State-dependent emergence of coupling between oscillatory and aperiodic neural activity

Neural oscillations and aperiodic activity are two quintessential mesoscopic-level features arising from shared circuits, yet what governs their relationship remains unclear. Here we show that coupling between oscillatory frequency and aperiodic exponent is sporadic and state-dependent. Bias-reduced analyses of 3,245 intracranial contacts from 61 awake subjects showed significant coupling in only <13% of contacts per band. A connectome-constrained dynamical model predicted that neither changes of input to local circuit nor removal of long-range connections modulated the coupling; whereas stronger local inhibitory feedback drove covariation between oscillatory frequency and aperiodic exponent. The model predictions were supported by three independent experiments: transcranial stimulation shifted each component independently and focal ablation of remote cortical tissues did not change coupling; whereas coupling emerged during seizures that altered local excitatory-inhibitory balance. These results suggest that the relation between periodic and aperiodic neural activity is neither intrinsically independent nor coupled, but determined by local circuit states.

Lu, Y., Li, Z., Mao, H., He, X., Liu, D., Chen, J., Tao, L., Xiao, Z.-C., Tian, X.

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