Differential brain responses to gradual intragastric nutrient infusion and gastric balloon distension: A role for gut peptides?

Huynh Giao Ly, Patrick Dupont, Koen Van Laere, Inge Depoortere, Jan Tack, Lukas Van Oudenhove

Journal: NeuroImage 2018;144(Pt A):101-112

PMID: 27639359

Full Text on Elsevier Science View on PubMed

Abstract

BACKGROUND

Rapid gastric balloon distension to discomfort threshold activates the "pain neuromatrix" and deactivates exteroceptive sensory and "default mode network" regions. However, little is known about brain mechanisms underlying tolerance of meal-induced gastric distension. We aimed to directly compare brain responses to gradual balloon distension and intragastric nutrient infusion and to explore the role of differential gut peptide release in these responses.

MATERIALS AND METHODS

Brain responses to balloon- and nutrient-induced distension (to individually titrated pain or maximal satiation threshold) were measured in 15 healthy volunteers using HO-PET on 2 separate days in counterbalanced order. The effects of increasing gastric distension and plasma levels of ghrelin and peptide YY (PYY) on neural activity were assessed.

RESULTS

Balloon distension progressively activated pain-responsive regions and deactivated exteroceptive sensory and "default mode network" areas. During nutrient infusion, "pain neuromatrix" regions and the orbitofrontal cortex were progressively deactivated, while the midbrain was activated. Plasma levels of PYY and ghrelin increased and decreased, respectively, during nutrient infusion only; decreasing ghrelin levels correlated with increasing midbrain activity.

CONCLUSION

Different brain responses to gastric balloon distension and intragastric nutrient infusion are associated with nutrient-induced gut-brain signals, particularly to the midbrain, where these signals may interfere with both descending pain modulatory and mesolimbic reward processes. Deactivation of the "pain neuromatrix" during nutrient infusion may constitute the neurophysiological mechanism underlying the tolerance of normal meal volumes in health without induction of (painful) symptoms. Nutrient-induced deactivation of the orbitofrontal cortex may represent a key interoceptive meal termination signal.

Address: Laboratory for Brain-Gut Axis Studies (LABGAS), Translational Research Center for Gastrointestinal Disorders (TARGID), Department of Clinical and Experimental Medicine, University of Leuven, Leuven, Belgium. Electronic address: [email protected].; Laboratory for Cognitive Neurology, Division of Experimental Neurology, Department of Neurosciences, University of Leuven, Leuven, Belgium.; Division of Nuclear Medicine and Molecular Imaging, University Hospitals Leuven, Leuven, Belgium.; Laboratory for Brain-Gut Axis Studies (LABGAS), Translational Research Center for Gastrointestinal Disorders (TARGID), Department of Clinical and Experimental Medicine, University of Leuven, Leuven, Belgium.; Laboratory for Brain-Gut Axis Studies (LABGAS), Translational Research Center for Gastrointestinal Disorders (TARGID), Department of Clinical and Experimental Medicine, University of Leuven, Leuven, Belgium; Consultation-Liaison Psychiatry, University Psychiatric Centre KU Leuven, Campus Gasthuisberg, University of Leuven, Leuven, Belgium.

DOI: 10.1016/j.neuroimage.2016.09.032

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MeSH Terms: Adult, Brain Mapping, Cerebral Cortex, Female, Gastric Balloon, Ghrelin, Humans, Interoception, Male, Mesencephalon, Pain Perception, Peptide Fragments, Peptide YY, Positron-Emission Tomography, Satiation, Stomach, Young Adult