Different regional brain activity during physiological gastric distension compared to balloon distension: a H215O-PET study

Abstract

Stepwise gastric balloon distension progressively activates a 'visceral pain neuromatrix', ultimately inducing discomfort and pain. On the other hand, normal meal ingestion requires gastric volume expansion without induction of pain. The aim was to test the hypothesis that physiological gastric distension (liquid meal infusion) until maximal satiation elicits brain responses similar to balloon distension at discomfort threshold. Brain H(2) (15) O-positron emission tomography (PET) was performed in two different groups of healthy volunteers (both n=14) during continuous and stepwise infusion of a liquid meal through a nasogastric tube, until maximal satiation. Brain (de)activation patterns were compared with historical controls in which discomfort was elicited using gastric balloon distension. This latter reference group was acquired on the same scanner using the same acquisition protocol; all data were analyzed using statistical parametric mapping (SPM2). Within each group, brain activity at maximal distension was compared to baseline activity and between-group comparisons were made. Intragastric volumes and satiation/gastric sensation scores at endpoint were similar in all groups. Continuous and stepwise nutrient infusion was associated with progressive deactivations in key areas of the 'visceral pain neuromatrix' that were activated during balloon distension. Additionally, stepwise infusion progressively activated prefrontal areas and showed deactivations in 'default network' brain regions also found to be deactivated during balloon distension. Compared to gastric balloon distension, physiological gastric distension using nutrient infusion elicits opposite brain responses in the 'visceral pain neuromatrix', but similar responses in other areas. We interpret this finding as a prerequisite for tolerance of normal meal volumes in health.