Common neural processes during action-stopping and infrequent stimulus detection: The frontocentral P3 as an index of generic motor inhibition

Abstract

The stop-signal task (SST) is used to study action-stopping in the laboratory. In SSTs, the P3 event-related potential following stop-signals is considered to be a neural index of motor inhibition. However, a similar P3 deflection is often observed following infrequent events in noninhibition tasks. Moreover, within SSTs, stop-signals are indeed infrequent events, presenting a systematic confound that hampers the interpretation of the stop-signal P3 (and other candidate neural indices of motor inhibition). Therefore, we performed two studies to test whether the stopsignal P3 is uniquely related to motor inhibition or reflects infrequency detection. In Study 1, participants completed the SST and a visually identical change-detection task requiring the detection of a task-relevant, frequent signal (but not motor inhibition). We observed a P3 associated with motor inhibition in the SST, but no such positivity in the change-detection task. In Study 2, we modified the change-detection task. Some task-relevant events were now infrequent, matching the frequency of stop-signals in the SST. These events indeed evoked a P3, though of smaller amplitude than the P3 in the SST. Independent component analysis suggested that stopsignal P3 and infrequency-P3 ERPs were non-independent and shared a common neural generator. Further analyses suggested that this common neural process likely reflects motor inhibition in both tasks: infrequent events in the change-detection task lead to a non-instructed, incidental slowing of motor responding, the degree of which was strongly correlated with P3 amplitude. These results have wide-reaching implications for the interpretation of neural signals in both stop-signal and infrequency/oddball-tasks.

β-bursts reveal the trial-to-trial dynamics of movement initiation and cancellation

“…234 healthy adult humans (mean age: 22.7, SEM: .43, 137 female, 25 left-handed) from the Iowa City community participated in the study, either for course credit or for an hourly payment. 123 of those datasets were published as part of other studies, none of which focused on β-bursting [54,[61][62][63]. All procedures were approved by the local ethics committee at the University of Iowa (IRB #201511709).…”

“…The task was identical to the one described in [54,[61][62][63]. In short, trials began with a fixation cross (500ms duration), followed by a white left-or rightward arrow (Go-signal).…”

Reconsidering electrophysiological markers of response inhibition in light of trigger failures in the stop-signal task

“…Alternatively, recent work has shown that the P3 on the stop-signal task shares common neural generators with the P3 elicited in tasks involving infrequent stimulus detection (Waller, Hazeltine, & Wessel, 2019;Wessel & Huber, 2019). If P3 indexes a stimulus detection process, the larger P3 on stop-success compared to stop-failure trials might simply index the successful detection of the stop signal on the former and/or poor detection on the later trial type.…”

Non-selective inhibition of the motor system following unexpected and expected infrequent events

“…This notion has spurred a fundamental discussion about which parts of the neural cascade of activity following stop-signals reflect the attentional detection of an infrequent instructed signal to stop, and which reflect the motor inhibition process itself (Aron et al, 2014;Hampshire & Sharp, 2015;Swick & Chatham, 2014). In many studies that address this question, an inferential contrast is used in which brain activity following stop-signals is compared to brain activity following perceptually identical, infrequent, expected events that do not convey a 'stopping' instruction (Schmajuk et al, 2006;Dimoska & Johnstone, 2008;Hampshire et al, 2010;Boehler et al, 2010;Tabu et al, 2011;Dodds et al, 2011;Chatham et al, 2012;Erika-Florence et al, 2014;Bissett & Logan, 2014;Elchlepp et al, 2015;Lawrence et al, 2015;Verbruggen et al, 2010;Waller, Hazeltine, and Wessel, 2019). In other words, those studies employ a purportedly 'noninhibitory' control condition that resembles the design of our current Experiment 2, where a go-signal is followed by an infrequent expected event.…”

“…In fact, one of the most controversial questions in the recent stopsignal literature is which exact neural or psychological processes following stop-signals are related to the attentional detection of the infrequent stop-signal itself, and which are related to the actual implementation of motor inhibition (Verbruggen et al, 2010;Hampshire et al, 2010;Matzke et al, 2013). To address this question, many studies have utilized control tasks whose stimulus layout matches the stop-signal task (i.e., a go-signal is followed by an infrequent second signal) but with an instruction that does not involve outright action stopping (e.g., to press a second button after the original go-response or to ignore the second signal entirely, Hampshire et al, 2010;Dodds et al, 2011;Chatham et al, 2012;Erika-Florence et al, 2014;Waller et al, 2019). If such expected infrequent stimuli presented outside of a stop-signal task produced the same type of reactive, nonselective motor inhibition that is found after unexpected infrequent stimuli, it would invalidate the assumption that a contrast between a stop-signal and an infrequent-signal control task would isolate the inhibitory process that is found in the stop-signal task.…”