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Journal ArticleDOI

Oxytocin and vasopressin neural networks: Implications for social behavioral diversity and translational neuroscience

TL;DR: Both conserved and variable features of central oxytocin and vasopressin systems are described in the context of social behavioral diversity, with a particular focus on neural networks that modulate social learning, behavior, and salience of sociosensory stimuli during species‐typical social contexts.
About: This article is published in Neuroscience & Biobehavioral Reviews.The article was published on 2017-05-01 and is currently open access. It has received 206 citations till now. The article focuses on the topics: Oxytocin receptor & Social learning.
Citations
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Journal ArticleDOI
01 Apr 2018-Nature
TL;DR: Galanin-expressing neurons in the medial preoptic area of the hypothalamus coordinate different aspects of motor, motivational, hormonal and social behaviour associated with parenting by projecting to different brain regions depending on the type of behaviour and sex and reproductive state of mice.
Abstract: Parenting is essential for the survival and wellbeing of mammalian offspring. However, we lack a circuit-level understanding of how distinct components of this behaviour are coordinated. Here we investigate how galanin-expressing neurons in the medial preoptic area (MPOAGal) of the hypothalamus coordinate motor, motivational, hormonal and social aspects of parenting in mice. These neurons integrate inputs from a large number of brain areas and the activation of these inputs depends on the animal’s sex and reproductive state. Subsets of MPOAGal neurons form discrete pools that are defined by their projection sites. While the MPOAGal population is active during all episodes of parental behaviour, individual pools are tuned to characteristic aspects of parenting. Optogenetic manipulation of MPOAGal projections mirrors this specificity, affecting discrete parenting components. This functional organization, reminiscent of the control of motor sequences by pools of spinal cord neurons, provides a new model for how discrete elements of a social behaviour are generated at the circuit level.

263 citations

Journal ArticleDOI
TL;DR: How neural representations of a partner become inherently rewarding, providing intriguing insights into the neural origins of love is discussed, in this Review.
Abstract: Love is one of our most powerful emotions, inspiring some of the greatest art, literature and conquests of human history. Although aspects of love are surely unique to our species, human romantic relationships are displays of a mating system characterized by pair bonding, likely built on ancient foundational neural mechanisms governing individual recognition, social reward, territorial behaviour and maternal nurturing. Studies in monogamous prairie voles and mice have revealed precise neural mechanisms regulating processes essential for the pair bond. Here, we discuss current viewpoints on the biology underlying pair bond formation, its maintenance and associated behaviours from neural and evolutionary perspectives.

208 citations

Journal ArticleDOI
TL;DR: This study contributes a clear example of status-dependent AVT modulation of agonistic behavior in teleosts, and reveals distinctive activation patterns of the AVT system between dominants and subordinates.
Abstract: Dominant-subordinate status emerges from agonistic encounters. The weakly electric fish, Gymnotus omarorum, displays a clear-cut example of non-breeding territorial aggression. The asymmetry in the behavior of dominants and subordinates is outstanding. Dominants are highly aggressive and subordinates signal submission in a precise sequence of locomotor and electric traits: retreating, decreasing their electric organ discharge rate, and emitting transient electric signals. The hypothalamic neuropeptide arginine-vasotocin (AVT) and its mammalian homolog arginine-vasopressin, are key modulators of social behavior, known to adapt their actions to different contexts. By analyzing the effects of pharmacological manipulations of the AVT system in both dominants and subordinates, we show evidence of distinct status-dependent actions of AVT. We demonstrate an endogenous effect of AVT on dominants' aggression levels: blocking the V1a AVT receptor induced a significant decrease in dominants' attack rate. AVT administered to subordinates enhanced the expression of the electric signals of submission, without affecting subordinates' locomotor displays. This study contributes a clear example of status-dependent AVT modulation of agonistic behavior in teleosts, and reveals distinctive activation patterns of the AVT system between dominants and subordinates.

199 citations


Cites background from "Oxytocin and vasopressin neural net..."

  • ...AVT/AVP modulation of social behavior varies between species, sexes, physiological states, phenotypes, and social contexts (Insel and Young, 2000; Goodson et al., 2009; Godwin and Thompson, 2012; Caldwell, 2017; Johnson and Young, 2017)....

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Journal ArticleDOI
TL;DR: Current findings and theories that contribute to male preponderance of neurodevelopmental disorders, with a focus on autism are reviewed, and the possibilities of female underdiagnosis and a multi-hit hypothesis are discussed.
Abstract: Neurodevelopmental disorders disproportionately affect males. The mechanisms underlying male vulnerability or female protection are not known and remain understudied. Determining the processes involved is crucial to understanding the etiology and advancing treatment of neurodevelopmental disorders. Here, we review current findings and theories that contribute to male preponderance of neurodevelopmental disorders, with a focus on autism. Recent work on the biological basis of the male preponderance of autism and other neurodevelopmental disorders includes discussion of a higher genetic burden in females and sex-specific gene mutations or epigenetic changes that differentially confer risk to males or protection to females. Other mechanisms discussed are sex chromosome and sex hormone involvement. Specifically, fetal testosterone is involved in many aspects of development and may interact with neurotransmitter, neuropeptide, or immune pathways to contribute to male vulnerability. Finally, the possibilities of female underdiagnosis and a multi-hit hypothesis are discussed. This review highlights current theories of male bias in developmental disorders. Topics include environmental, genetic, and epigenetic mechanisms; theories of sex chromosomes, hormones, neuroendocrine, and immune function; underdiagnosis of females; and a multi-hit hypothesis.

