A shared threat-anticipation circuit is dynamically engaged at different moments by certain and uncertain threat

Abstract

ABSTRACTTemporal dynamics play a central role in models of emotion:“fear”is widely conceptualized as a phasic response to certain-and-imminent danger, whereas“anxiety”is a sustained response to uncertain-or-distal harm. Yet the underlying human neurobiology remains contentious. Leveraging an ethnoracially diverse sample, translationally relevant paradigm, and theory-driven modeling approach, we demonstrate that certain and uncertain threat recruit a shared threat-anticipation circuit. This cortico-subcortical circuit exhibits persistently elevated activation when anticipating uncertain-threat encounters and a transient burst of activation in the moments before certain encounters. For many scientists and clinicians, feelings are the defining feature of human fear and anxiety. Here we used an independently validated brain signature to covertly decode the momentary dynamics of anticipatory distress for the first time. Results mirrored the dynamics of neural activation. These observations provide fresh insights into the neurobiology of threat-elicited emotions and set the stage for more ambitious clinical and mechanistic research.SIGNIFICANCE STATEMENT“Fear”is often viewed as a phasic response to certain-and-imminent danger, whereas“anxiety”is a sustained response to uncertain-or-distal harm. Prior work begun to reveal the neural systems recruited by different threats, but has yet to plumb the moment-by-moment dynamics anticipated by theory and behavioral research. Here we used a novel combination of neuroimaging techniques to demonstrate that certain and uncertain threat recruit a shared threat-anticipation circuit. Activity in this circuit and covert measures of distress showed similar patterns of context-dependent dynamics, exhibiting persistent increases when anticipating uncertain-threat encounters and transient surges in the seconds before certain encounters. These observations provide fresh insights into the neurobiology of fear and anxiety, laying the groundwork for more ambitious clinical and mechanistic research.