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Oxytocin, Vasopressin, and Human Social Behavior. (PDF YFRNE 404 No. of Pages 10, Model 5G ARTICLE IN PRESS 18 June 2009 Disk Used Frontiers in Neuroendocrinology xxx (2009) xxx–xxx 1 Contents lists available at ScienceDirect Frontiers in Neuroendocrinology journal homepage: www.elsevier.com/locate/yfrne 2 Review 3 Oxytocin, vasopressin, and human social behavior 4 Markus Heinrichs *, Bernadette von Dawans, Gregor Domes 5 Department of Psychology, Clinical Psychology and Psychobiology, University of Zürich, Zürich, Switzerland 6 article info abstract 238 9 Article history: There is substantial evidence from animal research indicating a key role of the neuropeptides oxytocin 24 10 Available online xxxx (OT) and arginine vasopressin (AVP) in the regulation of complex social cognition and behavior. As social 25 interaction permeates the whole of human society, and the fundamental ability to form attachment is 26 11 Keywords: indispensable for social relationships, studies are beginning to dissect the roles of OT and AVP in human 27 12 Neuropeptides social behavior. New experimental paradigms and technologies in human research allow a more nuanced 28 13 Oxytocin investigation of the molecular basis of social behavior. In addition, a better understanding of the neuro- 29 14 Arginine vasopressin biology and neurogenetics of human social cognition and behavior has important implications for the 30 15 Social behavior current development of novel clinical approaches for mental disorders that are associated with social def- 31 16 Stress 17 Anxiety icits (e.g., autism spectrum disorder, social anxiety disorder, and borderline personality disorder). This 32 18 Attachment review focuses on our recent knowledge of the behavioral, endocrine, genetic, and neural effects of OT 33 19 Affiliation and AVP in humans and provides a synthesis of recent advances made in the effort to implicate the 34 20 Approach behavior oxytocinergic system in the treatment of psychopathological states. 35 21 Psychobiological therapy Ó 2009 Elsevier Inc. All rights reserved. 36 22 37 38 39 1. Introduction amygdala are activated by OT and AVP receptor stimulation, 62 through which these peptides modulate the integration of excit- 63 40 In non-human mammals, receptors for the neuropeptides oxyto- atory information from the amygdala and cerebral cortex in oppo- 64 41 cin (OT) and arginine vasopressin (AVP) are distributed in various site manners. These results suggest that the endogenous balance 65 42 brain regions [94] associated with the central nervous control of between OT and AVP receptor expression and activation may set 66 43 stress and anxiety and with social behavior, including parental care, distinct, individually tuned levels for the activation of the auto- 67 44 pair-bonding, social memory, and social aggression. Specifically, OT nomic fear response. In general, centrally active AVP seems to be 68 45 seems both to enable animals to overcome their natural avoidance of associated with increased vigilance, anxiety, arousal, and activa- 69 46 proximity and to inhibit defensive behavior, thereby facilitating ap- tion, while OT has behavioral and neural effects associated with re- 70 47 proach behavior [24,26,28,45,84,124,147,164]. AVP has primarily duced anxiety, relaxation, growth, and restoration [25]. Thus, both 71 48 been implicated in male-typical social behaviors, including aggres- peptide hormones are important in social stress and in social inter- 72 49 sion, pair-bond formation, scent marking, and courtship [24,28,45, action, and in turn, a dysregulated activity may be associated with 73 50 104,165]. mental disorders of psychosocial relevance. While much of the 74 51 Aside from its effects on social behavior, OT shows significant knowledge regarding the ability of OT and AVP to regulate social 75 52 binding in the limbic system, including the amygdala [80,81, interactions is based on data from animals using centrally admin- 76 53 94,132], and decreases anxiety and the neuroendocrine response istered agonists and antagonists or knockout mice, initial studies 77 54 to stress in social interactions [11,27,120,123,158,159]. In contrast, suggest similar social and stress-related effects of both neuropep- 78 55 AVP seems to play an anxiogenic role, with elevated AVP expres- tides in humans (for review, see [12,68]). 79 56 sion in the hypothalamic paraventricular nucleus being associated Here, we review recent advances in the endeavor to understand 80 57 with increased behavioral and neuroendocrine anxiety levels the role of OT and AVP in human social behavior. In the first part of 81 58 [117]. In addition, Ferris and colleaguesUNCORRECTED[49] showed that the orally this review, we summarize PROOF the methodological approaches in hu- 82 59 active AVP V1a receptor antagonist SRX251 selectively blocks man neuropeptide research and examine the significance of OT 83 60 aggressive behavior in hamsters. At a cellular level, Huber and col- in stress-responsiveness, anxiety and prosocial behavior. In the 84 61 leagues [80] reported that distinct populations of neurons in the second part, we address the role of AVP in social behavior. Finally, 85 we conclude by outlining the clinical implications for mental disor- 86 ders that are associated with social deficits, and provide a synthesis 87 * Corresponding author. Address: Department of Psychology, Clinical Psychology and Psychobiology, University of Zürich, Binzmühlestrasse 14/Box 8, CH-8050 of the interactions of anxiety and stress, social approach behavior, 88 Zürich, Switzerland. Fax: +41 44 635 7159. and the oxytocinergic system. 