Active avoidance and attentive freezing in the face of approaching threat

•We examined brain dynamics and defensive response patterns during approaching threat that could either be avoided or not.•Inescapable threat was associated with attentive freezing behavior indicated by startle potentiation and fear bradycardia.•During escapable threat, defense behavior switched to active avoidance with startle inhibition and heart rate acceleration.•Approaching threat was associated with increasing anterior insula and periaqueductal grey activation.•The switch in defense behavior according to threat imminence and behavioral options was associated with vmPFC activity.

Defensive behaviors in animals and humans vary dynamically with increasing proximity of a threat and depending upon the behavioral repertoire at hand. The current study investigated physiological and behavioral adjustments and associated brain activation when participants were exposed to dynamically approaching threat that was either inevitable or could be avoided by motor action. When the approaching threat was inevitable, attentive freezing was observed as indicated by fear bradycardia, startle potentiation, and a dynamic increase in activation of the anterior insula and the periaqueductal grey. In preparation for active avoidance a switch in defensive behavior was observed characterized by startle inhibition and heart rate acceleration along with potentiated activation of the amygdala and the periaqueductal grey. Importantly, the modulation of defensive behavior according to threat imminence and the behavioral option at hand was associated with activity changes in the ventromedial prefrontal cortex. These findings improve our understanding of brain mechanisms guiding human behavior during approaching threat depending on available resources.