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.