Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

Abstract

Action-stopping is a canonical executive function thought to involve top-down control over the motor system. Here we aimed to validate this stopping system using high temporal resolution methods in humans. We show that, following the requirement to stop, there was an increase of right frontal beta (~13 to 30 Hz) at ~120 ms, likely a proxy of right inferior frontal gyrus; then, at 140 ms, there was a broad skeletomotor suppression, likely reflecting the impact of the subthalamic nucleus on basal ganglia output; then, at ~160 ms, suppression was detected in the muscle, and, finally, the behavioral time of stopping was ~220 ms. This temporal cascade supports a physiological model of action-stopping, and partitions it into subprocesses that are isolable to different nodes and are more precise than the behavioral latency of stopping. Variation in these subprocesses, including at the single-trial level, could better explain individual differences in impulse control.

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

“…Consistent with recent studies, this parametric estimation technique resulted in an attenuation of SSRT compared to the traditional nonparametric integration method (Band et al, 2003;Jana et al, 2020;Matzke, Love, et al, 2017;Skippen et al, 2019;Weigard et al, 2019). Importantly, SSRT int was only moderately correlated with SSRT EXG3 , but was strongly associated with trigger failure.…”

“…The notion of an automatic response inhibition process is supported by both the fast estimates of SSRT (≈130 ms; see also Matzke, Hughes, et al, 2017;Skippen et al, 2019) and by motor evoked potential studies that suggest the inhibition processes occurs around 140 ms (Coxon, Stinear, & Byblow, 2006;Jana et al, 2020;Raud & Huster, 2017;Waldvogel et al, 2000;Wilcoxon, Nadolski, Samarut, Chassande, & Redei, 2007). In fact, a recent multi-modal study by Jana et al (2020) showed that the cascade of processing that occurs during the stop-signal task suppresses muscle activity within 160 ms after a visual stop-signal onset. As the registration of auditory signals occurs around 30 ms earlier than visual signals (Jain, Bansal, Kumar, & Singh, 2015;Ramautar, Kok, et al, 2006), the 130 ms estimate of SSRT found here is consistent with the fast inhibition process described by Jana et al (2020).…”

“…Trigger failure, or the failure to initiate the stop process, has long been acknowledged as possibly contributing to performance on the stop-signal task (Logan, 1994), but cannot easily be taken into account with nonparametric methods of estimating SSRT (Band et al, 2003). Not accounting for trigger failure has been shown to produce biased estimates of SSRT (Band et al, 2003;Jana, Hannah, Muralidharan, & Aron, 2020;Matzke, Love, et al, 2017;Skippen et al, 2019;Weigard, Heathcote, Matzke, & Huang-Pollock, 2019), indicating that effective inhibitory control relies not only on fast SSRT, but also on the reliability of triggering the stop process (Chatham et al, 2012;Matzke, Love, et al, 2017).…”

“…In fact, a recent multi-modal study by Jana et al (2020) showed that the cascade of processing that occurs during the stop-signal task suppresses muscle activity within 160 ms after a visual stop-signal onset. As the registration of auditory signals occurs around 30 ms earlier than visual signals (Jain, Bansal, Kumar, & Singh, 2015;Ramautar, Kok, et al, 2006), the 130 ms estimate of SSRT found here is consistent with the fast inhibition process described by Jana et al (2020).…”

tDCS over the inferior frontal gyri and visual cortices did not improve response inhibition

“…In fact, studies have shown that both the peak and onset latency of the P3 might correlate with the SSRT [13][14][15][16] , suggesting that P3 latency measures could be potential neural markers of inhibitory capability. In addition to this, studies have found that the effects of inhibitory control can be measured by electromyographic (EMG) activity at response effector muscles in successful stop trials 4,[17][18][19] . While the onset of this so-called partial response EMG (prEMG) reflects the response to the preceding go stimuli, the point for the prEMG decline (i.e.…”