From threat to fear: the neural organization of defensive fear systems in humans.
Open accessAbstract
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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Even during rest/off task, individuals with PTSD have a predisposition to engage the innate alarm system, the subcortical brain network hypothesized to facilitate reflexive defensive responses to a perceived threat.
“Specifically, it appears that, even during rest/off task, individuals with PTSD have a predisposition to engage the innate alarm system, the subcortical brain network hypothesized to facilitate reflexive defensive responses to a perceived threat (Liddell et al., 2005; Mobbs et al., 2009; Steuwe et al., 2014; Lanius et al., 2017).”
From How Processing of Sensory Information From the Internal and External Worlds Shape the Perception and Engagement With the World in the Aftermath of Trauma: Implications for PTSD (2021) · cites this paper as Mobbs et al., 2009
The Discussion describes fast, “hard-wired” midbrain defenses during imminent threat, supporting the description of a subcortical system for rapid defensive responses. It does not establish that people with PTSD are predisposed to engage that system at rest or off task; its brief mention of PTSD concerns abnormalities reported in other studies. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe activations observed in the medial prefrontal network are consistent with previous imaging studies implicating medial prefrontal cortex in distal threat, and suggest that contextually induced sustained anxiety may involve complex oscillations in neural activity in key prefrontal regions such as pACC and sACC.
“Although the medial prefrontal network was not the focus of this study, the activations observed in this network are consistent with previous imaging studies implicating medial prefrontal cortex in distal threat (Mobbs et al., 2009), and suggest that contextually induced sustained anxiety may involve complex oscillations in neural activity in key prefrontal regions such as pACC and sACC.”
From Phasic and sustained fear in humans elicits distinct patterns of brain activity (2011) · cites this paper as Mobbs et al., 2009
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“…animal research (for an overview see https://fanselowlab.psych.ucla.edu/predatory-immine nce-continuum/) and Mobbs’ threat processing model (Mobbs et al., 2009), the defense cascade model by Lanius and colleagues (2018) posits that humans under severe threat initially respond with an…”
Backgroundde Souza Caetano, K. A., de Oliveira, A. R., & Brandão, M. L. (2013) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32836356c4 · Cited by 62 · see citing works
Vieira, J. B., Pierzchajlo, S. R., & Mitchell, D. G. V. (2020) · Social Neuroscience · doi:10.1080/17470919.2019.1626763 · Cited by 54 · see citing works
Effect of Parasympathetic Stimulation on Brain Activity During Appraisal of Fearful Expressions
Makovac, E., Garfinkel, S. N., Bassi, A., Basile, B., Macaluso, E., Cercignani, M., Calcagnini, G., Mattei, E., Agalliu, D., Cortelli, P., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.10 · Cited by 54 · see citing works
Loddo, G., Sessagesimi, E., Mignani, F., Cirignotta, F., Mondini, S., Licchetta, L., Bisulli, F., Tinuper, P., & Provini, F. (2018) · Sleep Medicine · doi:10.1016/j.sleep.2017.08.019 · Cited by 50 · see citing works
Vieira, J. B., Tavares, T. P., Marsh, A. A., & Mitchell, D. G. V. (2017) · Human Brain Mapping · doi:10.1002/hbm.23467 · Cited by 43 · see citing works
Neuroimaging the temporal dynamics of human avoidance to sustained threat
Schlund, M. W., Hudgins, C. D., Magee, S., & Dymond, S. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.09.042 · Cited by 33 · see citing works
Terpou, B. A., Densmore, M., Théberge, J., Thome, J., Frewen, P., McKinnon, M. C., & Lanius, R. A. (2019) · Chronic Stress · doi:10.1177/2470547019871369 · Cited by 26 · see citing works
Altered time course of amygdala activation during speech anticipation in social anxiety disorder
Davies, C. D., Young, K., Torre, J. B., Burklund, L. J., Goldin, P. R., Brown, L. A., Niles, A. N., Lieberman, M. D., & Craske, M. G. (2017) · Journal of Affective Disorders · doi:10.1016/j.jad.2016.11.014 · Cited by 21 · see citing works
Leicht, G., Mulert, C., Eser, D., Sämann, P. G., Ertl, M., Laenger, A., Karch, S., Pogarell, O., Meindl, T., Czisch, M., et al. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.09.004 · Cited by 21 · see citing works
- Authors
- Mobbs, D., Marchant, J. L., Hassabis, D., Seymour, B., Tan, G., Gray, M., Petrovic, P., Dolan, R. J., & Frith, C. D.
- Affiliations
- Wellcome Centre for Human Neuroimaging (GB)
- Brighton and Sussex Medical School (GB)
- Corresponding author
- Mobbs, Dean
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-09-30
- Volume
- 29
- Issue
- 39
- Pages
- 12236-12243
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2782300
- OpenAlex
- W1979538778
- Cited by
- 476
- References
- 58
- Citations by year
- 2026: 12 · 2025: 36 · 2024: 35 · 2023: 32 · 2022: 29 · 2021: 39 · 2020: 26 · 2019: 36 · 2018: 28 · 2017: 29 · 2016: 29 · 2015: 34 · 2014: 26 · 2013: 30 · 2012: 21
- FWCI
- 8.71
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by)
- UCL Discovery (University College London) (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- Cambridge University Engineering Department Publications Database (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (047963)
- Brain Research Trust
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Keywords
- threat anticipation, avoidance behavior, subgenual anterior cingulate cortex, pregenual anterior cingulate cortex, midbrain, amygdala, hippocampus, neural coupling, panic, threat probability
- MeSH terms
- Adult, Escape Reaction, Fear, Female, Humans, Magnetic Resonance Imaging, Male, Nerve Net, Panic, Photic Stimulation, Psychomotor Performance, Reaction Time, Young Adult
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