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Oxytocin shapes the priorities and neural representations of attitudes and values

Published online by Cambridge University Press:  30 October 2017

René Hurlemann
Affiliation:
Department of Psychiatry, University of Bonn, 53105 Bonn, Germany. renehurlemann@icloud.comhttp://renehurlemann.squarespace.com/welcome/ Division of Medical Psychology, University of Bonn, 53105 Bonn, Germany. n.marsh@gmx.dejohannes.schultz@gmail.comdirk-scheele@gmx.dehttps://sites.google.com/site/johannesschultz/http://psychiatrie.uni-bonn.de/
Nina Marsh
Affiliation:
Division of Medical Psychology, University of Bonn, 53105 Bonn, Germany. n.marsh@gmx.dejohannes.schultz@gmail.comdirk-scheele@gmx.dehttps://sites.google.com/site/johannesschultz/http://psychiatrie.uni-bonn.de/
Johannes Schultz
Affiliation:
Division of Medical Psychology, University of Bonn, 53105 Bonn, Germany. n.marsh@gmx.dejohannes.schultz@gmail.comdirk-scheele@gmx.dehttps://sites.google.com/site/johannesschultz/http://psychiatrie.uni-bonn.de/
Dirk Scheele
Affiliation:
Division of Medical Psychology, University of Bonn, 53105 Bonn, Germany. n.marsh@gmx.dejohannes.schultz@gmail.comdirk-scheele@gmx.dehttps://sites.google.com/site/johannesschultz/http://psychiatrie.uni-bonn.de/

Abstract

The phylogenetically ancient neuropeptide oxytocin has been linked to a plethora of social behaviors. Here, we argue that the action of oxytocin is not restricted to the downstream level of emotional responses, but substantially alters higher representations of attitudes and values by exerting a distant modulatory influence on cortical areas and their reciprocal interplay with subcortical regions and hormonal systems.

Type
Open Peer Commentary
Copyright
Copyright © Cambridge University Press 2017 

In their superb Attitude–Scenario–Emotion (ASE) model, Gervais & Fessler (G&F) propose that distinct sentiments such as contempt or love result from enduring attitudes which moderate discrete emotional outcomes across various scenarios in a top-down–like manner. When reflecting on the role of neuroendocrine systems in the light of the ASE model, the authors suggest that the canonical “functions of the [neuropeptide] oxytocin are not the attitudinal encoding of social value itself, but are specifically emotion-like” (sect. 6.2, para. 8), thus enabling different behavioral outcomes depending on superordinate a priori attitudes.

The past decade has witnessed a tremendous surge of interest in the modulatory effects of oxytocin (OXT) on social-cognitive and behavioral readouts in humans. These studies are feasible because intranasal delivery of synthetic OXT allows modeling of transient states of heightened brain OXT concentrations (Striepens et al. Reference Striepens, Kendrick, Hanking, Landgraf, Wüllner, Maier and Hurlemann2013). Converging evidence now suggests that the influence of OXT varies as a function of context and interpersonal variables (Olff et al. Reference Olff, Frijling, Kubzansky, Bradley, Ellenbogen, Cardoso, Bartz, Yee and van Zuiden2013). As such, OXT effects can be dependent upon the time point of administration (Eckstein et al. Reference Eckstein, Becker, Scheele, Scholz, Preckel, Schlaepfer, Grinevich, Kendrick, Maier and Hurlemann2015; Reference Eckstein, Scheele, Patin, Preckel, Becker, Walther, Domschke, Grinevich, Maier and Hurlemann2016), the presence of social cues (Scheele et al. Reference Scheele, Schwering, Elison, Spunt, Maier and Hurlemann2015), social provenience and parochialism (De Dreu et al. Reference De Dreu, Greer, Handgraaf, Shalvi, Van Kleef, Baas, Ten Velden, Van Dijk and Feith2010; Reference De Dreu, Greer, Van Kleef, Shalvi and Handgraaf2011), or neurodevelopmental characteristics (Scheele et al. Reference Scheele, Kendrick, Khouri, Kretzer, Schlapfer, Stoffel-Wagner, Gunturkun, Maier and Hurlemann2014a). However, G&F's interpretation that the peptide produces exclusively emotion-like effects has several shortcomings. For instance, it cannot account for the finding that exogenous OXT evokes differential effects in women and men (Scheele et al. Reference Scheele, Striepens, Kendrick, Schwering, Noelle, Wille, Schlapfer, Maier and Hurlemann2014b) and young and elderly participants (Ebner et al. Reference Ebner, Horta, Lin, Feifel, Fischer and Cohen2015), despite the absence of a priori group differences in the placebo condition. Moreover, the authors' interpretation does not fully account for OXT causing an enhancement of emotional empathy to the pain of an adversary outgroup (Shamay-Tsoory et al. Reference Shamay-Tsoory, Abu-Akel, Palgi, Sulieman, Fischer-Shofty, Levkovitz and Decety2013) and a newly induced social altruism bias at the cost of ecological responsibility (Marsh et al. Reference Marsh, Scheele, Gerhardt, Strang, Enax, Weber, Maier and Hurlemann2015), both of which rather suggest that the peptide can weaken or reverse a priori attitudinal representations and resultant behavioral priorities. Administration of OXT may even modify complex psychological constructs such as self-concept, for instance, by increasing the subjective experience of attachment security in insecurely attached adults (Buchheim et al. Reference Buchheim, Heinrichs, George, Pokorny, Koops, Henningsen, O'Connor and Gundel2009) or by eliciting stronger positive attitudes toward oneself (Colonnello & Heinrichs Reference Colonnello and Heinrichs2014). OXT also influences self-perception of extraversion and openness to new experiences, in the absence of mediation by stress or negative affect (Cardoso et al. Reference Cardoso, Ellenbogen and Linnen2012).

