Double-blind disruption of right inferior frontal cortex with TMS reduces right frontal beta power for action stopping.

Stopping action depends on the integrity of the right inferior frontal gyrus (rIFG). Electrocorticography from the rIFG shows an increase in beta power during action stopping. Scalp EEG shows a similar right frontal beta increase, but it is unknown whether this beta modulation relates to the underlying rIFG network. Demonstrating a causal relationship between the rIFG and right frontal beta in EEG during action stopping is important for putting this electrophysiological marker on a firmer footing. In a double-blind study with a true sham coil, we used fMRI-guided 1-Hz repetitive transcranial magnetic stimulation (rTMS) to disrupt the rIFG and to test whether this reduced right frontal beta and impaired action stopping. We found that rTMS selectively slowed stop signal reaction time (SSRT) (no effect on Go) and reduced right frontal beta (no effect on sensorimotor mu/beta related to Go); it also reduced the variance of a single-trial muscle marker of stopping. Surprisingly, sham stimulation also slowed SSRTs and reduced beta. Part of this effect, however, resulted from carryover of real stimulation in participants who received real stimulation first. A post hoc between-group comparison of those participants who received real first compared with those who received sham first showed that real stimulation reduced beta significantly more. Thus, real rTMS uniquely affected metrics of stopping in the muscle and resulted in a stronger erosion of beta. We argue that this causal test validates right frontal beta as a functional marker of action stopping.NEW & NOTEWORTHY Action stopping recruits the right inferior frontal gyrus (rIFG) and elicits increases in right frontal beta. The present study now provides causal evidence linking these stopping-related beta oscillations to the integrity of the underlying rIFG network. One-hertz transcranial magnetic stimulation (TMS) over the rIFG impaired stopping and reduced right frontal beta during a stop-signal task. Furthermore, the effect on neural oscillations was specific to stopping-related beta, with no change in sensorimotor mu/beta corresponding to the Go response.

Temporally-precise disruption of prefrontal cortex informed by the timing of beta bursts impairs human action-stopping.

Human action-stopping is thought to rely on a prefronto-basal ganglia-thalamocortical network, with right inferior frontal cortex (rIFC) posited to play a critical role in the early stage of implementation. Here we sought causal evidence for this idea in experiments involving healthy human participants. We first show that action-stopping is preceded by bursts of electroencephalographic activity in the beta band over prefrontal electrodes, putatively rIFC, and that the timing of these bursts correlates with the latency of stopping at a single-trial level: earlier bursts are associated with faster stopping. From this we reasoned that the integrity of rIFC at the time of beta bursts might be critical to successful stopping. We then used fMRI-guided transcranial magnetic stimulation (TMS) to disrupt rIFC at the approximate time of beta bursting. Stimulation prolonged stopping latencies and, moreover, the prolongation was most pronounced in individuals for whom the pulse appeared closer to the presumed time of beta bursting. These results help validate a model of the neural architecture and temporal dynamics of action-stopping. They also highlight the usefulness of prefrontal beta bursts to index an apparently important sub-process of stopping, the timing of which might help explain within- and between-individual variation in impulse control.

The Functional Role of Response Suppression during an Urge to Relieve Pain.

Being in the state of having both a strong impulse to act and a simultaneous need to withhold is commonly described as an "urge." Although urges are part of everyday life and also important to several clinical disorders, the components of urge are poorly understood. It has been conjectured that withholding an action during urge involves active response suppression. We tested that idea by designing an urge paradigm that required participants to resist an impulse to press a button and gain relief from heat (one hand was poised to press while the other arm had heat stimulation). We first used paired-pulse TMS over motor cortex (M1) to measure corticospinal excitability of the hand that could press for relief, while participants withheld movement. We observed increased short-interval intracortical inhibition, an index of M1 GABAergic interneuron activity that was maintained across seconds and specific to the task-relevant finger. A second experiment replicated this. We next used EEG to better "image" putative cortical signatures of motor suppression and pain. We found increased sensorimotor beta contralateral to the task-relevant hand while participants withheld the movement during heat. We interpret this as further evidence of a motor suppressive process. Additionally, there was beta desynchronization contralateral to the arm with heat, which could reflect a pain signature. Strikingly, participants who "suppressed" more exhibited less of a putative "pain" response. We speculate that, during urge, a suppressive state may have functional relevance for both resisting a prohibited action and for mitigating discomfort.