Review
Oxytocin, motivation and the role of dopamine

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Highlights

  • Recent evidence suggests oxytocin acts to increase the salience of social stimuli.

  • Oxytocin may affect social behaviors through its interaction with dopamine.

  • Potential for oxytocin to shift assessments of value and salience via dopamine

  • Interactions between oxytocin and dopamine will be reviewed.

Abstract

The hypothalamic neuropeptide oxytocin has drawn the attention of scientists for more than a century. The understanding of the function of oxytocin has expanded dramatically over the years from a simple peptide adept at inducing uterine contractions and milk ejection to a complex neuromodulator with a capacity to shape human social behavior. Decades of research have outlined oxytocin's ability to enhance intricate social activities ranging from pair bonding, sexual activity, affiliative preferences, and parental behaviors. The precise neural mechanisms underlying oxytocin's influence on such behaviors have just begun to be understood. Research suggests that oxytocin interacts closely with the neural pathways responsible for processing motivationally relevant stimuli. In particular, oxytocin appears to impact dopaminergic activity within the mesocorticolimbic dopamine system, which is crucial not only for reward and motivated behavior but also for the expression of affiliative behaviors. Though most of the work performed in this area has been done using animal models, several neuroimaging studies suggest similar relationships may be observed in humans. In order to introduce this topic further, this paper will review the recent evidence that oxytocin may exert some of its social–behavioral effects through its impact on motivational networks.

Introduction

This year marks the 60th anniversary since oxytocin was first synthesized and its structure established in the Nobel Prize winning work of Vincent du Vigneaud (du Vigneaud et al., 1953, du Vigneaud et al., 1954. Since that landmark work, scientists have grown to appreciate oxytocin both as a hormone contributing significantly to reproductive processes and as a complex neuromodulator capable of affecting a wide range of behaviors. While comprised of only nine amino acids, oxytocin is a highly influential neuropeptide known to significantly impact a variety of social and reproductive behaviors including pair bonding, as well as maternal, affiliative and sexual behaviors (see Burkett and Young, 2012, Campbell, 2010, Donaldson and Young, 2008, Lee et al., 2009, Meyer-Lindenberg et al., 2011).

While historically considered a prosocial hormone, research suggests oxytocin promotes both positive (i.e. maternal behaviors, pair-bonding, altruism, trust) and negative social interactions (i.e. aggression, territoriality) depending on the context. Experimental manipulations of oxytocin indicate this neuropeptide enhances the salience of social cues as evidenced by greater attention devoted toward inspecting social cues, heightened cognitive processing of social information, and increased effort devoted to engaging social entities. Oxytocin may also be involved in shifting attributions of motivational value or valence toward social stimuli, resulting in alternative appetitive and aversive value assignments to certain social objects. For instance, oxytocin appears to be responsible for the aversive to appetitive shift in the appraisal of newborn pups in female rats. How precisely oxytocinergic activity shapes such processes is still being explored; however, multiple intersecting lines of research have revealed oxytocinergic modulation of activity within motivational networks, particularly within dopaminergic mesocorticolimbic circuits, may be involved.

This review will discuss how oxytocin may facilitate social behavior by increasing the salience of social stimuli and by shifting valence assessments of social objects through its effects on motivational networks. First, major pathways responsible for processing motivationally relevant stimuli will be reviewed, placing special emphasis on the influence of oxytocin and dopamine within pathways. This will be followed by a description of how particular components of social motivation are impacted by oxytocinergic and dopaminergic activity. Finally, a brief comment will be given on oxytocin's potential role as a mediator of salience and valence attribution for objects imbued with social value.

Section snippets

Anatomy of motivation

Social interactions can be a source of joy or dread depending on the context. Key decisions must be made when encountering acquaintances and strangers; first, to determine whether they are friend or foe, then resolve whether any action is necessary and finally, if action is called for, settle on which action is appropriate (i.e. pursue, avoid, or attack). Such assessments are vital to survival and involve the engagement of motivational processes, which form an internal drive that pushes an

Role of dopamine in motivation

Dopamine was first implicated in “reward” processes in the 1950s in a series of experiments that explored electrical stimulation of the brain in rats. Olds and Milner noted that a rat that had been implanted with an electrode, within what was later identified to be the nucleus accumbens, preferentially spent time in the area where it had received electrical stimulation through the electrode the day prior (Olds and Milner, 1954). Further, when rats were trained to press a lever to electrically

Neurobiology of oxytocin

Oxytocin is a circular nonapeptide synthesized primarily within paraventricular nucleus (PVN) and the supraoptic nucleus (SON) of the hypothalamus. The posterior lobe of the pituitary contains axonal projections originating from the hypothalamus, which secrete oxytocin for release into circulation. Peripherally, oxytocin acts on reproductive physiologic processes to induce uterine contraction and stimulate milk ejection (Dale, 1906). Centrally, oxytocin neurons originating in the PVN also send

Oxytocin, dopamine and social salience

The location of oxytocin's receptors throughout the mesocorticolimbic dopamine system places oxytocin in an ideal position to influence a wide range of motivated behaviors. Several groups of researchers have posited that oxytocin's ability to influence behavioral responses to social stimuli is at least partially mediated by its capacity to increase the salience of social cues (Averbeck, 2010, Bartz et al., 2011, Burkett and Young, 2012, Gordon et al., 2011, Shamay-Tsoory et al., 2009). This

Final comment

Oxytocin clearly plays a central role in social behavior; however, researchers are still trying to grasp the main mechanism behind oxytocin's effects. First considered simply as a prosocial hormone, with recent data showing oxytocin can also increase elicited aggressive behaviors it now appears the effect of oxytocin is much more complex. Some have proposed oxytocin may act as a mediator of social salience, enhancing the processing of both positive and negative social stimuli thus promoting a

Acknowledgements

This review was supported by grant number UL1RR024986 from the National Center for Research Resources. The content is solely the responsibility of the authors and does not necessarily represent the official views of NCRR or the National Institutes of Health.

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