A general theory of coherence between brain areas

What does neuronal coherence tell us about neuronal communication? Does coherence between field potentials (e.g. LFP, EEG, MEG) reflect spiking entrainment or coupling between oscillators? Is it a mechanism for communication between brain areas, or a byproduct of interareal connectivity? We hypothesized that interareal coherence is explained by the fact that outputs from one cortical area give rise to synaptic inputs in the same brain area, and correlated synaptic inputs in another area. Our mathematical analysis demonstrates that coherence between a sending and receiving area is precisely predicted from only two parameters: Interareal connectivity and oscillatory synchronization in the sending area. This model predicts narrow-band coherence even in case of a flat transfer function and in the absence of spiking entrainment in a downstream area, and reproduces frequency-specific Granger-causality patterns between brain areas (gamma feedforward, beta feedback). In general, we find that Granger-causality between field potentials is dominated by oscillatory synchronization in the sending area, whereas spiking entrainment is determined by the resonant properties of the receiver. Our model accurately reproduces LFP-LFP beta-coherence between macaque areas 7B and F5 in the absence of beta phase-locking within area F5. Together, these findings uncover a precise mechanistic model of interareal coherence as a (by)product of connectivity and power.