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

Mobbs, Dean and Marchant, Jennifer L. and Hassabis, Demis and Seymour, Ben and Tan, Geoffrey and Gray, Marcus and Petrovic, Predrag and Dolan, Raymond J. and Frith, Christopher D. (2009) From Threat to Fear: The Neural Organization of Defensive Fear Systems in Humans. Journal of Neuroscience, 29 (39). pp. 12236-12243. ISSN 0270-6474. PMCID PMC2782300. doi:10.1523/JNEUROSCI.2378-09.2009. https://resolver.caltech.edu/CaltechAUTHORS:20180305-140448946

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1523/JNEUROSCI.2378-09.2009DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2782300/PubMed CentralArticle
ORCID:
AuthorORCID
Mobbs, Dean0000-0003-1175-3772
Dolan, Raymond J.0000-0001-9356-761X
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.
Funders:
Funding AgencyGrant Number
Wellcome TrustUNSPECIFIED
Brain Research TrustUNSPECIFIED
Medical Research Council (UK)UNSPECIFIED
Issue or Number:39
PubMed Central ID:PMC2782300
DOI:10.1523/JNEUROSCI.2378-09.2009
Record Number:CaltechAUTHORS:20180305-140448946
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180305-140448946
Official Citation:From Threat to Fear: The Neural Organization of Defensive Fear Systems in Humans Dean Mobbs, Jennifer L. Marchant, Demis Hassabis, Ben Seymour, Geoffrey Tan, Marcus Gray, Predrag Petrovic, Raymond J. Dolan, Christopher D. Frith Journal of Neuroscience 30 September 2009, 29 (39) 12236-12243; DOI: 10.1523/JNEUROSCI.2378-09.2009
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:85103
Collection:CaltechAUTHORS
Deposited By:INVALID USER
Deposited On:05 Mar 2018 22:23
Last Modified:15 Nov 2021 20:25

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