Ongoing oscillations and evoked responses are two main types of neuronal activity obtained with diverse electrophysiological recordings (EEG/MEG/iEEG/LFP). Although typically studied separately, they might in fact be closely related. One possibility to unite them is to demonstrate that neuronal oscillations have non-zero mean which predicts that stimulus- or task-triggered amplitude modulation of oscillations can contribute to the generation of evoked responses. We validated this mechanism using computational modelling and analysis of a large EEG data set. With a biophysical model, we indeed demonstrated that intracellular currents in the neuron are asymmetric and, consequently, the mean of alpha oscillations is non-zero. To understand the effect that neuronal currents exert on oscillatory mean, we varied several biophysical and morphological properties of neurons in the network, such as voltage-gated channel densities, length of dendrites, and intensity of incoming stimuli. For a very large range of model parameters, we observed evidence for non-zero mean of oscillations. Complimentary, we analysed empirical rest EEG recordings of 90 participants (50 young, 40 elderly) and, with spatio-spectral decomposition, detected at least one spatially-filtred oscillatory component of non-zero mean alpha oscillations in 93% of participants. In order to explain a complex relationship between the dynamics of amplitude-envelope and corresponding baseline shifts, we performed additional simulations with simple oscillators coupled with different time delays. We demonstrated that the extent of spatial synchronisation may obscure macroscopic estimation of alpha rhythm modulation while leaving baseline shifts unchanged. Overall, our results predict that amplitude modulation of neural oscillations should at least partially explain the generation of evoked responses. Therefore, inference about changes in evoked responses with respect to cognitive conditions, age or neuropathologies should be constructed while taking into account oscillatory neuronal dynamics.

Oscillations and evoked responses are two types of neuronal activity recorded non-invasively with EEG/MEG. Although typically studied separately, they might in fact represent the same process. One possibility to unite them is to demonstrate that neuronal oscillations have non-zero mean which would indicate that stimulus-relating amplitude modulation of neuronal oscillations should lead to the generation of evoked responses. We validated this mechanism using computational modelling and analysis of a large EEG data set. With a biophysical model generating alpha rhythm, we indeed demonstrated that the oscillatory mean is nonzero for a large range of model-parameter values. In EEG data we detected non-zero mean alpha oscillations in about 96% of the participants. Furthermore, using neuronal-ensemble modelling, we provided an explanation for the often observed discrepancies between amplitude modulation and baseline shifts. Overall, our results provide strong support for the unification of neuronal oscillations and evoked responses.

Evoked responses and ongoing oscillations represent two major electrophysiological phenomena in the human brain yet the link between them remains rather obscure. Here we show how these two types of brain activity can be mechanistically linked within the framework of the baseline-shift mechanism for the generation of evoked responses. We do so for the two most frequently studied EEG signals: the P300-evoked response and alpha oscillations (8-12 Hz). The baseline-shift mechanism states that oscillations may generate evoked responses if oscillations have a non-zero mean and their amplitude is modulated by the stimulus. Therefore, if the alpha amplitude modulation generates P300, the following predictions should hold: 1) the temporal evolution of P300 and alpha amplitude is similar, 2) spatial localisations of the P300 and alpha amplitude modulation overlap, 3) oscillations are non-zero mean with a sign of the mean being congruent to P300 polarity and direction of alpha amplitude change, 4) P300 and alpha amplitude modulation correlate with cognitive scores in a similar fashion. To fully and reliably validate these predictions, we analysed the data set of elderly participants (N=2230, 60-82 years old), using a) resting-state EEG recordings to compute the baseline-shift index (BSI) to quantify the mean of oscillations, b) the event-related data, to extract parameters of P300 and c) alpha rhythm amplitude envelope. The data was analysed both in sensor and source space. We showed that P300 is indeed linked to alpha amplitude modulation according to all four abovementioned predictions: 1) the time courses of P300 and alpha amplitude envelope correlate negatively; 2) both P300 and alpha rhythm spatially localised in the posterior region of the precuneus and posterior cingulate cortex; 3) the sign of the BSI at Pz electrode is predominantly negative, consistent with the positive polarity of P300 and decrease of alpha amplitude; moreover, a negative BSIs of higher magnitude corresponded to higher P300 amplitude; 4) attention, memory, and executive function scores have congruent correlations for P300 and alpha rhythm amplitude. Our results provide an unifying view on the interdependency of evoked responses and neuronal oscillations and suggest that P300, at least partly, is generated by the modulation of alpha oscillations. Therefore, changes in P300 related to different cognitive conditions, age, or neuropathologies should be interpreted by taking into account the spatio-temporal dynamics of neuronal oscillations.

Evoked responses and ongoing oscillations represent two major electrophysiological phenomena in the human brain yet the link between them remains rather obscure. Here we show how these two types of brain activity can be mechanistically linked within the framework of the baseline-shift mechanism for the generation of evoked responses. We do so for the two most frequently studied EEG signals: the P300-evoked response and alpha oscillations (8–12 Hz). The baseline-shift mechanism states that oscillations may generate evoked responses if oscillations have a non-zero mean and their amplitude is modulated by the stimulus. Therefore, if the alpha amplitude modulation generates P300, the following predictions should hold: 1) the temporal evolution of P300 and alpha amplitude is similar, 2) spatial localisations of the P300 and alpha amplitude modulation overlap, 3) oscillations are non-zero mean with a sign of the mean being congruent to P300 polarity and direction of alpha amplitude change, 4) P300 and alpha amplitude modulation correlate with cognitive scores in a similar fashion. To fully and reliably validate these predictions, we analysed the data set of elderly participants (N=2230, 60–82 years old), using a) resting-state EEG recordings to compute the baseline-shift index (BSI) to quantify the mean of oscillations, b) the event-related data, to extract parameters of P300 and c) alpha rhythm amplitude envelope. The data was analysed both in sensor and source space. We showed that P300 is indeed linked to alpha amplitude modulation according to all four abovementioned predictions: 1) the time courses of P300 and alpha amplitude envelope correlate negatively; 2) both P300 and alpha rhythm spatially localised in the posterior region of the precuneus and posterior cingulate cortex; 3) the sign of the BSI at Pz electrode is predominantly negative, consistent with the positive polarity of P300 and decrease of alpha amplitude; moreover, a negative BSIs of higher magnitude corresponded to higher P300 amplitude; 4) attention, memory, and executive function scores have congruent correlations for P300 and alpha rhythm amplitude. Our results provide an unifying view on the interdependency of evoked responses and neuronal oscillations and suggest that P300, at least partly, is generated by the modulation of alpha oscillations. Therefore, changes in P300 related to different cognitive conditions, age, or neuropathologies should be interpreted by taking into account the spatio-temporal dynamics of neuronal oscillations.