Task-induced topological and geometrical changes in whole-brain dynamics predict cognitive individual differences

Across the last three decades, functional magnetic resonance imaging (fMRI) research - through both resting-state (rsfMRI) and task-based (tfMRI) studies - has greatly advanced our understanding regarding the neural basis of cognition. Yet the mechanistic relationship between rsfMRI and tfMRI is still poorly understood. In particular, it remains unclear how and why the brain activation patterns observed during the resting state are linked to cognitive functioning and individual differences present during task performance. Here, we test a unifying computational account which postulates that task contexts modulate the nonlinear attractor landscape and associated dynamical properties of the brain present under resting conditions, and further that the nature of this modulation is impacted by meaningful cognitive individual differences. To test this account, we develop a joint rsfMRI-tfMRI modeling and analysis framework called Mesoscale Individualized NeuroDynamics with eXogenous inputs (MINDy-X) and apply it to resting and N-back working memory task data from the Human Connectome Project. We first validated that the joint model can simulate and predict both rsfMRI and tfMRI data accurately, consistent with a common underlying dynamical system. Analyses of this joint model revealed that task-related modulation bifurcated the predominantly multistable attractor dynamics present during the resting state towards a predominantly monostable dynamics observed during N-back task states. This topological shift was also accompanied by a geometric reconfiguration, with the task state characterized by an enrichment of dynamical attractor "motifs" clustered around the frontoparietal (FPN) and default mode (DMN) networks. Task-related modulations of this attractor landscape were further subject to clear individual differences, such that individuals who did not exhibit a shift in attractor topology were more error-prone and less cautious in responding, while closer geometric proximity to the FPN and DMN motifs explained additional aspects of task performance. N-back behavior was best characterized by the combination of topological and geometric properties present in both task and rest states, suggesting that they each account for unique aspects of individual variability. The current work supports a novel computational framework for understanding the whole-brain neural activity patterns observed during rsfMRI and tfMRI as reflecting different states within a common non-linear dynamical system. This framework provides a new vocabulary for characterizing cognitive functioning in terms of the unique geometric and topological configuration of the associated attractor landscapes, with the potential for wide application in many domains of basic and clinical neuroscience research.