Assembling the Puzzle: Pathways of Oxytocin Signaling in the Brain

Grinevich, Valery; Knobloch‐Bollmann, H. Sophie; Eliava, Marina; Busnelli, Marta; Chini, Bice

doi:10.1016/j.biopsych.2015.04.013

Cited by 248 publications

(206 citation statements)

References 89 publications

(115 reference statements)

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“…The oxytocin (OT) system is well poised for investigating these links. OT is a highly conserved neuro-peptide that modulates reproductive physiology and behavior across bilaterian animals, including nematode worms, rodents, and humans (Garrison et al, 2012; Grinevich et al, 2016; Lee et al, 2009). In vertebrates, the OT system innervates forebrain networks that modulate social behavior.…”

Section: Introductionmentioning

confidence: 99%

Oxytocin receptors modulate a social salience neural network in male prairie voles

Johnson

Walum

Xiao

et al. 2017

Hormones and Behavior

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Social behavior is regulated by conserved neural networks across vertebrates. Variation in the organization of neuropeptide systems across these networks is thought to contribute to individual and species diversity in network function during social contexts. For example, oxytocin (OT) is an ancient neuropeptide that binds to OT receptors (OTRs) in the brain and modulates social and reproductive behavior across vertebrate species, including humans. Central OTRs exhibit extraordinarily diverse expression patterns that are associated with individual and species differences in social behavior. In voles, OTR density in the nucleus accumbens (NAc)—a region important for social and reward learning—is associated with individual and species variation in social attachment behavior. Here we test whether OTRs in the NAc modulate a social salience network (SSN)—a network of interconnected brain nuclei thought to encode valence and incentive salience of sociosensory cues—during a social context in the socially monogamous male prairie vole. Using a selective OTR antagonist, we test whether activation of OTRs in the NAc during sociosexual interaction and mating modulates expression of the immediate early gene product Fos across nuclei of the SSN. We show that blockade of endogenous OTR signaling in the NAc during sociosexual interaction and mating does not strongly modulate levels of Fos expression in individual nodes of the network, but strongly modulates patterns of correlated Fos expression between the NAc and other SSN nuclei.

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Section: Introductionmentioning

confidence: 99%

Oxytocin receptors modulate a social salience neural network in male prairie voles

Johnson

Walum

Xiao

et al. 2017

Hormones and Behavior

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“…Nevertheless, the large volume of data now existing on the effects of OT across species have informed conceptualizations on the role of OT in social behavior (53, 64, 84, 107, 134,187,218,239). Updated conceptualizations posit that OT mediates salience assignment and regulates attentional selection to social signals via interactions with the dopaminergic system (239).…”

Section: Discussionmentioning

confidence: 99%

“…Magnocellular neurons also innervate the spinal cord, midbrain, and multiple forebrain regions, such as the nucleus accumbens (NAcc) and central amygdala (156,231,257,262). Magnocellular neurons can release neuropeptides via axonal, somatic, and dendritic release, resulting in passive diffusion and potentially into the third ventricle (107, 217, 262, 300). Parvocellular OT and AVP neurons project onto magnocellular neurons within the PVN as well as to the spinal cord, brain stem, forebrain, and median eminence, where release influences anterior pituitary function (13,82,161,262).…”

Section: Neuropeptides Oxytocin and Vasopressinmentioning

confidence: 99%

Neuropeptide Regulation of Social Attachment: The Prairie Vole Model

Tabbaa

Paedae

Liu

et al. 2016

Comprehensive Physiology

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Social attachments are ubiquitous among humans and integral to human health. Although great efforts have been made to elucidate the neural underpinnings regulating social attachments, we still know relatively little about the neuronal and neurochemical regulation of social attachments. As a laboratory animal research model, the socially monogamous prairie vole (Microtus ochrogaster) displays behaviors paralleling human social attachments and thus has provided unique insights into the neural regulation of social behaviors. Research in prairie voles has particularly highlighted the significance of neuropeptidergic regulation of social behaviors, especially of the roles of oxytocin (OT) and vasopressin (AVP). This article aims to review these findings. We begin by discussing the role of the OT and AVP systems in regulating social behaviors relevant to social attachments, and thereafter restrict our discussion to studies in prairie voles. Specifically, we discuss the role of OT and AVP in adult mate attachments, biparental care, social isolation, and social buffering as informed by studies utilizing the prairie vole model. Not only do these studies offer insight into social attachments in humans, but they also point to dysregulated mechanisms in several mental disorders. We conclude by discussing these implications for human health.

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“…Knowledge of the sites of origin for neuropeptides, and particularly the location of targets for these signaling molecules, can provide initial insights into the role(s) of these signaling systems in modulating social behavior. A recent comparative review highlighted commonalities and differences in a broad taxonomic context (Grinevich et al, 2015). We focus here on contrasts between the two mammalian taxa for which substantial information is available (OT/AVP signaling in the primate versus rodent brain), and then characterize common and unique pathways NWM vs. Old World monkeys and humans.…”

Section: Central Distribution Of Neuropeptidergic Neurons and Recementioning

confidence: 99%

“…Further, OT has been shown to be critical in the formation and maintenance of mother-infant bonds in mammals (Rilling and Young, 2014), a social process that further enhances the likelihood of offspring survivorship and hence reproductive success. There is also a growing interest in OT and the related neurohypophyseal nonapetide arginine vasopressin (AVP) and their analogues in the regulation of social behavior beyond the maternal context, including social attachments among adults, social cognition, and aggression (Albers, 2015; Caldwell and Young III, 2006; Donaldson and Young, 2008; Goodson, 2008; Insel, 2010; Kelly and Goodson, 2014) and more complex human social traits, including social dysfunction (Feldman et al, 2016; Grinevich et al, 2015; LoParo and Waldman, 2014). …”

Section: Introductionmentioning

confidence: 99%

Neuropeptide diversity and the regulation of social behavior in New World primates

French

Taylor

Mustoe

et al. 2016

Frontiers in Neuroendocrinology

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Oxytocin (OT) and vasopressin (AVP) are important hypothalamic neuropeptides that regulate peripheral physiology, and have emerged as important modulators of brain function, particularly in the social realm. OT structure and the genes that ultimately determine structure are highly conserved among diverse eutherian mammals, but recent discoveries have identified surprising variability in OT and peptide structure in New World monkeys (NWM), with five new OT variants identified to date. This review explores these new findings in light of comparative OT/AVP ligand evolution, documents coevolutionary changes in the oxytocin and vasopressin receptors (OTR and V1aR), and highlights the distribution of neuropeptidergic neurons and receptors in the primate brain. Finally, the behavioral consequences of OT and AVP in regulating NWM sociality are summarized, demonstrating important neuromodulatory effects of these compounds and OT ligand-specific influences in certain social domains.

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Assembling the Puzzle: Pathways of Oxytocin Signaling in the Brain

Cited by 248 publications

References 89 publications

Oxytocin receptors modulate a social salience neural network in male prairie voles

Oxytocin receptors modulate a social salience neural network in male prairie voles

Neuropeptide Regulation of Social Attachment: The Prairie Vole Model

Neuropeptide diversity and the regulation of social behavior in New World primates

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