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

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.

Leveling the Field for a Fairer Race between Going and Stopping: Neural Evidence for the Race Model of Motor Inhibition from a New Version of the Stop Signal Task.

The stop signal task (SST) is the gold standard experimental model of inhibitory control. However, neither SST condition-contrast (stop vs. go, successful vs. failed stop) purely operationalizes inhibition. Because stop trials include a second, infrequent signal, the stop versus go contrast confounds inhibition with attentional and stimulus processing demands. While this confound is controlled for in the successful versus failed stop contrast, the go process is systematically faster on failed stop trials, contaminating the contrast with a different noninhibitory confound. Here, we present an SST variant to address both confounds and evaluate putative neural indices of inhibition with these influences removed. In our variant, stop signals occurred on every trial, equating the noninhibitory demands of the stop versus go contrast. To entice participants to respond despite the impending stop signals, responses produced before stop signals were rewarded. This also reversed the go process bias that typically affects the successful versus failed stop contrast. We recorded scalp electroencephalography in this new version of the task (as well as a standard version of the SST with infrequent stop signal) and found that, even under these conditions, the properties of the frontocentral stop signal P3 ERP remained consistent with the race model. Specifically, in both tasks, the amplitude of the P3 was increased on stop versus go trials. Moreover, the onset of this P3 occurred earlier for successful compared with failed stop trials in both tasks, consistent with the proposal of the race model that an earlier start of the inhibition process will increase stopping success. Therefore, the frontocentral stop signal P3 represents a neural process whose properties are in line with the predictions of the race model of motor inhibition, even when the SST's confounds are controlled.

Non-selective inhibition of inappropriate motor-tendencies during response-conflict by a fronto-subthalamic mechanism.

To effectively interact with their environment, humans must often select actions from multiple incompatible options. Existing theories propose that during motoric response-conflict, inappropriate motor activity is actively (and perhaps non-selectively) suppressed by an inhibitory fronto-basal ganglia mechanism. We here tested this theory across three experiments. First, using scalp-EEG, we found that both outright action-stopping and response-conflict during action-selection invoke low-frequency activity of a common fronto-central source, whose activity relates to trial-by-trial behavioral indices of inhibition in both tasks. Second, using simultaneous intracranial recordings from the basal ganglia and motor cortex, we found that response-conflict increases the influence of the subthalamic nucleus on M1-representations of incorrect response-tendencies. Finally, using transcranial magnetic stimulation, we found that during the same time period when conflict-related STN-to-M1 communication is increased, cortico-spinal excitability is broadly suppressed. Together, these findings demonstrate that fronto-basal ganglia networks buttress action-selection under response-conflict by rapidly and non-selectively net-inhibiting inappropriate motor tendencies.

Perceptual Surprise Improves Action Stopping by Nonselectively Suppressing Motor Activity via a Neural Mechanism for Motor Inhibition.

Motor inhibition is a cognitive control ability that allows humans to stop actions rapidly even after initiation. Understanding and improving motor inhibition could benefit adaptive behavior in both health and disease. We recently found that presenting surprising, task-unrelated sounds when stopping is necessary improves the likelihood of successful stopping. In the current study, we investigated the neural underpinnings of this effect. Specifically, we tested whether surprise-related stopping improvements are due to a genuine increase in motor inhibition. In Experiment 1, we measured motor inhibition in primary motor cortex of male and female humans by quantifying corticospinal excitability (CSE) via transcranial magnetic stimulation and electromyography during a hybrid surprise-Go/NoGo task. Consistent with prior studies of motor inhibition, successful stopping was accompanied by nonselective suppression of CSE; that is, CSE was suppressed even in task-unrelated motor effectors. Importantly, unexpected sounds significantly increased this motor-system inhibition to a degree that was directly related to behavioral improvements in stopping. In Experiment 2, we then used scalp encephalography to investigate whether unexpected sounds increase motor-inhibition-related activity in the CNS. We used an independent stop-signal localizer task to identify a well characterized frontocentral low-frequency EEG component that indexes motor inhibition. We then investigated the activity of this component in the surprise-Go/NoGo task. Consistent with Experiment 1, this signature of motor inhibition was indeed increased when NoGo signals were followed by unexpected sounds. Together, these experiments provide converging evidence suggesting that unexpected events improve motor inhibition by automatically triggering inhibitory control.SIGNIFICANCE STATEMENT The ability to stop ongoing actions rapidly allows humans to adapt their behavior flexibly and rapidly. Action stopping is important in daily life (e.g., stopping to cross the street when a car approaches) and is severely impaired in many neuropsychiatric disorders. Therefore, finding ways to improve action stopping could aid adaptive behaviors in health and disease. Our current study shows that presenting unexpected sounds in stopping situations facilitates successful stopping. This improvement is specifically due to a surprise-related increase in a neural mechanism for motor inhibition, which rapidly suppresses the excitability of the motor system after unexpected events. These findings suggest a tight interaction between the neural systems for surprise processing and motor inhibition and yield a promising avenue for future research.