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.

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Available from: Thomas R Insel, Jun 04, 2015
    • "Oxytocin (OT) is a neuropeptide hormone that plays an essential role in mammalian reproduction, particularly during birth and lactation. The oxytocinergic system also promotes mammalian bonding (Bales and Carter, 2003;Bielsky and Young, 2004;Cho et al., 1999;Insel and Hulihan, 1995;Insel, 2010) and enhances social, cognitive, and emotional functions in humans (Kirsch et al., 2005;Lee et al., 2009). These improved functions include the recognition of complex mental states and emotions (Domes et al., 2007), memory of faces (Rimmele et al., 2009), eye contact (Guastella et al., 2008), encoding of positive social memories and words (Guastella et al., 2008;Unkelbach et al., 2008), trust, and altruism (Zak et al., 2005). "
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    ABSTRACT: One of the leading hypotheses regarding the mechanism underlying the social effects of Oxytocin (OT) is the “social salience hypothesis”, which proposes that OT alters the attentional salience of social cues in a context-dependent manner. Recently, OT was implicated in the process of anthropomorphism; specifically, OT was found to increase the tendency to ascribe social meaning to inanimate stimuli. However, the precise component of social interaction that contributes to this effect remains unclear. Because OT plays a role in the response to touch, whether or not objects are touching in a social context may represent the prominent trigger. Given that OT plays a major role in both anthropomorphism and touch, it is reasonable to assume that OT enhances anthropomorphism specifically for non-human touch, further clarifying its role in altering the perceptual salience of social cues. Here, we examined whether intranasal delivery of OT influences anthropomorphism for touch in inanimate objects. To that end, we implicitly measured the emotional reactions of participants (N = 51) to photos that depicted two humans or two inanimate objects either touching or not touching. We asked them to rate whether they will include each photo in an emotional album and found that OT treatment increased the likelihood of inclusion in an emotional album to photos that contain touch, particularly between inanimate objects. In a follow-up experiment we found that the more human the inanimate objects were perceived, the more included they were in the emotional album. Our findings demonstrate that OT can enhance the social meaning of touch between two inanimate objects and advance our understanding of the mechanisms underlying the ability of OT to anthropomorphize environmental cues.
    No preview · Article · Jan 2016 · Psychoneuroendocrinology
    • "Regula Graf Nicole Ochsenbein-Kölble 1 Smell & Taste Clinic, Department of Otorhinolaryngology, TU Dresden, Fetscherstrasse 74, 01307 Dresden, Germany 2 Center of Expertise on Gender Dysphoria, Department of Medical Psychology, Neuroscience Campus Amsterdam, VU University Medical Center, De Boelelaan 1131, 1081 HX Amsterdam, The Netherlands olfactory bulb (Kendrick et al. 1997; Bale et al. 2001; Meddle et al. 2007; Insel 2010 "
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    ABSTRACT: Background Despite the large body of literature on the effects of oxytocin via the exchange of social chemo-signals, no previous study tested the effects of oxytocin stimulation during parturition on the mother’s chemical senses. Therefore, in the present study, we investigated the effects of oxytocin, administered via intramyometrial and intravenous injection, on general odor processing andgustatory functioning in women shortly after giving birth via Caesarean section. Methods General olfactory and gustatory sensitivity, and subjectively perceived taste intensities and hedonic ratings, next to self-reported mood and nausea were assessed 1 day before the Caesarean section in 21 women and again a few hours after the oxytocin stimulations. Results We found no changes in general olfactory sensitivity, self-reported mood, or nausea between test sessions. However, following oxytocin, women rated the quality of sweet taste as significantly more positive and tended to exhibit higher gustatory sensitivity. Conclusions Although this study was performed in a highly controlled clinical environment, we cannot rule out potential confounders related to parturition, and our interpretation on the specific effects of oxytocin therefore is limited. However, our findings agree with the literature reporting oxytocin effects on chemo-sensory functions. We speculate that an increased preference for sweet taste might be particularly relevant during the early post-partum and breastfeeding period, facilitating thenecessary nutrient supply to the newborn via the intake of calorie-rich carbohydrate food.
    No preview · Article · Dec 2015 · Chemosensory Perception
    • "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.
    No preview · Article · Oct 2015 · Hormones and Behavior
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