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The Journal of Neuroscience, January 9, 2008, 28(2):349-359; doi:10.1523/JNEUROSCI.2500-07.2008

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Neurobiology of Disease
Reduced Brainstem Inhibition during Anticipated Pelvic Visceral Pain Correlates with Enhanced Brain Response to the Visceral Stimulus in Women with Irritable Bowel Syndrome

Steven M. Berman, Bruce D. Naliboff, Brandall Suyenobu, Jennifer S. Labus, Jean Stains, Gordon Ohning, Lisa Kilpatrick, Joshua A. Bueller, Kim Ruby, Johanna Jarcho, and Emeran A. Mayer

Departments of Medicine, Physiology, Psychiatry and Biobehavioral Sciences, and Brain Research Institute, University of California, Los Angeles Center for Neurovisceral Sciences and Women's Health, David Geffen School of Medicine at University of California, Los Angeles, Los Angeles, CA 90073, and Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, California 90073

Correspondence should be addressed to Dr. Emeran A. Mayer, Center for Neurovisceral Sciences and Women's Health, Veterans Affairs Greater Los Angeles Healthcare System, Building 115, Room 223, 11301 Wilshire Blvd, Los Angeles, CA 90073. Email: emayer{at}ucla.edu

Cognitive factors such as fear of pain and symptom-related anxiety play an important role in chronic pain states. The current study sought to characterize abnormalities in preparatory brain response before aversive pelvic visceral distention in irritable bowel syndrome (IBS) patients and their possible relationship to the consequences of distention. The brain functional magnetic resonance imaging (fMRI) blood oxygen level-dependent (BOLD) response to anticipated and delivered mild and moderate rectal distention was recorded from 14 female IBS patients and 12 healthy controls. During cued anticipation of distention, activity decreased in the insula, supragenual anterior cingulate cortex (sACC), amygdala, and dorsal brainstem (DBS) of controls. IBS patients showed less anticipatory inactivation. Group differences were significant in the right posterior insula and bilateral DBS. Self-rated measures of negative affect during scanning were higher in patients than controls (p < 0.001), and the anticipatory BOLD decreases in DBS were inversely correlated with these ratings. During subsequent distention, both groups showed activity increases in insula, dorsal ACC, and DBS and decreases in the infragenual ACC. The increases were more extensive in patients, producing significant group differences in dorsal ACC and DBS. The amplitude of the anticipatory decrease in the pontine portion of DBS was associated with greater activation during distention in right orbitofrontal cortex and bilateral sACC. Both regions have been associated previously with corticolimbic inhibition and cognitive coping. Deficits in preparatory inhibition of DBS, including the locus ceruleus complex and parabrachial nuclei, may interfere with descending corticolimbic inhibition and contribute to enhanced brain responsiveness and perceptual sensitivity to visceral stimuli in IBS.

Key words: fMRI; brainstem; irritable bowel syndrome; anticipation; pain; corticolimbic inhibition

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Received June 1, 2007; revised Oct. 3, 2007; accepted Oct. 20, 2007.

Correspondence should be addressed to Dr. Emeran A. Mayer, Center for Neurovisceral Sciences and Women's Health, Veterans Affairs Greater Los Angeles Healthcare System, Building 115, Room 223, 11301 Wilshire Blvd, Los Angeles, CA 90073. Email: emayer{at}ucla.edu

Related articles in J. Neurosci.:

Anticipatory Brain Activity in Irritable Bowel Syndrome

Jerry Chen and Udi Blankstein
J. Neurosci. 2008 28: 4113-4114. [Full Text]  

This article has been cited by other articles:

				J. Chen and U. Blankstein Anticipatory Brain Activity in Irritable Bowel Syndrome J. Neurosci., April 16, 2008; 28(16): 4113 - 4114. [Full Text] [PDF]

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