Attractor dynamics of a whole-cortex network model predicts emergence and structure of fMRI co-activation patterns in the mouse brain

Resting state fMRI signals in mammals exhibit rich dynamics on a fast, frame-by-frame timescale of seconds, including the robust emergence of recurring fMRI co-activation patterns (CAPs). To understand how such dynamics emerges from the underlying anatomical cortico-cortical connectivity, we developed a whole-cortex model of resting-state fMRI signals in the mouse. Our model implemented neural input-output nonlinearities and excitatory-inhibitory interactions within cortical regions, as well as directed anatomical connectivity between regions inferred from the Allen mouse brain atlas. We found that, even if the model parameters were fitted to explain static properties of fMRI signals on the timescale of minutes, the model generated rich frame-by-frame attractor dynamics, with multiple stationary and oscillatory attractors. Guided by these theoretical predictions, we found that empirical mouse fMRI time series exhibited analogous signatures of attractor dynamics, and that model attractors recapitulated the topographical organization of empirical fMRI CAPs. The model established key relationships between attractor dynamics, CAPs and features of the directed cortico-cortical intra- and inter-hemispheric anatomical connectivity. Specifically, we found that neglecting fiber directionality severely affected the number of model’s attractors and their ability to explain CAPs. Furthermore, modifying inter-hemispheric anatomical connectivity strength by decreasing or increasing it from the value of real mouse anatomical data, resulted in fewer attractors generated by cortico-cortical interactions and reduced non-homotopic features of the attractors generated by the model, which were important for better predicting empirical CAPs. These results offer novel theoretical insight into the dynamic organization of resting state fMRI in the mouse brain and suggest that the frame-wise BOLD activity captured by CAPs reflects an emerging property of cortical dynamics resulting from directed cortico-cortical interactions.