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Abstract

Humans, like other animals, alter their behavior depending on whether a threat is close or distant. We investigated spatial imminence of threat by developing an active avoidance paradigm in which volunteers were pursued through a maze by a virtual predator endowed with an ability to chase, capture, and inflict pain. Using functional magnetic resonance imaging, we found that as the virtual predator grew closer, brain activity shifted from the ventromedial prefrontal cortex to the periaqueductal gray. This shift showed maximal expression when a high degree of pain was anticipated. Moreover, imminence-driven periaqueductal gray activity correlated with increased subjective degree of dread and decreased confidence of escape. Our findings cast light on the neural dynamics of threat anticipation and have implications for the neurobiology of human anxiety-related disorders.

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References and Notes

1
R. J. Blanchard, D. C. Blanchard, in Fear and Defence, P. F. Brain, R. J. Blanchard, S. Parmigiani, Eds. (Harwood Academic, London, 1990), pp. 89–108.
2
M. S. Fanselow, L. S. Lester, in Evolution and Learning, R. C. Bolles, M. D. Beecher, Eds. (Erlbaum, Hillsdale, NJ, 1988), pp. 185–211.
3
M. S. Fanselow, Psychon. Bull. Rev.1, 429 (1994).
4
M. G. Craske, Anxiety Disorders: Psychological Approaches to Theory and Treatment (Westview, Boulder, CO, 1999).
5
V. Rau, M. S. Fanselow, in Understanding Trauma: Integrating Biological, Clinical, and Cultural Perspectives L. J. Kirmayer, R. Lemelson, M. Barad, Eds. (Cambridge Univ. Press, New York, 2007), pp. 27–40.
6
N. McNaughton, P. J. Corr, Neurosci. Biobehav. Rev.28, 285 (2004).
7
J. F. W. Deakin, F. G. Graeff, J. Psychopharmacol.5, 305 (1991).
8
P. J. Lang, M. Davis, Prog. Brain Res.156, 3 (2006).
9
G. S. Berns et al., Science312, 754 (2006).
10
J. M. Gorman, J. M. Kent, G. M. Sullivan, J. D. Coplan, Am. J. Psychiatry157, 493 (2000).
11
O. Devinsky, M. J. Morrell, B. A. Vogt, Brain118, 279 (1995).
12
P. H. Rudebeck, M. J. Buckley, M. E. Walton, M. F. Rushworth, Science313, 1310 (2006).
13
J. C. Hsieh, S. Stone-Elander, M. Ingvar, Neurosci. Lett.262, 61 (1999).
14
J. P. Johansen, H. L. Fields, Nat. Neurosci.7, 398 (2004).
15
K. Shima, J. Tanji, Science282, 1335 (1998).
16
G. Hadjipavlou, P. Dunckley, T. E. Behrens, I. Tracey, Pain123, 169 (2006).
17
J. L. Price, J. Comp. Neurol.493, 132 (2005).
18
J. Amat et al., Nat. Neurosci.8, 365 (2005).
19
F. G. Graeff, Neurosci. Biobehav. Rev.28, 239 (2004).
20
N. S. Floyd, J. L. Price, A. T. Ferry, K. A. Keay, R. Bandler, J. Comp. Neurol.422, 556 (2000).
21
R. Bandler, K. A. Keay, N. Floyd, J. Price, Brain Res. Bull.53, 95 (2000).
22
B. S. Nashold, W. P. Wilson, D. G. Slaughter, J. Neurosurg.30, 14 (1969).
23
M. R. Vianna et al., Braz. J. Med. Biol. Res.34, 233 (2001).
24
X. Protopopescu et al., Neuroreport17, 361 (2006).
25
E. M. Reiman et al., Arch. Gen. Psychiatry46, 493 (1989).
26
E. A. Phelps, M. R. Delgado, K. I. Nearing, J. E. LeDoux, Neuron43, 897 (2004).
27
H. M. Duvernoy, The Human Brain Stem and Cerebellum (Springer, New York, 1995).
28
We thank C. Hagan and U. Frith for helpful comments. Supported by a Brain Research Trust Prize studentship (D.M.) and by the Wellcome Trust.

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Published In

Science
Volume 317 | Issue 5841
24 August 2007

Submission history

Received: 26 April 2007
Accepted: 10 July 2007
Published in print: 24 August 2007

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Authors

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Dean Mobbs*
Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.
Predrag Petrovic
Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.
Jennifer L. Marchant
Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.
Demis Hassabis
Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.
Nikolaus Weiskopf
Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.
Ben Seymour
Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.
Raymond J. Dolan
Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.
Christopher D. Frith
Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.

Notes

* To whom correspondence should be addressed. E-mail: [email protected]

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