Rhythmic TMS Causes Local Entrainment of Natural Oscillatory Signatures

Background: Neuronal elements underlying perception, cognition, and action exhibit distinct oscillatory phenomena, measured in humans by electro- or magnetoencephalography (EEG/MEG). So far, the correlative or causal nature of the link between brain oscillations and functions has remained elusive. A compelling demonstration of causality would primarily generate oscillatory signatures that are known to correlate with particular cognitive functions and then assess the behavioral consequences. Here, we provide the first direct evidence for causal entrainment of brain oscillations by transcranial magnetic stimulation (TMS) using concurrent EEG. Results: We used rhythmic TMS bursts to directly interact with an MEG-identified parietal alpha-oscillator, activated by attention and linked to perception. With TMS bursts tuned to its preferred alpha-frequency (alpha-TMS), we confirmed the three main predictions of entrainment of a natural oscillator: (1) that alpha-oscillations are induced during alpha-TMS (reproducing an oscillatory signature of the stimulated parietal cortex), (2) that there is progressive enhancement of this alpha-activity (synchronizing the targeted, alpha-generator to the alpha-TMS train), and (3) that this depends on the pre-TMS phase of the background alpha-rhythm (entrainment of natural, ongoing alpha-oscillations). Control conditions testing different TMS burst profiles and TMS-EEG in a phantom head confirmed specificity of alpha-boosting to the case of synchronization between TMS train and neural oscillator. Conclusions: The periodic electromagnetic force that is generated during rhythmic TMS can cause local entrainment of natural brain oscillations, emulating oscillatory signatures activated by cognitive tasks. This reveals a new mechanism of online TMS action on brain activity and can account for frequency-specific behavioral TMS effects at the level of biologically relevant rhythms.