When reality and beliefs differ: oxytocin biases communicative choices towards reality

Human referential communication is often adjusted to the presumed knowledge and characteristics of addressees (“audience design”; Clark, 1996). For instance, utterances directed towards children show systematic verbal and gestural adjustments (Snow and Ferguson, 1977; Campisi and Ozyurek, 2013). However, it remains unclear which neurobiological mechanisms drive communicators to implement those adjustments, and alter them on the basis of the ongoing communicative behaviour. Here we explore whether oxytocin, a neuropeptide known to promote prosocial behaviours and to sharpen processing of socially-relevant information (Bartz et al., 2011), biases communicative adjustments towards prosocial beliefs or towards the information acquired during an interaction. Fifty-eight healthy male adults participated in a randomized, double-blind, placebo controlled experiment involving the intranasal administration of oxytocin (24 IU). Participants communicated to an addressee the location of a token in a 3x3 grid (visible only to the communicator) by means of their movements on the grid (visible to both communicator and addressee). Participants spontaneously marked the token’s position by waiting longer on that location as compared to other locations visited during their movements on the grid (“TimeOnTarget” effect). Crucially, participants were made to believe that they interacted with a child and with another adult, in alternation. In fact, an adult confederate performed the role of both addressees, while remaining blind to which one of the two roles she was performing in any given trial. Accordingly, both performance and response times of the two presumed addressees were matched. This feature of this previously validated protocol (Newman-Norlund et al., 2009; Stolk et al., 2013) allowed us to test how oxytocin modulates communicative adjustments driven by the mere belief of interacting with addressees with different abilities, while matching their behaviour. If oxytocin up-regulates prosocial behaviours, then intranasal oxytocin should enhance belief-driven communicative adjustments, increasing audience design effects when compared to placebo administration. Alternatively, if oxytocin sharpens the perception and saliency of social information, then intranasal oxytocin should enhance behaviour-related communicative adjustments, reducing audience design effects when compared to placebo administration. Participants believed they interacted with different addressees, attributing to them different age and cognitive abilities. Communication was effective (69% correct, chance-level: 6.6%), with participants spending longer time on the field containing the target. Participants receiving placebo showed a larger TimeOnTarget effect when they thought they were communicating with a child. Crucially, participants receiving oxytocin did not show a differential TimeOnTarget effect between the two addressees. Further exploration of the temporal dynamics of this between-group difference in communicative adjustments revealed that, at the onset of the communicative game, participants receiving oxytocin had a longer TimeOnTarget when addressing a presumed child. This effect disappeared over the course of the experiment. Participants that received placebo showed the opposite pattern. These findings shed light on a neurobiological mechanism that modulates the balance between two elements of audience design: belief-driven and behaviour-driven adjustments. Oxytocin drives interlocutors to adjust their communicative utterances towards the actual behaviour experienced in addressees, and away from their beliefs on the abilities of those addressees