Relations between large scale brain connectivity and effects of regional stimulation depend on collective dynamical state

Abstract

At the macroscale, the brain operates as a network of interconnected neuronal populations, which display rhythmic dynamics that support interareal communication. Understanding how stimulation of a particular brain area impacts such concerted activity is important for gaining basic insights into brain function and for developing neuromodulation as a therapeutic tool. However, it remains difficult to predict the downstream effects of focal stimulation. Specifically, little is known about how the collective oscillatory regime of network activity may affect the outcomes of regional perturbations on cooperative dynamics. Here, we combine connectome data and biophysical modeling to begin filling these gaps. By tuning parameters that control the collective dynamics of the network, we identify distinct states of simulated brain activity, and investigate how the distributed effects of stimulation manifest in different states. When baseline oscillations are weak, the stimulated area exhibits enhanced power and frequency, and due to network interactions, nearby regions develop phase locked activity in the excited frequency band. Importantly, we find that focal stimulation also causes more distributed modifications to network coherence at regions' baseline oscillation frequencies, and that these effects are better predicted by functional rather than structural connectivity. In contrast, when the network operates in a regime of stronger endogenous oscillations, stimulation causes only slight shifts in power and frequency, and network averaged changes in coherence are more homogenous across the choice of the stimulated area. In sum, this work builds upon and extends previous computational studies investigating the impacts of stimulation, and highlights that both the stimulation site, and, crucially, the regime of brain network dynamics, can influence the network wide responses to local perturbations.