Oxytocin modulates human communication by enhancing cognitive exploration
Introduction
Oxytocin is a neuromodulatory hormone involved in controlling the physiology of reproductive behavior across several species. In social mammals, oxytocin is involved in social and affiliative behaviors, reducing social anxiety and increasing sensitivity to social cues. In humans, administration of this hormone influences a number of cognitive processes involving other agents, enhancing mental-states recognition and material resource-sharing with familiar partners (Declerck et al., 2010, Domes et al., 2007, Kosfield and Heinrich, 2005). Humans routinely share non-material resources such as knowledge, but in an evolutionarily unusual manner. This resource is not simply broadcasted, but shared by generating signals out of the manifold possibilities by which one can express meaning [“referential flexibility”; (Levinson, 2006, Tomasello et al., 2005)]. Those signals are also continuously adjusted to the presumed characteristics of an addressee [“audience design”; (Bell, 1984, Brand et al., 2002, Campisi and Ozyürek, 2013, Clark and Carlson, 1982, Clark and Murphy, 1982, Levinson, 2006, Newman-Norlund et al., 2009, Snow and Ferguson, 1977, Tomasello, 2008)]. These two distinctive features of human knowledge-sharing have been extensively described (Brennan et al., 2010, Clark, 1996, Galantucci and Garrod, 2011), but mechanistic insights on their neurobiological implementation are lacking. Given oxytocin’s ability to influence motivational and cognitive processes involving material resource sharing with other agents, here we explore whether and how this neuropeptide modulates those two distinctive features of human knowledge-sharing. We focus on the generation of signals with new meanings that minimize referential ambiguity, in order to capture “referential quality”, i.e. how well people solve the referential flexibility problem. We also focus on the adjustment of those signals to the presumed characteristics of an addressee, in order to capture audience design.
We consider three non-mutually exclusive possibilities grounded on different models of oxytocin function. Those predictions are tested by quantifying the production of novel communicative behaviors during live interactions with an adult and a child addressee. First, if oxytocin operates by unconditionally enhancing prosociality (Kosfield and Heinrich, 2005, Zak et al., 2007), then oxytocin administration should have a directional effect on audience design, i.e. enhancing the spontaneous adjustments that adult communicators produce when directing their speech, gestures, and accompanying motions towards child addressees (Brand et al., 2002; rek, 2013; Newman-Norlund et al., 2009,b; Stolk et al., 2013a, Stolk et al., 2013b). Second, if oxytocin increases sensitivity to social cues (Bartz et al., 2011, Shamay-Tsoory and Abu-Akel, 2016), then oxytocin administration should have a different effect on audience design, i.e. leading interlocutors to make their communicative behavior as emphatic and precise as required by the cues reflecting the level of comprehension of the addressee (Grice, 1969, Newman-Norlund et al., 2009). Third, if the social anxiolytic effects of oxytocin promote social exploration (Bale et al., 2001, Chang and Platt, 2014, Ring et al., 2006, Windle et al., 1997), then oxytocin administration should influence both referential quality and audience design. Namely, oxytocin could drive interlocutors to explore more pervasively possible behaviors for conveying their intention (De Dreu et al., 2013, Hare et al., 2007), leading them to generate signals that solve a larger portion of a communicative challenge. By the same token, oxytocin could also drive interlocutors to explore diverse models of the addressees, leading to rapid communicative adjustments to the level of comprehension of the addressee.
Section snippets
Participants
Fifty-eight right-handed healthy males (mean age = 22, SD = 3 years) participated in this study. A power analysis (power = 80%) based on the medium-large effect size (d = 0.5 and d = 0.7) of previous studies assessing the effects of oxytocin intervention on human social behavior (Kosfield and Heinrich, 2005, Zak et al., 2007) indicated that a sample size between N = 26 and N = 49 would be adequate to assess the presence of an effect of oxytocin. Although those studies were not addressing exactly the same
Results
The first finding of this study pertains to oxytocin-related variations in the referential quality of the communicative behaviors generated by the participants (Fig. 3B; for statistics see Table S3A).
Communicators in the Oxytocin and Placebo group composed communicative signals with different referential quality (main effect of DRUG: F(4,50) = 3.88, p = 0.008, η2 = 0.237) while producing communicative signals of comparable referential quality for the two presumed Addressees (main effect of ADDRESSEE:
Discussion
This study tests if and how oxytocin influences two distinctive features of human knowledge-sharing, the generation of novel signals able to disambiguate the many-to-many mappings that exist between a signal’s form and meaning, and their adjustment to the presumed characteristics of an addressee (capturing “audience design”). The effects of oxytocin on those features have been quantified with an open-ended communication game, using nonverbal signals, over multiple live interactions with human
Conclusion
This study provides evidence that oxytocin alters two distinguishing features of human knowledge sharing during live communicative interactions: namely the ability to provide solutions to the many-to-many mappings that exist between a signal’s form and meaning (“referential quality”), and adjustments of those signals to the presumed cognitive characteristics of the addressee (“audience design”). Oxytocin enhances participants’ ability to pro-actively consider possible communicative problems
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Funding and disclosure
This study was supported by a VICI grant (grant number 453-08-002) from the Netherlands Organisation for Scientific Research to IT, by a PhD grant from Donders Centre for Cognition at the Radboud University to IvR, IT and Pim Haselager, and by the Cluster of Excellence Cognitive Interaction Technology “CITEC” (EXC 277) at Bielefeld University, which is funded by the German Research Foundation (DFG). The funders had no role in study design, data collection and analysis, decision to publish, or
Acknowledgements
We thank José Kivits for assistance with data collection and EgbeRt HaRtstRa for his valuable feedback on R analysis.
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