The Challenge of Translation in Social Neuroscience: A Review of Oxytocin, Vasopressin, and Affiliative Behavior

National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA.
Neuron (Impact Factor: 15.05). 03/2010; 65(6):768-79. DOI: 10.1016/j.neuron.2010.03.005
Source: PubMed


Social neuroscience is rapidly exploring the complex territory between perception and action where recognition, value, and meaning are instantiated. This review follows the trail of research on oxytocin and vasopressin as an exemplar of one path for exploring the "dark matter" of social neuroscience. Studies across vertebrate species suggest that these neuropeptides are important for social cognition, with gender- and steroid-dependent effects. Comparative research in voles yields a model based on interspecies and intraspecies variation of the geography of oxytocin receptors and vasopressin V1a receptors in the forebrain. Highly affiliative species have receptors in brain circuits related to reward or reinforcement. The neuroanatomical distribution of these receptors may be guided by variations in the regulatory regions of their respective genes. This review describes the promises and problems of extrapolating these findings to human social cognition, with specific reference to the social deficits of autism.


Available from: Thomas R Insel, Jun 04, 2015
    • "However, few experiments focus on how nonapeptides might be acting in the brain as social behavior is developing . Yet the paucity of comparative developmental data has not slowed the speculation that nonapeptides may be implicated in the development of social deficit disorders in humans (Carter, 2007; Insel, 2010; Kenkel et al., 2014; Marazziti and Dell'Osso, 2008). To our knowledge, there is only one experiment providing evidence that the nonapeptides underlie differences in social behaviors during development in any nonrodent species: systemic injections of AVT altered approach behavior to an imprinting stimulus in newly-hatched ducklings (Martin et al., 1979; Martin and Van Wimersma Greidanus, 1978). "
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    ABSTRACT: Zebra finches demonstrate selective affiliation between juvenile offspring and parents, which, like affiliation between pair partners, is characterized by proximity, vocal communication and contact behaviors. This experiment tested the hypothesis that the nonapeptide arginine vasotocin (AVT, avian homologue of vasopressin) and nonapeptide receptors play a role prior to fledging in the development of affiliative behavior. Zebra finch hatchlings of both sexes received daily intracranial injections (post-hatch days 2-8) of either AVT, Manning Compound (MC, a potent V1a receptor antagonist) or saline (vehicle control). The social development of both sexes was assessed by measuring responsiveness to isolation from the family and subsequent reunion with the male parent after fledging. In addition, we assessed the changes in affiliation with the parents, unfamiliar males, and unfamiliar females each week throughout juvenile development. Compared to controls, MC subjects showed decreased attachment to the parents and MC males did not show the normal increase in affiliative interest in opposite sex individuals as they reached reproductive maturity. In contrast, AVT subjects showed a sustained affiliative interest in parents throughout development, and males showed increased interest in opposite sex conspecifics as they matured. These results provide the first evidence suggesting that AVT and nonapeptide receptors play organizational roles in social development in a bird.
    Hormones and Behavior 10/2015; 78. DOI:10.1016/j.yhbeh.2015.10.005 · 4.63 Impact Factor
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    • "In particular, they suggest that oxytocin has an influential role on sociosexual interaction by facilitating social motivational and memory processes. There is considerable evidence that highly affiliative animal species have oxytocin receptors in specific brain circuits that are related to reward and reinforcement (Donaldson, 2008; Insel, 2010) and that these are important for social cognition. Until recently convincing similar evidence for humans has been lacking. "
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    DESCRIPTION: This short monograph describes the motivational system that underlies childbearing, as represented by the author's Traits-Desires-Intentions Behavior framework. It then examines how the three motivational components of this framework are related to consciousness, how they are affected by executive functions, and how they are represented and integrated within the brain. Finally, it briefly describes how this motivational system affects the set of behaviors that influence reproductive outcomes.
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    • "The role of the oxytocin and vasopressin systems in social functioning has developed out of a large body of animal research, focusing primarily on rodents. This literature has been extensively reviewed elsewhere (Wang et al., 1998; Insel, 2010). For example, oxytocin has been pituitary; and the V2 receptor is found primarily in the kidneys. "
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    ABSTRACT: Oxytocin and vasopressin are pituitary neuropeptides that have been shown to affect social processes in mammals. There is growing interest in these molecules and their receptors as potential precipitants of, and/or treatments for, social deficits in neurodevelopmental disorders, including autism spectrum disorder. Numerous behavioral-genetic studies suggest that there is an association between these peptides and individual social abilities; however, an explanatory model that links hormonal activity at the receptor level to complex human behavior remains elusive. The following review summarizes the known associations between the oxytocin and vasopressin neuropeptide systems and social neurocircuits in the brain. Following a micro- to macro- level trajectory, current literature on the synthesis and secretion of these peptides, and the structure, function and distribution of their respective receptors is first surveyed. Next, current models regarding the mechanism of action of these peptides on microcircuitry and other neurotransmitter systems are discussed. Functional neuroimaging evidence on the acute effects of exogenous administration of these peptides on brain activity is then reviewed. Overall, a model in which the local neuromodulatory effects of pituitary neuropeptides on brainstem and basal forebrain regions strengthen signaling within social neurocircuits proves appealing. However, these findings are derived from animal models; more research is needed to clarify the relevance of these mechanisms to human behavior and treatment of social deficits in neuropsychiatric disorders.
    Frontiers in Neuroscience 09/2015; 9. DOI:10.3389/fnins.2015.00335 · 3.66 Impact Factor
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