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

Abstract

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.

Keywords: Go/NoGo task; corticospinal excitability; motor evoked potentials; motor inhibition; stop-signal P3; surprise.