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The Journal of Neuroscience, December 3, 2008, 28(49):13354-13362; doi:10.1523/JNEUROSCI.2944-08.2008
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A Functional Magnetic Resonance Imaging Study on the Neural Mechanisms of Hyperalgesic Nocebo Effect
Jian Kong,1,2 Randy L. Gollub,1,2,3 Ginger Polich,1 Irving Kirsch,4 Peter LaViolette,1,2 Mark Vangel,2,3 Bruce Rosen,2 andTed J. Kaptchuk5 1Department of Psychiatry, Massachusetts General Hospital, 2Massachusetts General Hospital/Massachusetts Institute of Technology/Harvard Medical School Athinoula A. Martinos Center for Biomedical Imaging, and 3Massachusetts General Hospital Clinical Research Center Biomedical Imaging Core, Charlestown, Massachusetts 02129, 4Department of Psychology, University of Hull, Hull HU6 7RX, United Kingdom, and 5Osher Institute, Harvard Medical School, Boston, Massachusetts 02215
Correspondence should be addressed to Jian Kong, Psychiatry Department, Massachusetts General Hospital, Building 149, 13th Street, Suite 2661, Charlestown, MA 02129. Email: kongj{at}nmr.mgh.harvard.edu
Previous studies suggest that nocebo effects, sometimes termed "negative placebo effects," can contribute appreciably to a variety of medical symptoms and adverse events in clinical trials and medical care. In this study, using a within-subject design, we combined functional magnetic resonance imaging (fMRI) and an expectation/conditioning manipulation model to investigate the neural substrates of nocebo hyperalgesia using heat pain on the right forearm. Thirteen subjects completed the study. Results showed that, after administering inert treatment, subjective pain intensity ratings increased significantly more on nocebo regions compared with the control regions in which no expectancy/conditioning manipulation was performed. fMRI analysis of hyperalgesic nocebo responses to identical calibrated noxious stimuli showed signal increases in brain regions including bilateral dorsal anterior cingulate cortex (ACC), insula, superior temporal gyrus; left frontal and parietal operculum, medial frontal gyrus, orbital prefrontal cortex, superior parietal lobule, and hippocampus; right claustrum/putamen, lateral prefrontal gyrus, and middle temporal gyrus. Functional connectivity analysis of spontaneous resting-state fMRI data from the same cohort of subjects showed a correlation between two seed regions (left frontal operculum and hippocampus) and pain network including bilateral insula, operculum, ACC, and left S1/M1. In conclusion, we found evidence that nocebo hyperalgesia may be predominantly produced through an affective–cognitive pain pathway (medial pain system), and the left hippocampus may play an important role in this process.
Key words: nocebo; nocebo effect; hyperalgesia; hyperalgesic nocebo effect; functional connectivity; spontaneous fMRI; resting state; placebo effect; expectancy; expectancy manipulation; sham acupuncture
Received June 25, 2008; revised Oct. 22, 2008; accepted Oct. 27, 2008.
Correspondence should be addressed to Jian Kong, Psychiatry Department, Massachusetts General Hospital, Building 149, 13th Street, Suite 2661, Charlestown, MA 02129. Email: kongj{at}nmr.mgh.harvard.edu
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