The functional relevance of brain oscillations in the alpha frequency range (8–13 Hz) has been repeatedly investigated through the use of rhythmic visual stimulation. The underlying mechanism of the steady-state visual evoked potential (SSVEP) measured in EEG during rhythmic stimulation, however, is not known. There are two hypotheses on the origin of SSVEPs: entrainment of brain oscillations and superposition of event-related responses (ERPs). The entrainment but not the superposition hypothesis justifies rhythmic visual stimulation as a means to manipulate brain oscillations, because superposition assumes a linear summation of single responses, independent from ongoing brain oscillations. Here, we stimulated participants with a rhythmic flickering light of different frequencies and intensities. We measured entrainment by comparing the phase coupling of brain oscillations stimulated by rhythmic visual flicker with the oscillations induced by arrhythmic jittered stimulation, varying the time, stimulation frequency, and intensity conditions. In line with a theoretical concept of entrainment (the so called Arnold tongue), we found the phase coupling to be more pronounced with increasing stimulation intensity as well as at stimulation frequencies closer to each participant's intrinsic frequency. Only inside the Arnold tongue did the conditions significantly differ from the jittered stimulation. Furthermore, even in a single sequence of an SSVEP, we found non-linear features (intermittency of phase locking) that contradict the linear summation of single responses, as assumed by the superposition hypothesis. Our findings provide unequivocal evidence that visual rhythmic stimulation entrains brain oscillations, thus validating the approach of rhythmic stimulation as a manipulation of brain oscillations.

Previous studies have shown that alpha oscillations (8–13 Hz) in human electroencephalogram (EEG) modulate perception via phase-dependent inhibition. If entrained to an external driving force, inhibition maxima and minima of the oscillation appear more distinct in time and make potential phase-dependent perception predictable. There is an ongoing debate about whether visual stimulation is suitable to entrain alpha oscillations. On the one hand, it has been argued that a series of light flashes results in transient event-related responses (ERPs) superimposed on the ongoing EEG. On the other hand, it has been demonstrated that alpha oscillations become entrained to a series of light flashes if they are presented at a certain temporal regularity. This raises the question under which circumstances a sequence of light flashes causes entrainment, i.e., whether an arrhythmic stream of light flashes would also result in entrainment. Here, we measured detection rates in response to visual targets at two opposing stimulation phases during rhythmic and arrhythmic light stimulation. We introduce a new measure called “behavioral modulation depth” to determine differences in perception. This measure is capable of correcting for inevitable artifacts that occur in visual detection tasks during visual stimulation. The physical concept of entrainment predicts that increased stimulation intensity should produce stronger entrainment. Thus, two experiments with medium (Experiment 1) and high (Experiment 2) stimulation intensity were performed. Data from the first experiment show that the behavioral modulation depth (alpha phase-dependent differences in detection threshold) increases with increasing entrainment of alpha oscillations. Furthermore, individual alpha phase delays of entrained alpha oscillations determine the behavioral modulation depth: the largest behavioral modulation depth can be found if targets presented during the minimum of the entrained oscillation are compared to those presented during the maximum. In the second experiment stimulation with higher light intensity during both rhythmic and arrhythmic stimulation lead to an increased behavioral modulation depth, supposedly as a consequence of stronger entrainment during rhythmic stimulation. Altogether, our results reveal evidence for rhythmic and arrhythmic visual stimulation to induce fundamentally different processes in the brain: we suggest that rhythmic but not arrhythmic stimulation interacts with ongoing alpha oscillations via entrainment.

Transcranial alternating current stimulation has emerged as an effective tool for the exploration of brain oscillations. By applying a weak alternating current between electrodes placed on the scalp matched to the endogenous frequency, tACS enables the specific modulation of targeted brain oscillations This results in alterations in cognitive functions or persistent physiological changes. Most studies that utilize tACS determine a fixed stimulation frequency prior to the stimulation that is kept constant throughout the experiment. Yet it is known that brain rhythms can encounter shifts in their endogenous frequency. This could potentially move the ongoing brain oscillations into a frequency region where it is no longer affected by the stimulation, thereby decreasing or negating the effect of tACS. Such an effect of a mismatch between stimulation frequency and endogenous frequency on the outcome of stimulation has been shown before for the parietal alpha-activity. In this study, we employed an intermittent closed loop stimulation protocol, where the stimulation is divided into short epochs, between which an EEG is recorded and rapidly analyzed to determine a new stimulation frequency for the next stimulation epoch. This stimulation protocol was tested in a three-group study against a classical fixed stimulation protocol and a sham-treatment. We targeted the parietal alpha rhythm and hypothesized that this setup will ensure a constant close match between the frequencies of tACS and alpha activity. This closer match should lead to an increased modulation of detection of visual luminance changes depending on the phase of the tACS and an increased rise in alpha peak power post stimulation when compared to a protocol with fixed pre-determined stimulation frequency. Contrary to our hypothesis, our results show that only a fixed stimulation protocol leads to a persistent increase in post-stimulation alpha power as compared to sham. Furthermore, in none of the stimulated groups significant modulation of detection performance occurred. While the lack of behavioral effects is inconclusive due to the short selection of different phase bins and trials, the physiological results suggest that a constant stimulation with a fixed frequency is actually beneficial, when the goal is to produce persistent synaptic changes.

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