Repetitive transcranial magnetic stimulation affects behavior by biasing endogenous cortical oscillations

Abstract

A governing assumption about repetitive transcranial magnetic stimulation (rTMS) has been that it interferes with task-related neuronal activity – in effect, by “injecting noise” into the brain – and thereby disrupts behavior. Recent reports of rTMS-produced behavioral enhancement, however, call this assumption into question. We investigated the neurophysiological effects of rTMS delivered during the delay period of a visual working memory task by simultaneously recording brain activity with electroencephalography (EEG). Subjects performed visual working memory for locations or for shapes, and in half the trials a 10-Hz train of rTMS was delivered to the superior parietal lobule (SPL) or a control brain area. The wide range of individual differences in the effects of rTMS on task accuracy, from improvement to impairment, was predicted by individual differences in the effect of rTMS on power in the alpha-band of the EEG (∼10 Hz): a decrease in alpha-band power corresponded to improved performance, whereas an increase in alpha-band power corresponded to the opposite. The EEG effect was localized to cortical sources encompassing the frontal eye fields and the intraparietal sulcus, and was specific to task (location, but not object memory) and to rTMS target (SPL, not control area). Furthermore, for the same task condition, rTMS-induced changes in cross-frequency phase synchrony between alpha- and gamma-band (>40 Hz) oscillations predicted changes in behavior. These results suggest that alpha-band oscillations play an active role cognitive processes and do not simply reflect absence of processing. Furthermore, this study shows that the complex effects of rTMS on behavior can result from biasing endogenous patterns of network-level oscillations.

Event-related rTMS at encoding affects differently deep and shallow memory traces

“…In other words, disproportionately out-of-phase rTMS with respect to the intrinsic oscillatory brain activity seems a plausible mechanism to explain how online rTMS may inject neural noise -or random depolarization of neurons (Harris et al, 2008) in the cognitive process being undertaken, thereby temporarily disrupting task performance. Future combined TMS-EEG studies, which are disclosing complex effects of rTMS on endogenous patterns of network-level oscillations (Hamidi et al, 2009), are required to definitely test this hypothesis.…”

Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex enhances working memory

“…DLPFC may regulate the signal-tonoise ratio of the parietal cortex to enable increased storage capacity (Edin et al 2009). Prior electrophysiological studies have shown that high-frequency rTMS can entrain endogenous alpha frequency in the stimulated area, which then leads to suppression of distracters and thus enhancement of WM capacity (Sauseng et al 2009;Hamidi et al 2009;Thut and Miniussi 2009;Klimesch et al 2003). Other evidence points to the executive role of DLPFC in suppressing interfering task-irrelevant information (Sandrini et al 2008) and updating goal representations based on context information or task-related demands (Brunoni 2014;Barch et al 2003).…”

Dynamic network structure of interhemispheric coordination

“…We hypothesized that the transfer of visual word information, potentially modulated by effects of spatial attention, would occur primarily between posterior brain regions of extrastriate cortex. Given the novelty of our approach, we chose to limit our analysis to the α-band, where oscillatory activity has been shown to play a role in similar tasks (83)(84)(85)(86). We chose a commonly used α-frequency bandwidth (8-12 Hz), but we note that other studies suggest a functional distinction between the upper and lower α-bands (87).…”