Neural correlates of pair-bonding in a monogamous primate

Abstract

The neurobiology of social bonding, despite its relevance to human mental health, has been studied primarily in rodents. In this study we used position emission tomography (PET), registered with structural magnetic resonance imaging (MRI) to investigate central glucose uptake in seventeen males of a monogamous primate species, the titi monkey (Callicebus cupreus). Twelve pair-bonded males (including six with a lesion of the prefrontal cortex) and five lone males were scanned. The five lone males were re-scanned 48 hours after pairing with a female. Significant differences in glucose uptake were found between males in long-term pair-bonds and lone males in areas including the nucleus accumbens, ventral pallidum, medial preoptic area, medial amygdala, and the supraoptic nucleus of the hypothalamus. In paired before and after comparisons, males showed significant changes following pairing in the right nucleus accumbens and ventral pallidum but not in other areas. Lesioned males showed significantly higher uptake in the posterior cingulate cortex than all other males. These results indicate some basic similarities between rodents and primates in the formation and maintenance of selective social bonds, but emphasize the importance of studying long-term maintenance in addition to short-term formation of social bonds.

Reexamining Human Origins in Light of Ardipithecus ramidus

“…AVP receptor distributions in monogamous marmosets (91,92) and titi monkeys (93), as well as in polygnous rhesus macaques (94), parallel those observed in monogamous and promiscuous voles, respectively, confirming that this reward pathway functions similarly in primates. Although receptor distributions such as those now available for some monkey species are not yet available for humans, there are marked parallels in other related cerebral phenomena revealed by functional magnetic resonance imaging (see also below).…”

Neurobiological mechanisms of social attachment and pair bonding

“…These data have contributed to the hypothesis that pair bonds represent social addictions between mating partners, mediated in part by organization and plasticity of mesolimbic DA pathways [33]. Studies in the zebra finch and coppery titi monkey have also reported reorganization in mesolimbic reward areas following bond formation, suggesting that neural plasticity in these pathways may be an evolutionarily conserved feature of pair bonding across species [34,35]. …”

Oxytocin receptor gene sequences in owl monkeys and other primates show remarkable interspecific regulatory and protein coding variation

“…Functioning in these ways, OT plays an important role 82 in positive social interactions, such as grooming, sex, childbirth 83 and parental care (Carter et al, 2008). OT has also been associated 84 with social signaling (Bales et al, 2007a;Bales et al, 2007b;Bales 85 et al, 2007c), and deficits in the processing of social information 86 have been linked to low OT levels (Takayanagi et al, 2005). 87 Furthermore, it has been suggested that the social deficits in 88 certain autism spectrum disorders in humans might be related to 89 low levels of OT (Wu et al, 2005;Jacob et al, 2007;Gregory 90 et al, 2009), although inconsistent findings relating oxytocin to 91 autism have been noted (Tansey et al, 2010).…”