Why we interact: On the functional role of the striatum in the subjective experience of social interaction

Abstract

There is ample evidence that human primates strive for social contact and experience interactions with conspecifics as intrinsically rewarding. Focusing on gaze behavior as a crucial means of human interaction, this study employed a unique combination of neuroimaging, eye-tracking, and computer-animated virtual agents to assess the neural mechanisms underlying this component of behavior. In the interaction task, participants believed that during each interaction the agent's gaze behavior could either be controlled by another participant or by a computer program. Their task was to indicate whether they experienced a given interaction as an interaction with another human participant or the computer program based on the agent's reaction. Unbeknownst to them, the agent was always controlled by a computer to enable a systematic manipulation of gaze reactions by varying the degree to which the agent engaged in joint attention. This allowed creating a tool to distinguish neural activity underlying the subjective experience of being engaged in social and non-social interaction. In contrast to previous research, this allows measuring neural activity while participants experience active engagement in real-time social interactions. Results demonstrate that gaze-based interactions with a perceived human partner are associated with activity in the ventral striatum, a core component of reward-related neurocircuitry. In contrast, interactions with a computer-driven agent activate attention networks. Comparisons of neural activity during interaction with behaviorally naïve and explicitly cooperative partners demonstrate different temporal dynamics of the reward system and indicate that the mere experience of engagement in social interaction is sufficient to recruit this system.

Turn-Taking in Human Communicative Interaction

“…Even unaddressed participants, who do not take a turn in the question-response sequences in our data, show evidence in their gaze behavior of a fine attunement to this feature of the turn-taking system 4 . Our findings that unaddressed participants' gaze behavior during question-response sequences appears to be organized according to a principle that optimizes recipiency also fits well with the notion of an 'intrinsic motivation for participation,' as it were Pfeiffer et al, 2014). Both Schilbach et al (2010) and Pfeiffer et al (2014) demonstrate that, in the context of gaze-based interactions, humans experience social-interactional engagement as rewarding, as evidenced by cerebral activity patterns in reward-related neurocircuitry.…”

Towards a second-person neuropsychiatry

“…In addition, different lines of research implicate dysfunction of striatal neurocircuitry in schizophrenia, which has been associated with impairments of wanting, liking and learning and could be particularly relevant for social interaction, as it has been shown that successful and enjoyable participation in social interaction significantly draws upon these neurocircuits [22,49]. Mesolimbic dopamine circuitry has been shown to play a role in so-called 'wanting' responses in animals and humans, i.e.…”

Perceived live interaction modulates the developing social brain

“…interaction may be intrinsically rewarding; Mundy and Neal, 2000;Schilbach et al, 2010;Pfeiffer et al, 2014), one component of successful social interaction is the creation of a shared psychological state between partners (Clark, 1996;Sperber and Wilson, 1996;Tomasello et al, 2005). Consistent with this perspective, recent behavioral (e.g.…”

“…Adult neuroimaging research has begun to identify the neural bases of social interaction (e.g. Redcay et al, 2010;Schilbach et al, 2010;Pö nk€ anen et al, 2011;Pfeiffer et al, 2014;Rice and Redcay, 2016), but few studies have investigated how the developing brain supports social interaction. Understanding the developmental bases of realworld social behaviors will provide insight into both typical and atypical social development, where disorders such as autism and social anxiety are characterized by interpersonal difficulties (e.g.…”