Unexpected events induce motor slowing via a brain mechanism for action-stopping with global suppressive effects

Abstract

When an unexpected event occurs in everyday life (e.g., a car honking), one experiences a slowing down of ongoing action (e.g., of walking into the street). Motor slowing following unexpected events is a ubiquitous phenomenon, both in laboratory experiments as well as such everyday situations, yet the underlying mechanism is unknown. We hypothesized that unexpected events recruit the same inhibition network in the brain as does complete cancellation of an action (i.e., action-stopping). Using electroencephalography and independent component analysis in humans, we show that a brain signature of successful outright action-stopping also exhibits activity following unexpected events, and more so in blocks with greater motor slowing. Further, using transcranial magnetic stimulation to measure corticospinal excitability, we show that an unexpected event has a global motor suppressive effect, just like outright action-stopping. Thus, unexpected events recruit a common mechanism with outright action-stopping, moreover with global suppressive effects. These findings imply that we can now leverage the considerable extant knowledge of the neural architecture and functional properties of the stopping system to better understand the processing of unexpected events, including perhaps how they induce distraction via global suppression.

Figure 1.

Task schematics. A, Verbal reaction time task. B, SST. Note that on stop-trials, the letter turned red.

Figure 2.

Successful-stopping-related independent components; group average. A, Mean topographical distribution of IC weights. Since sign of the weight matrix is arbitrary, all weight matrices were flipped to show positive activity at electrode FCz. B, ERP projection at electrode FCz. C, Delta-band (0.5–4 Hz) power. D, Theta-band (4–8 Hz) power.

Figure 3.

Behavioral results from the novelty task. A, Experiment 1. B, Experiment 2 (EEG). Note that the sample size in Experiment 1 is significantly larger than the sample size of Experiment 2, which is why significant RT slowing in Experiment 2 is limited to the first block. Error bars denote SEM.

Figure 4.

Activity of successful-stopping-related independent components for the novelty task. A, Full frequency band ERSP. Colors indicate percentage change from baseline (warm colors, increase; cold colors, decrease). Black outlines denote significance at p < 0.05 (FDR corrected). B, ERP projection at electrode FCz. C, Delta-band (0.5–4 Hz) power. D, Theta-band (4–8 Hz) power. E, Alpha-band (8–12 Hz) power.

Figure 5.

Individual participants' activity of successful-stopping-related IC activity on the novelty task. IC topographies represent the topographical distribution of the IC weight maps (rectified to show positivity at electrode FCz). Wave boards show individual frequency band activity for novels and standard trials in the three frequency bands that showed significantly enlarged activity on novel trials on the group level. Shading represents SEM.

Figure 6.

Comparison of novel-related activity in the novelty task based on experimental block. First block showed significant behavioral slowing; last block did not. All parts show difference between novel and standard trials. A, Full frequency band ERSP. Colors indicate percentage change from baseline (warm colors, increase; cold colors, decrease). Black outlines denote significance at p < 0.05 (FDR corrected). B, ERP projection at electrode FCz. C, Delta-band (0.5–4 Hz) power.

Figure 7.

CSE as measured by the MEP (normalized by an ITI baseline) in the novelty task. Error bars denote SEM.