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Modulation of Activity in Swallowing Motor Cortex Following Esophageal Acidification: A Functional Magnetic Resonance Imaging Study

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Abstract

Esophageal acid exposure induces sensory and motility changes in the upper gastrointestinal tract; however, the mechanisms involved and the effects on activity in the brain regions that control swallowing are unknown. The aim of this study was to examine functional changes in the cortical swallowing network as a result of esophageal acidification using functional magnetic resonance imaging (fMRI). Seven healthy volunteers (3 female, age range = 20–30 years) were randomized to receive either a 0.1 M hydrochloric acid or (control) saline infusion for 30 min into the distal esophagus. Postinfusion, subjects underwent four 8 min blocks of fMRI over 1 h. These alternated between 1 min swallowing water boluses and 1 min rest. Three-dimensional cluster analysis for group brain activation during swallowing was performed together with repeated-measures ANOVA for differences between acid and saline. After acid infusion, swallowing-induced activation was seen predominantly in postcentral gyrus (p < 0.004). ANOVA comparison of acid with saline showed a significant relative reduction in activation during swallowing of the precentral gyrus (M1) BA 4 (p < 0.008) in response to acid infusion. No areas of increased cortical activation were identified with acid vs. saline during swallowing. Esophageal acidification inhibits motor and association cortical areas during a swallowing task, probably via changes in vagal afferent or nociceptive input from the esophagus. This mechanism may play a protective role, facilitating acid clearance by reduced descending central motor inhibition of enteric/spinal reflexes, or by preventing further ingestion of injurious agents.

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Acknowledgments

P. Paine was funded by the Wellcome Trust (UK). The authors thank the MR radiography staff for their invaluable assistance.

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Authors and Affiliations

  1. GI Sciences, University of Manchester, Manchester, UK

    Peter A. Paine, Shaheen Hamdy & Qasim Aziz

  2. Translational Imaging Unit, University of Manchester, Manchester, UK

    Lloyd J. Gregory & Steve Williams

  3. Institute of Psychiatry, London, UK

    Xavier Chitnis, Vincent Giampietro & Mick Brammer

  4. Department of Gastrointestinal Sciences, University of Manchester, Clinical Sciences Building, Hope Hospital, Eccles Old Road, Salford, M6 8HD, UK

    Peter A. Paine

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  1. Peter A. Paine
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  2. Shaheen Hamdy
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  3. Xavier Chitnis
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Correspondence to Peter A. Paine.

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Studies were performed in the Department of GI Sciences and Translational Imaging Unit, University of Manchester, UK

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Paine, P.A., Hamdy, S., Chitnis, X. et al. Modulation of Activity in Swallowing Motor Cortex Following Esophageal Acidification: A Functional Magnetic Resonance Imaging Study. Dysphagia 23, 146–154 (2008). https://doi.org/10.1007/s00455-007-9114-3

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  • DOI: https://doi.org/10.1007/s00455-007-9114-3

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