Fear and stop: a role for the amygdala in motor inhibition by emotional signals

Abstract

Rapid interruption of ongoing motor actions is crucial to respond to unexpected and potentially threatening situations. Yet, it remains unclear how motor inhibition interacts with emotional processes. Here we used a modified stop-signal task including an emotional component (fearful faces) to investigate whether neural circuits engaged by action suppression are modulated by task-irrelevant threat-related signals. Behavioral performance showed that reaction times were prolonged in the presence of incidental threat information, and this emotional slowing was enhanced when incorrect responses were made following stop signals. However, the speed and efficacy of voluntary inhibition was unaffected by emotion. Brain imaging data revealed that emotional cues during stop trials interacted with activity in limbic regions encompassing the basal amygdala and sublenticular extended amygdala region, as well as with the supplementary motor area (SMA). In addition, successful motor inhibition to threat signals selectively recruited a region in lateral orbitofrontal cortex, distinct from areas in inferior frontal gyrus typically associated with voluntary inhibition. Activity in primary motor cortex was lower when incorrect responses were made on stop signal trials accompanied by a fearful face, relative to neutral, in parallel with the slower response times observed behaviorally. Taken together, our findings suggest that the amygdala may not only promote protective motor reactions in emotionally-significant contexts (such as freezing or defensive behavior) but also influence the execution of ongoing actions by modulating brain circuits involved in motor control, so as to afford quick and adaptive changes in current behavior.