and decrease with pair bond maintenance [49].…”

Dopamine receptor manipulation does not alter patterns of partner preference in long-term marmoset pairs

“…Second, this study provides an important stepping stone between the well-documented role of the DA system in rodent models of social monogamy and the less understood role of DA in regulating nonhuman and human primate social behavior. While previous research has found similarities in the way in which the DA system regulates social interest and behavior between primates and rodents [16,17], the current study highlights the potential for the DA system to function differently in primates than in prairie voles in regulating social interactions. This lack of specialization in the DA system may underlie the behavioral flexibility that is characteristic of both marmoset and human social relationships.…”

“…This pattern is not observed when females in short term pairs receive treatment manipulating the D1R. However, when female marmosets from long term pairs receive manipulation (agonist or antagonist) of the D1R, the pair displays reduced proximity behavior during reunion compared to when males receive the same treatment, while proximity behavior patterns during reunion are unaffected by manipulation of the D2R [17]. Together, this set of findings suggests that the distinct roles of the D1Rs in mediating maintenance of attachment, and D2Rs in regulating formation of attachments in socially monogamous primate behavior may be conserved from rodents to primates.…”