Attention Modulates TMS-Locked Alpha Oscillations in the Visual Cortex

Abstract

Cortical oscillations, such as 8–12 Hz alpha-band activity, are thought to subserve gating of information processing in the human brain. While most of the supporting evidence is correlational, causal evidence comes from attempts to externally drive (“entrain”) these oscillations by transcranial magnetic stimulation (TMS). Indeed, the frequency profile of TMS-evoked potentials (TEPs) closely resembles that of oscillations spontaneously emerging in the same brain region. However, it is unclear whether TMS-locked and spontaneous oscillations are produced by the same neuronal mechanisms. If so, they should react in a similar manner to top-down modulation by endogenous attention. To test this prediction, we assessed the alpha-like EEG response to TMS of the visual cortex during periods of high and low visual attention while participants attended to either the visual or auditory modality in a cross-modal attention task. We observed a TMS-locked local oscillatory alpha response lasting several cycles after TMS (but not after sham stimulation). Importantly, TMS-locked alpha power was suppressed during deployment of visual relative to auditory attention, mirroring spontaneous alpha amplitudes. In addition, the early N40 TEP component, located at the stimulation site, was amplified by visual attention. The extent of attentional modulation for both TMS-locked alpha power and N40 amplitude did depend, with opposite sign, on the individual ability to modulate spontaneous alpha power at the stimulation site. We therefore argue that TMS-locked and spontaneous oscillations are of common neurophysiological origin, whereas the N40 TEP component may serve as an index of current cortical excitability at the time of stimulation.

SIGNIFICANCE STATEMENT Rhythmic transcranial magnetic stimulation (TMS) is a promising tool to experimentally “entrain” cortical activity. If TMS-locked oscillatory responses actually recruit the same neuronal mechanisms as spontaneous cortical oscillations, they qualify as a valid tool to study the causal role of neuronal oscillations in cognition but also to enable new treatments targeting aberrant oscillatory activity in, for example, neurological conditions. Here, we provide first-time evidence that TMS-locked and spontaneous oscillations are indeed tightly related and are likely to rely on the same neuronal generators. In addition, we demonstrate that an early local component of the TMS-evoked potential (the N40) may serve as a new objective and noninvasive probe of visual cortex excitability, which so far was only accessible via subjective phosphene reports.