Roberta Sclocco1,2,3, Harrison Fisher1, Rowan Staley1,4, Kyungsun Han1,5, April Mendez4, Andrew Bolender1,4, Jaume Coll-Font6,7, Norman W Kettner2, Christopher Nguyen6,7,8, Braden Kuo4, Vitaly Napadow1,2,3. 1. Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital Radiology, Harvard Medical School, Charlestown, Massachusetts, USA. 2. Department of Radiology, Logan University, Chesterfield, Missouri, USA. 3. Scott Schoen and Nancy Adams Discovery Center for Recovery from Chronic Pain, Spaulding Rehabilitation Hospital, Charlestown, Massachusetts, USA. 4. Department of Gastroenterology and Center for Neurointestinal Health, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA. 5. Korean Institute of Oriental Medicine, Daejeon, South Korea. 6. Cardiovascular Research Center, Massachusetts General Hospital, Charlestown, Massachusetts, USA. 7. Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts, USA. 8. Division of Health Sciences and Technology, Harvard-Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
Abstract
BACKGROUND: Functional dyspepsia (FD) is a disorder of gut-brain interaction, and its putative pathophysiology involves dysregulation of gastric motility and central processing of gastric afference. The vagus nerve modulates gastric peristalsis and carries afferent sensory information to brainstem nuclei, specifically the nucleus tractus solitarii (NTS). Here, we combine MRI assessment of gastric kinematics with measures of NTS functional connectivity to the brain in patients with FD and healthy controls (HC), in order to elucidate how gut-brain axis communication is associated with FD pathophysiology. METHODS: Functional dyspepsia and HC subjects experienced serial gastric MRI and brain fMRI following ingestion of a food-based contrast meal. Gastric function indices estimated from 4D cine MRI data were compared between FD and HC groups using repeated measure ANOVA models, controlling for ingested volume. Brain connectivity of the NTS was contrasted between groups and associated with gastric function indices. KEY RESULTS: Propagation velocity of antral peristalsis was significantly lower in FD compared to HC. The brain network defined by NTS connectivity loaded most strongly onto the Default Mode Network, and more strongly onto the Frontoparietal Network in FD. FD also demonstrated higher NTS connectivity to insula, anterior cingulate and prefrontal cortices, and pre-supplementary motor area. NTS connectivity was linked to propagation velocity in HC, but not FD, whereas peristalsis frequency was linked with NTS connectivity in patients with FD. CONCLUSIONS & INFERENCES: Our multi-modal MRI approach revealed lower peristaltic propagation velocity linked to altered brainstem-cortical functional connectivity in patients suffering from FD suggesting specific plasticity in gut-brain communication.
BACKGROUND: Functional dyspepsia (FD) is a disorder of gut-brain interaction, and its putative pathophysiology involves dysregulation of gastric motility and central processing of gastric afference. The vagus nerve modulates gastric peristalsis and carries afferent sensory information to brainstem nuclei, specifically the nucleus tractus solitarii (NTS). Here, we combine MRI assessment of gastric kinematics with measures of NTS functional connectivity to the brain in patients with FD and healthy controls (HC), in order to elucidate how gut-brain axis communication is associated with FD pathophysiology. METHODS: Functional dyspepsia and HC subjects experienced serial gastric MRI and brain fMRI following ingestion of a food-based contrast meal. Gastric function indices estimated from 4D cine MRI data were compared between FD and HC groups using repeated measure ANOVA models, controlling for ingested volume. Brain connectivity of the NTS was contrasted between groups and associated with gastric function indices. KEY RESULTS: Propagation velocity of antral peristalsis was significantly lower in FD compared to HC. The brain network defined by NTS connectivity loaded most strongly onto the Default Mode Network, and more strongly onto the Frontoparietal Network in FD. FD also demonstrated higher NTS connectivity to insula, anterior cingulate and prefrontal cortices, and pre-supplementary motor area. NTS connectivity was linked to propagation velocity in HC, but not FD, whereas peristalsis frequency was linked with NTS connectivity in patients with FD. CONCLUSIONS & INFERENCES: Our multi-modal MRI approach revealed lower peristaltic propagation velocity linked to altered brainstem-cortical functional connectivity in patients suffering from FD suggesting specific plasticity in gut-brain communication.
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