Oxytocin modulates human communication by enhancing cognitive exploration

Highlights

• Oxytocin is known to influence how humans share material resources.

• This study shows that oxytocin influences how humans share knowledge.

• Oxytocin drives individuals to generate signals that better disambiguate the many-to-many mappings between a signal’s form and meaning.

• Communicators receiving oxytocin more rapidly adjust their signals to what the addressee understands.

• Those effects suggest that oxytocin regulates exploration of cognitive models of the (social) environment.

Abstract

Oxytocin is a neuropeptide known to influence how humans share material resources. Here we explore whether oxytocin influences how we share knowledge. We focus on two distinguishing features of human communication, namely the ability to select communicative signals that disambiguate the many-to-many mappings that exist between a signal’s form and meaning, and adjustments of those signals to the presumed cognitive characteristics of the addressee (“audience design”). Fifty-five males participated in a randomized, double-blind, placebo controlled experiment involving the intranasal administration of oxytocin. The participants produced novel non-verbal communicative signals towards two different addressees, an adult or a child, in an experimentally-controlled live interactive setting. We found that oxytocin administration drives participants to generate signals of higher referential quality, i.e. signals that disambiguate more communicative problems; and to rapidly adjust those communicative signals to what the addressee understands. The combined effects of oxytocin on referential quality and audience design fit with the notion that oxytocin administration leads participants to explore more pervasively behaviors that can convey their intention, and diverse models of the addressees. These findings suggest that, besides affecting prosocial drive and salience of social cues, oxytocin influences how we share knowledge by promoting 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.