89 E-mail address: [email protected] (M. Heinrichs). 0091-3022/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.yfrne.2009.05.005 Please cite this article in press as: M. Heinrichs et al., Oxytocin, vasopressin, and human social behavior, Front. Neuroendocrinol. (2009), doi:10.1016/ j.yfrne.2009.05.005 YFRNE 404 No. of Pages 10, Model 5G ARTICLE IN PRESS 18 June 2009 Disk Used 2 M. Heinrichs et al. / Frontiers in Neuroendocrinology xxx (2009) xxx–xxx 90 2. Methodological approaches in human neuropeptide research if breast-feeding starts 30–60 min before stress exposure, depend- 151 ing on the kind of stressor [3,6,70]. As no effect of stress has been 152 91 Our current knowledge of the behavioral effects of neuropep- found on OT plasma levels, OT does not seem to mediate the atten- 153 92 tides in humans is based on: (i) correlational studies measuring uation of cortisol stress responses at the adrenal level [72]. Thus, 154 93 OT or AVP in urine, saliva, blood or CSF, (ii) correlational studies the inhibitory effect of OT on HPA axis responsiveness points to a 155 94 involving genotyping of receptor polymorphisms, and (iii) experi- more central modulation and could, in fact, be localized in the 156 95 mental studies manipulating the availability of OT or AVP using paraventricular nucleus and in the septum, as demonstrated in rats 157 96 intravenous or intranasal administration. All of these approaches [120,121]. Interestingly, breast-feeding mothers with increased 158 97 bear different levels of invasiveness and side effects and do not plasma OT in response to a speech stressor that immediately fol- 159 98 have an equivalent informative value in terms of the underlying lowed baby-holding were found to have lower blood pressure than 160 99 central nervous mechanisms of the peptides. mothers with a decrease in OT after stress [103]. Furthermore, non- 161 100 Whereas the assessment and interpretation of urine or saliva postpartum healthy women who showed increased plasma OT lev- 162 101 measures provide inconsistent findings and need further investiga- els in response to positive emotion and massage and who main- 163 102 tion [9,29,51,79,157], CSF levels of OT or AVP are accompanied by tained OT levels during negative emotion were less likely to 164 103 high invasiveness. Besides the endogenous stimulation of OT during report interpersonal problems associated with intrusiveness 165 104 breast-feeding and positive physical contact, leading to attenuated [146]. Maintaining OT levels during sadness has also been associ- 166 105 endocrine responses to stress in women [3,38,66,70,72,103,146], ated with lower anxiety in close relationships [146]. Recently, Dit- 167 106 studies in humans have also been carried out with exogenous zen and colleagues [38] showed that women receiving 168 107 administration of OT and AVP. Intravenous OT infusion has been standardized physical contact from their partner (neck and shoul- 169 108 shown to induce significant behavioral effects [76,77], but it appears der massage) before stress exposure exhibited significantly lower 170 109 that only a small fraction of the neuropeptide passes the blood-brain cortisol and heart rate responses to stress compared with women 171 110 barrier [87], and possible side effects are more likely following intra- who received verbal social support or no social interaction from 172 111 venous infusion of neuropeptides. the partner. Another study by Holt-Lunstad and colleagues com- 173 112 Recent neuropharmacological research has shown that neuro- pared a warm touch intervention in couples with a monitoring- 174 113 peptides gain access to the human brain after intranasal adminis- only control groupPROOF[78]. Touch resulted in increased salivary OT 175 114 tration [18,41,66,129], providing a useful method for studying and a subsequent reduction in sympathetic tone indicated by low- 176 115 the central nervous effects of OT and AVP in humans [68]. In par- er systolic blood pressure as well as reduced alpha amylase. Alto- 177 116 ticular, a potential clinical use is dependent on a more direct and gether, these results from human studies suggest a possible 178 117 secure pathway to the human brain. In addition, a neurogenetic ap- protective effect of endogenous OT stimulation. 179 118 proach provides new insight into the individual variation of social Within this context, however, it should be noted that there are a 180 119 behavior and can easily be combined with behavioral measures variety of confounding factors, in particular the release of other 181 120 and functional imaging [92,113].
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