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Cerebral Cortex Advance Access published online on August 13, 2009
Cerebral Cortex, doi:10.1093/cercor/bhp155
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© The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Uncertainty during Anticipation Modulates Neural Responses to Aversion in Human Insula and Amygdala

I. Sarinopoulos1, D. W. Grupe2, K. L. Mackiewicz3, J. D. Herrington4, M. Lor5, E. E. Steege6 and J. B. Nitschke2

1 Departments of Psychology and Radiology, Michigan State University, East Lansing, MI 48824, USA, 2 Waisman Laboratory for Brain Imaging and Behavior, Departments of Psychiatry and Psychology, University of Wisconsin, Madison, WI 53705, USA, 3 Department of Psychology, University of Colorado, Boulder, CO 80309, USA, 4 Center for Autism Research, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA, 5 Columbia University School of Social Work, New York City, NY 10027, USA, 6 College of Physical Education and Sport Science, West Virginia University, Morgantown, WV 26506, USA

Address correspondence to Jack B. Nitschke, PhD, Waisman Laboratory for Brain Imaging and Behavior, 1500 Highland Avenue, Madison, WI 53705-2280, USA. Email: jnitschke{at}wisc.edu.

Uncertainty about potential negative future outcomes can cause stress and is a central feature of anxiety disorders. The stress and anxiety associated with uncertain situations may lead individuals to overestimate the frequency with which uncertain cues are followed by negative outcomes, an example of covariation bias. Using functional magnetic resonance imaging, we found that uncertainty-related expectations modulated neural responses to aversion. Insula and amygdala responses to aversive pictures were larger after an uncertain cue (that preceded aversive or neutral pictures) than a certain cue (that always preceded aversive pictures). Anticipatory anterior cingulate cortex (ACC) activity elicited by the cues was inversely associated with the insula and amygdala responses to aversive pictures following the cues. Nearly 75% of subjects overestimated the frequency of aversive pictures following uncertain cues, and ACC and insula activity predicted this uncertainty-related covariation bias. Findings provide the first evidence of the brain mechanisms of covariation bias and highlight the temporal dynamics of ACC, insula, and amygdala recruitment for processing aversion in the context of uncertainty.

Key Words: anterior cingulate cortex • covariation bias • emotion • expectancy • fMRI


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