Connectome-Based Attractor Dynamics Guide Brain Activity in Rest, Task, and Disease

Abstract

Functional brain connectivity has been instrumental in uncovering the large-scale organization of the brain and its relation to various behavioral and clinical phenotypes. Understanding how this functional architecture relates to the brains dynamic activity repertoire is an essential next step towards interpretable generative models of brain function. We propose functional connectivity-based Attractor Neural Networks (fcANNs), a theoretically inspired model of macro-scale brain dynamics, simulating recurrent activity flow among brain regions based on first principles of self-organization. In the fcANN framework, brain dynamics are understood in relation to attractor states; neurobiologically meaningful activity configurations that minimize the free energy of the system. We provide the first evidence that large-scale brain attractors - as reconstructed by fcANNs - exhibit an approximately orthogonal organization, which is a signature of the self-orthogonalization mechanism of the underlying theoretical framework of free-energy-minimizing attractor networks. Analyses of 7 distinct datasets demonstrate that fcANNs can accurately reconstruct and predict brain dynamics under a wide range of conditions, including resting and task states, and brain disorders. By establishing a formal link between connectivity and activity, fcANNs offer a simple and interpretable computational alternative to conventional descriptive analyses. Key PointsO_LIWe present a simple yet powerful generative computational model for large-scale brain dynamics C_LIO_LIBased on the theory of artificial attractor neural networks emerging from first principles of self-organization C_LIO_LIModel dynamics accurately reconstruct several characteristics of resting-state brain dynamics and confirm theoretical predictions of emergent attractor self-orthogonalization C_LIO_LIOur model captures both task-induced and pathological changes in brain activity C_LIO_LIfcANNs offer a simple and interpretable computational alternative to conventional descriptive analyses of brain function C_LI Project website (with interactive manuscript)https://pni-lab.github.io/connattractor