Slow escape decisions are swayed by trait anxiety

• Published in: Nature human behaviour Vol. 3; no. 7; pp. 702 - 708
• Main Authors: Fung, Bowen J., Qi, Song, Hassabis, Demis, Daw, Nathaniel, Mobbs, Dean
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.07.2019; Nature Publishing Group
• Subjects: 4014/477/2811; 631/378/1457/1284; 631/378/1457/1369; 631/378/1457/1945; 631/378/2649/1409; Adolescent; Adult; Amygdala; Amygdala - diagnostic imaging; Amygdala - physiology; Amygdala - physiopathology; Anxiety; Anxiety - physiopathology; Anxiety - psychology; Behavioral Sciences; Biomedical and Life Sciences; Blood; Brain; Brain - diagnostic imaging; Brain - physiology; Brain - physiopathology; Cerebral Cortex - diagnostic imaging; Cerebral Cortex - physiology; Cerebral Cortex - physiopathology; Circuits; Cognition - physiology; Cognitive-behavioral factors; Cortex; Decision Making - physiology; Escape; Escape Reaction - physiology; Experimental Psychology; Fear; Fear & phobias; Female; Functional magnetic resonance imaging; Functional Neuroimaging; Hippocampus; Hippocampus - diagnostic imaging; Hippocampus - physiology; Hippocampus - physiopathology; Humans; Individual differences; Letter; Life Sciences; Magnetic Resonance Imaging; Male; Microeconomics; Models, Theoretical; Neurosciences; Oxygen; Periaqueductal Gray - diagnostic imaging; Periaqueductal Gray - physiology; Periaqueductal Gray - physiopathology; Personality; Personality and Social Psychology; Prefrontal Cortex - diagnostic imaging; Prefrontal Cortex - physiology; Prefrontal Cortex - physiopathology; Trait anxiety; Young Adult
• ISSN: 2397-3374; 2397-3374
• DOI: 10.1038/s41562-019-0595-5

Theoretical models distinguish between neural responses elicited by distal threats and those evoked by more immediate threats 1 – 3 . Specifically, slower ‘cognitive’ fear responses towards distal threats involve a network of brain regions including the ventral hippocampus (vHPC) and medial prefrontal cortex (mPFC), while immediate ‘reactive’ fear responses rely on regions such as the periaqueductal grey 4 , 5 . However, it is unclear how anxiety and its neural substrates relate to these distinct defensive survival circuits. We tested whether individual differences in trait anxiety would impact escape behaviour and neural responses to slow and fast attacking predators: conditions designed to evoke cognitive and reactive fear, respectively. Behaviourally, we found that trait anxiety was not related to escape decisions for fast threats, but individuals with higher trait anxiety escaped earlier during slow threats. Functional magnetic resonance imaging showed that when subjects faced slow threats, trait anxiety positively correlated with activity in the vHPC, mPFC, amygdala and insula. Furthermore, the strength of functional coupling between two components of the cognitive circuit—the vHPC and mPFC—was correlated with the degree of trait anxiety. This suggests that anxiety predominantly affects cognitive fear circuits that are involved in volitional strategic escape. Fung et al. show that participants’ trait anxiety is associated with earlier escape decisions when facing slowly approaching threats. Anxiety correlates with task-driven blood-oxygen-level-dependent activity in the cognitive fear circuits.