Two-brain states characterise within- and between-brain connectivity during intergenerational collaborative drawing

Abstract Engaging with others in social scenarios can result in the alignment of brain activity between individuals. Dyadic (i.e., hyperscanning) studies typically estimate average region-specific levels of connectivity between brains (as opposed to within brains) across a given task to quantify brain activity alignment. This approach assumes symmetric interactions with equal and mutual adaptation from both dyad members, excluding asymmetric (e.g., leader–follower) contexts. Such approaches also obscure spatial dynamics (i.e., relationship between different brain regions) and temporal dynamics during unfolding interactions. To overcome these challenges, we took a data-driven approach to quantify within- and between-brain connectivity during collaborative drawing among dyads. Specifically, we used sliding windows and Riemannian-geometry-based k -means clustering to identify recurrent two-brain states while 61 dyads drew alone and together at 6 weekly timepoints. Thirty dyads comprised young adults only (same generation) and 31 dyads comprised one older and one younger individual (intergenerational). We identified 7 two-brain states, 3 of which were specific to real (not pseudo) dyads. One two-brain state showed convincing evidence of sensitivity to collaboration context: During collaborative drawing, low-to-medium between-brain connectivity and prominent within-brain connectivity in bilateral IFG in a single dyad member arose for longer periods in intergenerational than same generation dyads (co-occurring with reduced turn-taking behaviour). No two-brain state showed evidence of longitudinal changes across sessions. These findings inform recent accounts of neural dynamics that emphasise the complementary roles of within-brain and between-brain connectivity. Furthermore, they suggest that state-based analyses can inform neural dynamics in a way not captured by traditional analysis techniques. Highlights Two-brain states can characterise within- and between-brain connectivity. Seven two-brain states identified using data-driven approach. Intergenerational collaborative drawing linked to asymmetric connectivity.