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Effects of Preceding Stimulation on Brain Activation in Response to Colonic Distention in Humans

Hamaguchi, Toyohiro PhD; Kano, Michiko MD, PhD; Kanazawa, Motoyori MD, PhD; Itoh, Masatoshi MD, PhD; Yanai, Kazuhiko MD, PhD; Fukudo, Shin MD, PhD

doi: 10.1097/PSY.0b013e3182926682
Special Series on Neuroscience in Health and Disease

Objective It has been suggested that the pattern of distension (moderate following mild and vice versa) might influence brain activation and the experience of hypersensitivity, offset analgesia, and anticipation. Nevertheless, how the pattern of stimulation affects sensitization and/or desensitization to visceral stimulation remains unknown.

Methods In 45 nonclinical healthy participants (12 women, 33 men; 20–26 years old), brain processing of visceral sensation induced by colonic distension was examined using H2 15O positron emission tomography. Subjective feelings regarding the stimuli were also measured. The descending colon was stimulated using six patterns of three bag pressures (0, 20, and 40 mm Hg). To evaluate the neural sensitization to visceral stimulation arising from the precedence effect, the effects of a 20- or 40-mm Hg distention after a sham or 20- or 40-mm Hg distension were analyzed using statistical parametric mapping. The level of significance was set at a voxelwise level of p < .0001, with cluster extent sizes of k > 50.

Results The midbrain, insula, and cerebellum, were more strongly activated by a 20-mm Hg distension with a preceding 40-mm Hg distention than by a 20-mm Hg distention without a preceding stimulation (p < .0001). Conversely, a sham stimulation after the experience of an intense stimulation activated the midcingulate cortex, compared with a sham stimulation without the experience of actual visceral stimulation (p < .0001).

Conclusions By directly comparing different patterns of visceral stimuli, preceding visceral stimuli may affect neural sensitization and/or desensitization in humans, including elevated midbrain, insula, and midcingulate cortex.

From the Departments of Behavioral Medicine (T.H., M.K., M.K., S.F.) and Pharmacology (K.Y.), Graduate School of Medicine, and Cyclotron Radio Isotope Center (M.I.), Tohoku University, Aoba, Sendai, Japan.

Address correspondence and reprint requests to Shin Fukudo, MD, PhD, Department of Behavioral Medicine, Graduate School of Medicine, Tohoku University, 2-1 Seiryo, Aoba, Sendai 980-8575, Japan. E-mail:

Received for publication December 21, 2011; revision received February 21, 2013.

Copyright © 2013 by American Psychosomatic Society
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