From Threat to Fear: The Neural Organization of Defensive Fear Systems in Humans
Abstract
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.
Additional Information
© 2009 Society for Neuroscience. For the first six months after publication SfN's license will be exclusive. Beginning six months after publication the Work will be made freely available to the public on SfN's website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). Received May 21, 2009; accepted July 1, 2009. This work was funded by the Wellcome Trust research programme grants. D.M. was supported by a Brain Research Trust Prize studentship and the Medical Research Council. We thank C. Hagan, L. Passamonti, C Hutton, and N. Weiskopf for discussions and help with data analysis.Attached Files
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Additional details
- PMCID
- PMC2782300
- Eprint ID
- 85103
- Resolver ID
- CaltechAUTHORS:20180305-140448946
- Wellcome Trust
- Brain Research Trust
- Medical Research Council (UK)
- Created
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2018-03-05Created from EPrint's datestamp field
- Updated
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2021-11-15Created from EPrint's last_modified field