Neural substrates of shared attention as social memory: A hyperscanning functional magnetic resonance imaging study

Abstract

During a dyadic social interaction, two individuals can share visual attention through gaze, directed to each other (mutual gaze) or to a third person or an object (joint attention). Shared attention is fundamental to dyadic face-to-face interaction, but how attention is shared, retained, and neutrally represented in a pair-specific manner has not been well studied. Here, we conducted a two-day hyperscanning functional magnetic resonance imaging study in which pairs of participants performed a real-time mutual gaze task followed by a joint attention task on the first day, and mutual gaze tasks several days later. The joint attention task enhanced eye-blink synchronization, which is believed to be a behavioral index of shared attention. When the same participant pairs underwent mutual gaze without joint attention on the second day, enhanced eye-blink synchronization persisted, and this was positively correlated with inter-individual neural synchronization within the right inferior frontal gyrus. Neural synchronization was also positively correlated with enhanced eye-blink synchronization during the previous joint attention task session. Consistent with the Hebbian association hypothesis, the right inferior frontal gyrus had been activated both by initiating and responding to joint attention. These results indicate that shared attention is represented and retained by pair-specific neural synchronization that cannot be reduced to the individual level.

Perceived live interaction modulates the developing social brain

“…Ultimately, however, it is possible that isolating the effect of social interaction will be difficult, as attentional or motivational processes may be inextricably linked to the emergent properties of real-world social interaction (e.g. see Koike et al, 2016 for evidence that social partners' eyeblinks become synchronized). This study was not well-suited to examine such emergent properties, as the analyzed portion of live speech did not involve a temporally unfolding interaction between actors.…”

“…Thus, unlike studies targeting the intersubject neural synchronization that emerges during interaction (e.g. Dumas et al, 2010;Stephens et al, 2010;Kawasaki et al, 2013;Koike et al, 2016), this paradigm was developed to specifically determine the effects of socialinteractive context on speech processing in a well-controlled design.…”

Development of social systems neuroscience using macaques

“…The ‘interactive brain hypothesis’ posits that social interaction engages neural processes that either do not occur or are less active during similar solo conditions. 158–160) Indeed, oscillatory coupling of neural signals between two brains has been reported during interactive tasks using fMRI, 161,162) functional near-infrared spectroscopy, 163–167) and electroencephalography 168) in humans. Although this technique, called hyperscanning, has not been applied to macaques, simultaneous recording of neural activities in two interacting subjects will provide important insights into the neural underpinnings of synchronous activity with precise spatiotemporal resolution.…”

Let's chat: developmental neural bases of social motivation during real‐time peer interaction

“…In such studies a participant responds to or directs another's gaze (e.g., Koike et al, 2016;Oberwelland et al, 2016;Schilbach et al, 2010). In such studies a participant responds to or directs another's gaze (e.g., Koike et al, 2016;Oberwelland et al, 2016;Schilbach et al, 2010).…”