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The Journal of Neuroscience, September 30, 2009, 29(39):12236-12243; doi:10.1523/JNEUROSCI.2378-09.2009

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Behavioral/Systems/Cognitive
From Threat to Fear: The Neural Organization of Defensive Fear Systems in Humans

Dean Mobbs,^1,2 Jennifer L. Marchant,¹ Demis Hassabis,¹ Ben Seymour,¹ Geoffrey Tan,¹ Marcus Gray,^1,5 Predrag Petrovic,^1,3 Raymond J. Dolan,¹ and Christopher D. Frith^1,4

¹Wellcome Trust Centre for Neuroimaging, University College London, London WC1 3BG, United Kingdom, ²Medical Research Council-Cognition and Brain Sciences Unit, Cambridge CB2 7EF, United Kingdom, ³Department of Clinical Neuroscience, Karolinska Institute, 71 76 Stockholm, Sweden, ⁴Centre for Functional Integrative Neuroscience, Aarhus University Hospital, DK-800 Aarhus C, Denmark, and ⁵Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex, Brighton, East Sussex BN1 9PX, United Kingdom

Correspondence should be addressed to Dr. Dean Mobbs, Medical Research Council-Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, UK. Email: dean.mobbs{at}mrc-cbu.cam.ac.uk

Postencounter and circa-strike defensive contexts represent two adaptive responses to potential and imminent danger. In the context of a predator, the postencounter reflects the initial detection of the potential threat, whereas the circa-strike is associated with direct predatory attack. We used functional magnetic resonance imaging to investigate the neural organization of anticipation and avoidance of artificial predators with high or low probability of capturing the subject across analogous postencounter and circa-strike contexts of threat. Consistent with defense systems models, postencounter threat elicited activity in forebrain areas, including subgenual anterior cingulate cortex (sgACC), hippocampus, and amygdala. Conversely, active avoidance during circa-strike threat increased activity in mid-dorsal ACC and midbrain areas. During the circa-strike condition, subjects showed increased coupling between the midbrain and mid-dorsal ACC and decreased coupling with the sgACC, amygdala, and hippocampus. Greater activity was observed in the right pregenual ACC for high compared with low probability of capture during circa-strike threat. This region showed decreased coupling with the amygdala, insula, and ventromedial prefrontal cortex. Finally, we found that locomotor errors correlated with subjective reports of panic for the high compared with low probability of capture during the circa-strike threat, and these panic-related locomotor errors were correlated with midbrain activity. These findings support models suggesting that higher forebrain areas are involved in early-threat responses, including the assignment and control of fear, whereas imminent danger results in fast, likely "hard-wired," defensive reactions mediated by the midbrain.

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Received May 21, 2009; accepted July 1, 2009.

Correspondence should be addressed to Dr. Dean Mobbs, Medical Research Council-Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, UK. Email: dean.mobbs{at}mrc-cbu.cam.ac.uk

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