Abstract
Eye-to-eye contact is a spontaneous behavior between interacting partners that occurs naturally during social interactions. However, individuals differ with respect to eye gaze behaviors such as frequency of eye-to-eye contacts, and these variations may reflect underlying differences in social behavior in the population. While the use of eye signaling to indicate a shared object of attention in joint attention tasks has been well-studied, the effects of the natural variation in establishing eye contact during joint attention have not been isolated. Here, we investigate this question using a novel two-person joint attention task. Participants were not instructed regarding the use of eye contacts; thus all mutual eye contact events between interacting partners that occurred during the joint attention task were spontaneous and varied with respect to frequency. We predicted that joint attention systems would be modulated by differences in the social behavior across participant pairs, which could be measured by the frequency of eye contact behavior. We used functional near-infrared spectroscopy (fNIRS) hyperscanning and eye-tracking to measure the neural signals associated with joint attention in interacting dyads and to record the number of eye contact events between them. Participants engaged in a social joint attention task in which real partners used eye gaze to direct each other’s attention to specific targets. Findings were compared to a non-social joint attention task in which an LED cue directed both partners’ attention to the same target. The social joint attention condition showed greater activity in right temporoparietal junction than the non-social condition, replicating prior joint attention results. Eye-contact frequency modulated the joint attention activity, revealing bilateral activity in social and high level visual areas associated with partners who made more eye contact. Additionally, when the number of mutual eye contact events was used to classify each pair as either “high eye contact” or “low eye contact” dyads, cross-brain coherence analysis revealed greater coherence between high eye contact dyads than low eye contact dyads in these same areas. Together, findings suggest that variation in social behavior as measured by eye contact modulates activity in a subunit of the network associated with joint attention.
Highlights
Eye contact is one of the most basic and prevalent behaviors that can occur between two individuals
Most eye contact events occurred before joint attention to the target; for some dyads, some eye contact events occurred during the trial but after joint gaze on the target was achieved, resulting in greater than 18 events
The high eye contact dyads had an average of 17.1 eye contacts events, while the low eye contact dyads had an average of 4.8 eye contact events
Summary
Eye contact is one of the most basic and prevalent behaviors that can occur between two individuals. Based on the neural coupling hypothesis that cross-brain neural synchrony reflects shared information between dyads, we hypothesize that these differences are driven, not just by the interaction, but by the number of eye contact events during the joint attention task. Prior fMRI joint attention studies involve tasks in which subjects are explicitly asked to make direct gaze with a partner on a video screen prior to directing their attention In this way, joint attention has typically been thought of as an extension of eye contact-based communication between the initiator of joint attention and the responder. Our hypothesis was two-fold: first, that increased engagement in mutual eye contact would result in the modulation of social and highlevel visual areas distinct from the neural responses to the joint attention task itself; and second, that pairs who engaged in more mutual eye contact would show greater cross-brain coherence between these areas
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