Brain-Environment Alignment during Movie Watching Predicts Cognitive-Affective Function in Adulthood

BOLD fMRI studies have provided compelling evidence that the human brain demonstrates substantial moment-to-moment fluctuations in both activity and functional connectivity patterns. While the role of brain signal variability in fostering cognitive adaptation to ongoing environmental demands is well-documented, the relevance of moment-to-moment changes in functional brain architecture is still debated. To probe the role of architectural variability in naturalistic information processing, we used neuroimaging and behavioural data collected during movie watching by the Cambridge Centre for Ageing and Neuroscience (N = 642, 326 women) and the Human Connectome Project (N = 176, 106 women). Both moment-to-moment and contextual change-evoked architectural variability increased from young to older adulthood. However, coupling between moment-to-moment changes in functional brain architecture and concrete environmental features was stronger at younger ages. Architectural variability (both momentary and context-evoked) was associated with age-distinct profiles of network communication, specifically, greater functional integration of the default mode network in older adulthood, but greater informational flow across neural networks implicated in environmentally driven attention and control (cingulo-opercular, salience, ventral attention) in younger adulthood. Whole-brain communication pathways anchored in default mode regions relevant to episodic and semantic context creation (i.e., angular and middle temporal gyri) contributed to greater brain reconfiguration in response to narrative context changes, as well as stronger coupling between moment-to-moment changes in functional brain architecture and changes in concrete environmental features. Cognitive adaptation was directly linked to levels of brain-environment alignment, but only indirectly associated with levels of architectural variability. Specifically, stronger coupling between moment-to-moment variability in brain architecture and concrete environmental features predicted poorer cognitive adaptation (i.e., fluid IQ) and greater affectively driven environmental vigilance. Complementarily, across the adult lifespan, higher fluid (but not crystallized) IQ was related to stronger expression of the network communication profile underlying momentary and context-based architectural variability during youth. Our results indicate that the adaptiveness of dynamic brain reconfiguration during naturalistic information processing changes across the lifespan due to the associated network communication profiles. Moreover, our findings on brain-environment alignment complement the existing literature on the beneficial consequences of modulating brain signal variability in response to environmental complexity. Specifically, they imply that coupling between moment-to-moment variability in functional brain architecture and concrete environmental features may index a bias towards perceptually-bound, rather than conceptual processing, which hinders affective functioning and strategic engagement with the external environment.