Further support for the notion that the effects of OXT are not restricted to downstream emotional responses, but in fact shape attitudes and values, comes from clinical studies documenting the peptide's therapeutic potential to improve social functioning in individuals with autism (Yatawara et al. Reference Yatawara, Einfeld, Hickie, Davenport and Guastella2016) and schizophrenia (Davis et al. Reference Davis, Green, Lee, Horan, Senturk, Clarke and Marder2014). In these studies, improvements were observed far beyond the emotional level, namely, in social awareness, capacity for reciprocal social communication, and empathic accuracy. Dysfunctional cognitive schemata can be influenced as well: OXT as an adjunct to exposure therapy for social anxiety disorder has been found to mitigate the exaggerated negative beliefs about oneself which are typical for patients with social anxiety (Guastella et al. Reference Guastella, Howard, Dadds, Mitchell and Carson2009).

In addition, G&F propose to reconceptualize psychopathy as a sentiment disorder in which an inability to value others disrupts downstream social emotions including empathy. Concordant with this view is neuroimaging evidence that spontaneous empathy is reduced in psychopathy, whereas deliberate empathy is not (Meffert et al. Reference Meffert, Gazzola, den Boer, Bartels and Keysers2013). OXT has a key role in empathy (Domes et al. Reference Domes, Heinrichs, Michel, Berger and Herpertz2007; Hurlemann et al. Reference Hurlemann, Patin, Onur, Cohen, Baumgartner, Metzler, Dziobek, Gallinat, Wagner, Maier and Kendrick2010), and evidence suggests abnormalities of the OXT system in psychopathy and related callous-unemotional traits: For example, lower peripheral OXT concentrations are associated with stronger callous-unemotional traits (Levy et al. Reference Levy, Bloch, Bar-Maisels, Gat-Yablonski, Djalovski, Borodkin and Apter2015). Notably, a recent longitudinal epigenetic study detected a positive link between methylation of the OXT receptor gene at birth and callous-unemotional traits at age 13, which corroborates the hypothesis of abnormalities in the oxytocin system as a core element of developmental pathways to callous-unemotional traits (Cecil et al. Reference Cecil, Lysenko, Jaffee, Pingault, Smith, Relton, Woodward, McArdle, Mill and Barker2014). These findings, together with the relationship between variations in common polymorphisms of the OXT receptor gene and antisocial behavior (Hovey et al. Reference Hovey, Lindstedt, Zettergren, Jonsson, Johansson, Melke, Kerekes, Anckarsater, Lichtenstein, Lundstrom and Westberg2016), and high callous-unemotional traits (Beitchman et al. Reference Beitchman, Zai, Muir, Berall, Nowrouzi, Choi and Kennedy2012; Dadds et al. Reference Dadds, Moul, Cauchi, Dobson-Stone, Hawes, Brennan, Urwin and Ebstein2014), all point to an involvement of the OXT system in upstream attitudinal representations.

On the neural level, exogenously administered OXT affects activity not only in key components of the salience network including the amygdala (Eckstein et al. Reference Eckstein, Becker, Scheele, Scholz, Preckel, Schlaepfer, Grinevich, Kendrick, Maier and Hurlemann2015), insula (Striepens et al. Reference Striepens, Scheele, Kendrick, Becker, Schafer, Schwalba, Reul, Maier and Hurlemann2012), and anterior cingulate cortex (Preckel et al. Reference Preckel, Scheele, Eckstein, Maier and Hurlemann2015), but also in the precuneus (Scheele et al. Reference Scheele, Striepens, Kendrick, Schwering, Noelle, Wille, Schlapfer, Maier and Hurlemann2014b), which is consistent with current concepts that the peptide's effects are not limited to the modulation of arousal responses orchestrated by evolutionary ancient areas. OXT also influences, and interacts with, representations of attitudes and values in more recently developed cortical regions (Hurlemann & Scheele Reference Hurlemann and Scheele2016). Furthermore, the modulatory effects of OXT on reward-associated responses in the ventral tegmental area (VTA) or nucleus accumbens are critically influenced by gonadal hormones (Scheele et al. Reference Scheele, Wille, Kendrick, Stoffel-Wagner, Becker, Güntürkün, Maier and Hurlemann2013; Reference Scheele, Plota, Stoffel-Wagner, Maier and Hurlemann2016), suggesting that at least some representations of value are susceptible to hormonal signals and their interactions, especially in the sexual domain (Hurlemann & Scheele Reference Hurlemann and Scheele2016). Specifically, it has been proposed that OXT attaches salience to socially relevant cues by modulating activity in the VTA (Gregory et al. Reference Gregory, Cheng, Rupp, Sengelaub and Heiman2015; Groppe et al. Reference Groppe, Gossen, Rademacher, Hahn, Westphal, Grunder and Spreckelmeyer2013). While it would seem simplistic to reduce relational values to a single peripheral OXT concentration, these findings are consistent with the idea that OXT contributes to the representation of sentiments not only at the behavioral and emotional level, but also at the level of relationship values and attitudes.

Taken together, the effect profile of OXT is not confined to the peptide's modulatory role in proximate emotional responding. In fact, to understand how OXT influences human social behavior, we need to consider the close cross-talk between OXT and other hormonal systems through which sentiments such as contempt may be shaped at various levels.

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