Interplay of spinal and vagal pathways on esophageal acid-related anterior cingulate cortex functional networks in rats. Am J Physiol Gastrointest Liver Physiol 2019 May 01;316(5):G615-G622
Date
03/01/2019Pubmed ID
30817181Pubmed Central ID
PMC6580238DOI
10.1152/ajpgi.00228.2018Scopus ID
2-s2.0-85065859796 (requires institutional sign-in at Scopus site) 3 CitationsAbstract
Esophageal acid sensory signals are transmitted by both vagal and spinal pathways to the cerebral cortex. The influence and interplay of these pathways on esophageal acid-related functional connectivity has been elusive. Our aim was to evaluate the esophageal acid exposure-related effect on the anterior cingulate cortex (ACC) functional connectivity networks using functional MRI-guided functional connectivity MRI (fcMRI) analysis. We studied six Sprague-Dawley rats for fcMRI experiments under dexmedetomidine hydrochloride anesthesia. Each rat was scanned for 6 min before and after esophageal hydrochloric acid infusion (0.1 N, 0.2 ml/min). The protocol was repeated before and after bilateral cervical vagotomy on the same rat. Seed-based fcMRI analysis was used to examine ACC networks and acid-induced network alterations. Three-factor repeated-measures ANOVA analysis among all four subgroups revealed that the interaction of acid infusion and bilateral vagotomy was mainly detected in the hypothalamus, insula, left secondary somatosensory cortex, left parietal cortex, and right thalamus in the left ACC network. In the right ACC network, this interaction effect was detected in the caudate putamen, insula, motor, primary somatosensory cortex, secondary somatosensory cortex, and thalamic regions. These regions in the ACC networks showed decreased intranetwork connectivity due to acid infusion. However, after bilateral vagotomy, intranetwork connectivity strength inversed and became stronger following postvagotomy acid infusion. Signals transmitted through both the vagal nerve and spinal nerves play a role in esophageal acid-related functional connectivity of the ACC. The vagal signals appear to dampen the acid sensation-related functional connectivity of the ACC networks. NEW & NOTEWORTHY These studies show that esophageal acid-induced brain functional connectivity changes are vagally mediated and suggest that signals transmitted through both the vagal nerve and spinal nerves play a role in esophageal acid-related functional connectivity of the anterior cingulate cortex. This paper focuses on the development of a novel rat functional MRI model fostering improved understanding of acid-related esophageal disorders.
Author List
Sanvanson P, Li Z, Mei L, Kounev V, Kern M, Ward BD, Medda B, Shaker RAuthors
Bidyut K. Medda PhD Associate Professor in the Medicine department at Medical College of WisconsinLing Mei MD Associate Professor in the Medicine department at Medical College of Wisconsin
Patrick P. Sanvanson MD Associate Professor in the Medicine department at Medical College of Wisconsin
Reza Shaker MD Assoc Provost, Sr Assoc Dean, Ctr Dir, Chief, Prof in the Medicine department at Medical College of Wisconsin
MESH terms used to index this publication - Major topics in bold
AnimalsBrain Mapping
Esophagus
Gyrus Cinguli
Hydrochloric Acid
Magnetic Resonance Imaging
Neural Pathways
Rats
Rats, Sprague-Dawley
Spinal Nerves
Vagotomy
Vagus Nerve