1/f electrophysiological spectra in resting and drug-induced states can be explained by the dynamics of multiple oscillatory relaxation processes

Neurophysiological recordings are dominated by arhythmical activity whose spectra can be characterised by power-law functions, and on this basis are often referred to as reflecting scale-free brain dynamics (1/f (beta)). Relatively little is known regarding the neural generators and temporal dynamics of this arhythmical behaviour compared to rhythmical behaviour. Here we used Irregularly Resampled AutoSpectral Analysis (IRASA) to quantify beta, in both the high (5-100 Hz, beta(hf)) and low frequency bands (0.1-2.5 Hz, beta(lf)) in MEG/EEG/ECoG recordings and to separate arhythmical from rhythmical modes of activity, such as, alpha rhythms. In MEG/EEG/ECoG data, we demonstrate that oscillatory alpha power dynamically correlates over time with beta(hf) and similarly, participants with higher rhythmical alpha power have higher beta(hf). In a series of pharmaco-MEG investigations using the GABA reuptake inhibitor tiagabine, the glutamatergic AMPA receptor antagonist perampanel, the NMDA receptor antagonist ketamine and the mixed partial serotonergic agonist LSD, a variety of effects on both beta(hf) and beta(lf) were observed. Additionally, strong modulations of beta(hf) were seen in monkey ECoG data during general anaesthesia using propofol and ketamine. We develop and test a unifying model which can explain, the 1/f nature of electrophysiological spectra, their dynamic interaction with oscillatory rhythms as well as the sensitivity of 1/f activity to drug interventions by considering electrophysiological spectra as being generated by a collection of stochastically perturbed damped oscillators having a distribution of relaxation rates.