Influence of ongoing alpha rhythm on the visual evoked potential
Introduction
The human electroencephalogram (EEG) is dominated by spontaneous rhythms, one of the most prominent being the alpha rhythm (8–12 Hz). Evoked potentials (EPs) being of small amplitudes are often obscured by such rhythms and can be revealed by averaging several epochs. This effect is reconcilable with linear summation of ongoing and evoked activity (Arieli et al., 1996), i.e. by an “evoked theory” or “additive theory” of EP generation. In this theory, ongoing activity, e.g. the alpha rhythm has no functional significance for EP generation. Another theory of EP generation is the “oscillatory theory” also known as “phase-reset theory”, assuming the EP to be generated by alpha rhythm phase resetting (Sayers et al., 1974, Makeig et al., 2002). Although both theories apparently differ in their assumed relationship between ongoing and evoked activity, there is controversy on how to validate the theories (Makeig et al., 2002, Makinen et al., 2005, Klimesch et al., 2006, Fuentemilla et al., 2006, Mazaheri and Jensen, 2006, Hanslmayr et al., 2006). Shah et al. (2004) suggested two criteria for differentiation: Sufficient ongoing alpha amplitude is required for EP generation in the oscillatory theory, while an event-related increase in signal power supports the evoked model. However, the conclusion, that in case of no increase or of a decrease in average post-stimulus alpha-band power the oscillatory model – i.e. an alpha rhythm phase reset – holds, may be premature. Such a situation can be caused either by veridical alpha phase resetting but also by a “masking” of an evoked process by a dominant but desynchronizing alpha rhythm (Hanslmayr et al., 2006). Without further positive evidence of a functional significance of the alpha rhythm for EP generation, the oscillatory theory can neither be discarded nor be proven. While several studies on the impact of the ongoing alpha amplitude on the evoked response have been reported (Makeig et al., 2002, Basar, 1980, Jasiukaitis and Hakerem, 1988, Rahn and Basar, 1993, Makinen et al., 2005), findings were contradictory or not related to model predictions and so far have not led to a general consensus on the mechanisms of EP generation.
In this study, we combine theoretical modeling and experimental data analysis to examine the functional role of the ongoing alpha rhythm for VEP generation.
In theoretical modeling, we evaluate the relationship between ongoing activity and evoked activity for both theories. Model-specific predictions are derived for varying pre-stimulus alpha amplitudes. Initially, both models contain a common subset of data, where an EP is accompanied by a dominating and desynchronizing alpha rhythm. We aim to demonstrate that by variation of pre-stimulus alpha amplitude both models are clearly differentiated with respect to their predictions. Subsequently, in experimental data the influence of pre-stimulus alpha amplitude on EP generation is investigated. Based on the comparison of these empirical findings and the simulated EP parameters, the influence of alpha rhythm on EP generation is defined in the light of the two opposing models.
Section snippets
Models
In order to model the evoked and the oscillatory theory of EP generation, we simulated EEG single trial activity composed of two types of subunit signals as detailed below and shown in Fig. 1. The evoked model assumes “dual generators” for alpha rhythm and EP generation whereas the oscillatory model assumes “shared generators” producing both the alpha rhythm and the evoked response (Mazaheri and Jensen, 2006). In a first step, a subset of data is generated for each model which assumes an EP
Results
In the following, we first show the results of our theoretical modeling approach, thereby demonstrating the usefulness of the proposed pre-stimulus alpha-variation for the differentiation of prevailing theories of EP generation. Secondly, we compare the outcome of the models with experimental data in order to identify the model that is more compatible with our experimental data.
Discussion
We have demonstrated that variation of the ongoing alpha amplitude allows differentiation of the two theories of EP generation, even when a subset of the data is ambiguous with respect to the two theories. Our experimental data show significant differences in EP parameters for varying pre-stimulus alpha amplitudes with early EP components being most consistent with the evoked theory, while later components co-vary with pre-stimulus but are not generated by post-stimulus alpha rhythm.
Acknowledgments
The authors thank Steven Lemm, Peter Brunecker, Robert Schmidt and Matthias Reinacher for helpful comments. This work was supported by the German Federal Ministry for Education and Research BMBF (Berlin NeuroImaging Center and Bernstein Center for Computational Neuroscience Berlin) and the German Research Foundation DFG (Berlin School of Mind and Brain).
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These authors contributed equally.