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Science 24 August 2007:
Vol. 317. no. 5841, pp. 1079 - 1083
DOI: 10.1126/science.1144298

Reports

When Fear Is Near: Threat Imminence Elicits Prefrontal-Periaqueductal Gray Shifts in Humans

Dean Mobbs*, Predrag Petrovic, Jennifer L. Marchant, Demis Hassabis, Nikolaus Weiskopf, Ben Seymour, Raymond J. Dolan and Christopher D. Frith

Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London WC1N 3BG, UK.


Figure 1 Fig. 1. The virtual predator and prey paradigm. Subjects were presented with a two-dimensional maze containing a 9 x 13 rectangle grid of walls (black squares) and paths (white squares). All experimental conditions commenced with a "neutral phase" where a preprogrammed artificially intelligent (AI) gray circle (AIneutral) appeared at the left-bottom side of the maze (A). The AIneutral was presented on average for 6 s (jitter ± 2 s) and programmed to wander the maze indiscriminately. After this, the "cue phase" commenced with the AIneutral changed into a predator (AIpredator) or a yoked control condition. The change from AIneutral to AIpredator was signaled by the circle flashing between red and gray. The flashing AIpredator appeared for 2 s, and during this time it wandered the maze indiscriminately. Directly after this, subjects were also informed for 2 s of the amount of cutaneous electrical shock they would receive if the AIpredator captured them: (B) one shock (AI Formula), (C) no shock, or (D) three shocks (AIFormula). During the cue phase, subjects were passive and unable to move the blue triangle situated in the upper right corner of the maze. The "chase phase" began with the AIpredator ceasingtoflash andthe subject moving the blue triangle to (E) escape the AIFormula,(F) mimic the movements of the triangle in a replay of a previous experimental condition, or (G) escape the AIFormula.(H) After escape or capture, a rest period was presented before the onset of the next trial. To ensure that subjects would not anticipate the end of the chase, we randomly varied the time each AIpredator encounter was played (e.g., 16, 20, 24, 28, 32 s). The subjects were not informed that the length of trials varied or given any indication of how much time they had on each trial. To enhance the feelings of spatial distance, mazes were intentionally designed so that chases were long unimpeded runs with no dead-ends. Each block was interleaved with 8, 10, or 12 s of black screen. Further details can be found in the supporting online material. [View Larger Version of this Image (27K GIF file)]
 

Figure 2 Fig. 2. Statistical parametric maps illustrating BOLD responses to the aversive cues and activation for the AIpredator conditions collapsed across blocks. Mean activity is shown for regions within 4 mm of peak. (A and B) Activity for the AIpredator (red circle) minus the AIneutral (blue circle) cue in (A) rACC and (B) periaqueductal gray (PAG) activity increased during all AIpredator blocks minus yoked blocks. (C) Activity in the rACC/mPFC and vmPFC (table S2) for yoked blocks minus AIpredator blocks. [View Larger Version of this Image (48K GIF file)]
 

Figure 3 Fig. 3. fMRI results illustrating the imminence effect in the predator condition. For distal threat there was greater activity in vmPFC (horizontal view) for both (A) AIFormula and (B) AIFormula shock expectation. (C) For proximal threat there was greater activity in the PAG for AIFormula [left panel, sagittal view; center panel, horizontal view; right panel, schematic depiction of the midbrain with PAG shown in orange; modified from (27)]. See fig. S2 for images of the PAG activity for the AIFormula imminence. See fig. S4 for coronal view of the PAG activity. [View Larger Version of this Image (43K GIF file)]
 

Figure 4 Fig. 4. Subject-specific differences in dread of capture and confidence of escape. (A and B) Scatterplots of regions of the PAG that correlated with threat distance and increased dread of being caught by the (A) AIFormula and (B) AIFormula.(C and D) Regions associated with threat distance and decreased confidence of escaping the (C) AI Formula and (D) AIFormula. Each point represents an individual's response on post-scan questionnaire. [View Larger Version of this Image (21K GIF file)]
 





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Science. ISSN 0036-8075 (print), 1095-9203 (online)