Dynamical models reveal anatomically reliable attractor landscapes embedded in resting state brain networks

Analyses of functional connectivity (FC) in resting-state brain networks (RSNs) have generated many insights into cognition. However, the mechanistic underpinnings of FC and RSNs are still not well-understood. It remains debated whether resting state activity is best characterized as noise-driven fluctuations around a single stable state, or instead, as a nonlinear dynamical system with nontrivial attractors embedded in the RSNs. Here, we provide evidence for the latter, by constructing whole-brain dynamical systems models from individual resting-state fMRI (rfMRI) recordings, using the Mesoscale Individualized NeuroDynamic (MINDy) platform. The MINDy models consist of hundreds of neural masses representing brain parcels, connected by fully trainable, individualized weights. We found that our models manifested a diverse taxonomy of nontrivial attractor landscapes including multiple equilibria and limit cycles. However, when projected into anatomical space, these attractors mapped onto a limited set of canonical RSNs, including the default mode network (DMN) and frontoparietal control network (FPN), which were reliable at the individual level. Further, by creating convex combinations of models, bifurcations were induced that recapitulated the full spectrum of dynamics found via fitting. These findings suggest that the resting brain traverses a diverse set of dynamics, which generates several distinct but anatomically overlapping attractor landscapes. Treating rfMRI as a unimodal stationary process (i.e., conventional FC) may miss critical attractor properties and structure within the resting brain. Instead, these may be better captured through neural dynamical modeling and analytic approaches. The results provide new insights into the generative mechanisms and intrinsic spatiotemporal organization of brain networks. Significance Statement Our brain remains active even when not engaged in cognitively demanding tasks. However, the processes that determine such ‘resting state’ activity are still not well-understood. Using a large (n > 1000) functional neuroimaging dataset and new techniques for computationally modeling brain activity, we found that the resting brain possesses several distinct mechanisms by which activity can be generated. These mechanisms, or dynamics, vary moment to moment, but result in the activation of similar anatomical regions across different individuals. Our results suggest that the resting brain is neither idle, nor monolithic in its governing mechanisms, but rather possesses a diverse but consistent taxonomy of ways in which it can activate and hence transition to cognitive tasks.