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 non-inhibition 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 stop-signal 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 stop-signal 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.

Keywords: Action-stopping; Event-related potentials; Frontocentral P3; Infrequency detection; Motor inhibition.

Figure 1

Behavioral tasks used in Study 1.

Figure 2

Behavioral tasks used in Study 2.

Figure 3

ERPs from the SST in Study 1 time-locked to stop-signal onset and plotted over average of Cz and FCz electrodes. Gray shading indicates significant differences between successful and failed stop trials (FDR corrected at p <. 05). A) ERPs and P3 peak topography for failed and successful stop trials plotted during the same time range on matched go trials. B) ERPs and peak P3 topography for successful and failed stop trials and matched-go trials plotted using only the selected Frontocentral P3 IC. C) ERPs and peak P3 topography for successful and failed stop trials and matched-go trials plotted using all independent components besides the selected Frontocentral P3 IC.

Figure 4

ERPs from the visual change-detection task in Study 1 time locked to the onset of white and red arrows, respectively, plotted using an average of Cz and FCz electrodes. Gray shading indicates a significant difference between ERP responses to white and red arrows (FDR corrected at p < .05). A) ERPs and P3 peak topographies following white versus red arrow stimulus onset. B) ERPs and P3 peak topographies following white versus red arrow stimulus onset plotted using only the selected Frontocentral P3 IC. C) ERPs and P3 peak topographies following white versus red arrow stimulus onset. B) ERPs and P3 peak topographies following white versus red arrow stimulus onset plotted using all independent components besides the selected Frontocentral P3 IC.

Figure 5

ERPs from the SSTs in Study 2 time-locked to stop-signal onset and plotted over average of Cz and FCz electrodes. Gray shading indicates significant differences between successful and failed stop trials (FDR corrected at p <. 05). A) ERPs and P3 peak topography for failed and successful stop trials from the adaptive-delay SST plotted during the same time range on matched go trials. B) ERPs and peak P3 topography for successful and failed stop trials and matched-go trials from the adaptive-delay SST plotted using only the selected P3a independent component. C) ERPs and peak P3 for successful and failed stop trials and matched-go trials from the adaptive-delay SST plotted using all independent components besides the selected Frontocentral P3 IC. D) ERPs and P3 peak topography for failed and successful stop trials from the adaptive-delay SST plotted during the same time range on matched go trials. E) ERPs and peak P3 topography for successful and failed stop trials and matched-go trials from the adaptive-delay SST plotted using only the selected Frontocentral P3 IC. F) ERPs and peak P3 for successful and failed stop trials and matched-go trials from the adaptive-delay SST plotted using all independent components besides the selected Frontocentral P3 IC.

Figure 6

ERPs from the visual change-detection task in Study 2 time locked to the onset of black (frequent stimulus) and red arrows (infrequent stimulus), respectively, plotted using an average of Cz and FCz electrodes. Gray shading indicates a significant difference between ERP responses to black and red arrows (FDR corrected at p < .05). A) ERPs and P3 peak topographies following black versus red arrow stimulus onset. B) ERPs and P3 peak topographies following black versus red arrow stimulus onset plotted using only the selected Frontocentral P3 IC. C) ERPs and P3 peak topographies following black versus red arrow stimulus onset. B) ERPs and P3 peak topographies following black versus red arrow stimulus onset plotted using all independent components besides the selected Frontocentral P3 IC.

Figure 7

Analysis of the correlation between Frontocentral P3 peak amplitude and RT slowing in Study 2’s visual change-detection task. A) ERPs in response to black and red arrow onsets, plotted only using the activation of the Frontocentral P3 IC over the average of Cz and FCz. B) Mean RT to black arrows on black arrow-only trials, mean RT to black arrows on trials where both arrow colors were present, and mean RT to red arrows. Mean RT to black arrows on trials where red arrows were also present was significantly longer than the mean RT to black arrows on black arrow-only trials (** designates a significant difference as shown by t-test at p < .001). C) Scatter plot of participant-wise Frontocentral P3 amplitude difference and black arrow RT slowing (calculated as a proportion of the black arrow-only RT) with line of best fit.