Recovering Arrhythmic EEG Transients from Their Stochastic Interference

Abstract

Traditionally, the neuronal dynamics underlying electroencephalograms (EEG) have been understood as arising from \textit{rhythmic oscillators with varying degrees of synchronization}. This dominant metaphor employs frequency domain EEG analysis to identify the most prominent populations of neuronal current sources in terms of their frequency and spectral power. However, emerging perspectives on EEG highlight its arrhythmic nature, which is primarily inferred from broadband EEG properties like the ubiquitous $1/f$ spectrum. In the present study, we use an \textit{arrhythmic superposition of pulses} as a metaphor to explain the origin of EEG. This conceptualization has a fundamental problem because the interference produced by the superpositions of pulses generates colored Gaussian noise, masking the temporal profile of the generating pulse. We solved this problem by developing a mathematical method involving the derivative of the autocovariance function to recover excellent approximations of the underlying pulses, significantly extending the analysis of this type of stochastic processes. When the method is applied to spontaneous mouse EEG sampled at $5$ kHz during the sleep-wake cycle, specific patterns -- called $\Psi$-patterns -- characterizing NREM sleep, REM sleep, and wakefulness are revealed. $\Psi$-patterns can be understood theoretically as \textit{power density in the time domain} and correspond to combinations of generating pulses at different time scales. Remarkably, we report the first EEG wakefulness-specific feature, which corresponds to an ultra-fast ($\sim 1$ ms) transient component of the observed patterns. By shifting the paradigm of EEG genesis from oscillators to random pulse generators, our theoretical framework pushes the boundaries of traditional Fourier-based EEG analysis, paving the way for new insights into the arrhythmic components of neural dynamics.