Contributions of action potentials to scalp EEG: Theory and biophysical simulations

Differences in the apparent 1/f component of neural power spectra require correction depending on the underlying neural mechanisms, which remain incompletely understood. Past studies suggest that neuronal spiking produces broadband signals and shapes the spectral trend of invasive macroscopic recordings, but it is unclear to what extent action potentials (APs) influence scalp EEG. Here, we combined biophysical simulations with statistical modelling to examine the amplitude and spectral content of scalp potentials generated by the electric fields from spiking activity. In physiological parameter regimes, we found that APs contribute negligibly to the EEG spectral trend. Consistent with this, comparing our biophysical simulations with previously published data from pharmacologically paralyzed subjects suggested that the EEG spectral trend can be explained by a combination of synaptic timescales and electromyogram contamination. We also modelled rhythmic EEG generation, finding that APs can generate detectable narrowband power between approximately 60 and 1000 Hz, reaching frequencies much faster than would be possible from synaptic currents. Finally, we show that different spectral detrending strategies are required for AP generated oscillations compared to synaptically generated oscillations, suggesting that existing detrending methods for EEG spectra need to be modified for high frequency signals.