Adaptive frequency-based modeling of whole-brain oscillations: Predicting regional vulnerability and hazardousness rates

Abstract

Whole-brain computational modeling based on structural connectivity has shown great promise in successfully simulating fMRI BOLD signals with temporal coactivation patterns that are highly similar to empirical functional connectivity patterns during resting state. Importantly, previous studies have shown that spontaneous fluctuations in coactivation patterns of distributed brain regions have an inherent dynamic nature with regard to the frequency spectrum of intrinsic brain oscillations. In this modeling study, we introduced frequency dynamics into a system of coupled oscillators, where each oscillator represents the local mean-field model of a brain region. We first showed that the collective behavior of interacting oscillators reproduces previously shown features of brain dynamics. Second, we examined the effect of simulated lesions in gray matter by applying an in silico perturbation protocol to the brain model. We present a new approach to map the effects of vulnerability in brain networks and introduce a measure of regional hazardousness based on mapping of the degree of divergence in a feature space.

Author Summary

Computational modeling of the brain enables us to test different hypotheses without any experimental complication, and it provides us with a platform for improving our understanding of different brain mechanisms. In this study, we proposed a new macroscopic computational model of the brain oscillations for resting-state fMRI. Optimizing model parameters using empirical data was performed based on several measures of functional connectivity and instantaneous coherence. We simulated the effect of malfunction in a brain region by changing that region’s dynamics to evoke noisy behavior. Together with presenting a new paradigm for local vulnerability mapping in the brain connectome, we evaluated the hazard rate induced after perturbing a brain region by measuring divergence of the perturbed model from the original model in feature space. The analysis of hazard rates induced by primary failures of individual brain regions provides relevant insights not only into the size of the damage inflicted on the connectome by a particular failure, but also into the potential origins of disease. Furthermore, we proposed a spatial brain map that is associated with the regional hazardousness rates, which is in good agreement with the known pathophysiologic roles of malfunction in different functional systems in the brain.