189 citations

Journal ArticleDOI
TL;DR: The increasing body of evidence that exogenously administered and endogenously released OT and AVP can activate each other's canonical receptors is reviewed and the possibility that receptor cross-talk following the synaptic and non-synaptic release of OT andAVP contributes to their distinct roles in the brain and periphery is examined.

150 citations

References
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Journal ArticleDOI
TL;DR: The regulation by gonadal and adrenal steroids is one of the most remarkable features of the OT system and is, unfortunately, the least understood.
Abstract: The neurohypophysial peptide oxytocin (OT) and OT-like hormones facilitate reproduction in all vertebrates at several levels. The major site of OT gene expression is the magnocellular neurons of the hypothalamic paraventricular and supraoptic nuclei. In response to a variety of stimuli such as suckling, parturition, or certain kinds of stress, the processed OT peptide is released from the posterior pituitary into the systemic circulation. Such stimuli also lead to an intranuclear release of OT. Moreover, oxytocinergic neurons display widespread projections throughout the central nervous system. However, OT is also synthesized in peripheral tissues, e.g., uterus, placenta, amnion, corpus luteum, testis, and heart. The OT receptor is a typical class I G protein-coupled receptor that is primarily coupled via Gq proteins to phospholipase C-β. The high-affinity receptor state requires both Mg2+ and cholesterol, which probably function as allosteric modulators. The agonist-binding region of the receptor has bee...

2,691 citations

Journal ArticleDOI
TL;DR: It is concluded that social neuroscience paradigms provide reliable and accurate insights into complex social phenomena such as empathy and that meta-analyses of previous studies are a valuable tool in this endeavor.

1,604 citations


"Oxytocin and vasopressin neural net..." refers background in this paper

  • ...…and emotion recognition, aising the possibility of conserved neural mechanisms modulatng empathic behavior in rodents and humans (Burkett et al., 2016; obehavioral Reviews 76 (2017) 87–98 Domes et al., 2007; Hurlemann et al., 2010; Lamm et al., 2011; Laursen et al., 2014; Uzefovsky et al., 2015)....

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Journal ArticleDOI
TL;DR: Temporal patterns of anuran reproduction fall into two broad categories: prolonged breeding and explosive breeding, and many aspects of vocal behaviour and chorus organization can be viewed as consequences of intrasexual competition.

1,501 citations


"Oxytocin and vasopressin neural net..." refers background in this paper

  • ...Many frogs also rely on visual throat displays and posturing during dominance interactions (Wells, 1977), and OT/AVP-like receptors are densely expressed in visual processing nuclei (e.g. optic tectum) (Acharjee et al., 2004)....

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Journal ArticleDOI
TL;DR: It is shown that human amygdala function is strongly modulated by oxytocin, and this results indicate a neural mechanism for the effects of Oxytocin in social cognition in the human brain and provide a methodology and rationale for exploring therapeutic strategies in disorders in which abnormal amygdala function has been implicated, such as social phobia or autism.
Abstract: In non-human mammals, the neuropeptide oxytocin is a key mediator of complex emotional and social behaviors, including attachment, social recognition, and aggression. Oxytocin reduces anxiety and impacts on fear conditioning and extinction. Recently, oxytocin administration in humans was shown to increase trust, suggesting involvement of the amygdala, a central component of the neurocircuitry of fear and social cognition that has been linked to trust and highly expresses oxytocin receptors in many mammals. However, no human data on the effects of this peptide on brain function were available. Here, we show that human amygdala function is strongly modulated by oxytocin. We used functional magnetic resonance imaging to image amygdala activation by fear-inducing visual stimuli in 15 healthy males after double-blind crossover intranasal application of placebo or oxytocin. Compared with placebo, oxytocin potently reduced activation of the amygdala and reduced coupling of the amygdala to brainstem regions implicated in autonomic and behavioral manifestations of fear. Our results indicate a neural mechanism for the effects of oxytocin in social cognition in the human brain and provide a methodology and rationale for exploring therapeutic strategies in disorders in which abnormal amygdala function has been implicated, such as social phobia or autism.

1,477 citations


"Oxytocin and vasopressin neural net..." refers background in this paper

  • ...…were adapted from (Johnson ; NAcs = nucleus accumbens shell. istration modulates functional coupling between cortical, limbic, and/or striatal nuclei during processing of emotional facial expressions in both rhesus macaques and humans (Hu et al., 2015; Kirsch et al., 2005; Liu et al., 2015b)....

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  • ...istration modulates functional coupling between cortical, limbic, and/or striatal nuclei during processing of emotional facial expressions in both rhesus macaques and humans (Hu et al., 2015; Kirsch et al., 2005; Liu et al., 2015b)....

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Journal ArticleDOI
07 Nov 2008-Science
TL;DR: There is growing evidence that the neuropeptides oxytocin and vasopressin modulate complex social behavior and social cognition and suggest that variation in the genes encoding their receptors may contribute to variation in human social behavior by altering brain function.
Abstract: There is growing evidence that the neuropeptides oxytocin and vasopressin modulate complex social behavior and social cognition. These ancient neuropeptides display a marked conservation in gene structure and expression, yet diversity in the genetic regulation of their receptors seems to underlie natural variation in social behavior, both between and within species. Human studies are beginning to explore the roles of these neuropeptides in social cognition and behavior and suggest that variation in the genes encoding their receptors may contribute to variation in human social behavior by altering brain function. Understanding the neurobiology and neurogenetics of social cognition and behavior has important implications, both clinically and for society.

1,445 citations