4.4 Article

Excessive coupling of the salience network with intrinsic neurocognitive brain networks during rectal distension in adolescents with irritable bowel syndrome: a preliminary report

Journal

NEUROGASTROENTEROLOGY AND MOTILITY
Volume 28, Issue 1, Pages 43-53

Publisher

WILEY-BLACKWELL
DOI: 10.1111/nmo.12695

Keywords

emotional arousal network; fMRI-guided functional connectivity analysis; homeostatic afferent processing network; irritable bowel syndrome; salience network

Funding

  1. Digestive Diseases Center, Medical College of Wisconsin
  2. National Institutes of Health (NIH) [R01GM103894, R01DK025731]
  3. NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES [R01DK025731] Funding Source: NIH RePORTER
  4. NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES [R01GM103894] Funding Source: NIH RePORTER

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BackgroundThe neural network mechanisms underlying visceral hypersensitivity in irritable bowel syndrome (IBS) are incompletely understood. It has been proposed that an intrinsic salience network plays an important role in chronic pain and IBS symptoms. Using neuroimaging, we examined brain responses to rectal distension in adolescent IBS patients, focusing on determining the alteration of salience network integrity in IBS and its functional implications in current theoretical frameworks. We hypothesized that (i) brain responses to visceral stimulation in adolescents are similar to those in adults, and (ii) IBS is associated with an altered salience network interaction with other neurocognitive networks, particularly the default mode network (DMN) and executive control network (ECN), as predicted by the theoretical models. MethodsIrritable bowel syndrome patients and controls received subliminal and liminal rectal distension during imaging. Stimulus-induced brain activations were determined. Salience network integrity was evaluated by the functional connectivity of its seed regions activated by rectal distension in the insular and cingulate cortices. Key ResultsCompared with controls, IBS patients demonstrated greater activation to rectal distension in neural structures of the homeostatic afferent and emotional arousal networks, especially the anterior cingulate and insular cortices. Greater brain responses to liminal vs subliminal distension were observed in both groups. Particularly, IBS is uniquely associated with an excessive coupling of the salience network with the DMN and ECN in their key frontal and parietal node areas. Conclusions & InferencesOur study provided consistent evidence supporting the theoretical predictions of altered salience network functioning as a neuropathological mechanism of IBS symptoms.

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