Gastric-brain coupling dynamics in response to a cognitive challenge reveal distinct autonomic and psychological correlates in healthy individuals and patients with irritable bowel syndrome
Jeanne, R.; Minjoz, S.; Bonaz, B.; Sinniger, V.; Hot, P.; Kibleur, A.; Pellissier, S.
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The gastrics intrinsic slow-wave rhythm couples to ongoing cortical activity in humans, but the functional significance of this gastric-brain coupling remains poorly understood. Using simultaneous electroencephalography and electrogastrography, we examined how gastric-brain coupling changes during a mental task and subsequent recovery and whether these dynamics relate to autonomic responses in healthy adults (HA) and individuals with Irritable Bowel Syndrome (IBS), a disorder of gut-brain interactions. In HA, gastric-brain coupling decreased during mental task and gradually returned to baseline during recovery, primarily for cortical alpha rhythms. Greater reductions in gastric-brain coupling were associated with stronger sympathetic arousal, indicating that gastric-brain coupling is associated with physiological responses to cognitive demand. In IBS, gastric-brain coupling dynamics were preserved. However, unlike HA, sympathetic arousal was not associated with gastric-brain coupling reductions, suggesting an alteration in the functional relationship between gastric-brain coupling and autonomic regulation despite preserved coupling dynamics. Further, in HA, greater reductions in gastric-brain coupling were associated with higher anxiety and neuroticism and lower interoceptive awareness. In contrast, these relationships were reversed in IBS, with greater gastric-brain coupling dynamics observed in individuals with higher anxiety and neuroticism and lower interoceptive awareness. Together, gastric-brain coupling emerges as a dynamic physiological process associated with autonomic responses to cognitive demand. In IBS, these dynamics are preserved but their physiological and psychological associations are altered, indicating a dissociation between gastric-brain coupling and its functional correlates. Significance StatementThe functional role of gastric-brain coupling remains largely unknown. We show that coupling between the gastrics intrinsic slow-wave rhythm and cortical activity is dynamically reduced during mental engagement and recovers afterward, primarily through alpha rhythms. In healthy adults, these changes follow sympathetic arousal, linking gastric-brain coupling to autonomic responses to cognitive demands. In irritable bowel syndrome, coupling dynamics remain intact but lose their relationship with autonomic responses and show altered associations with anxiety, neuroticism, and interoceptive awareness. These findings suggest that gastric-brain coupling contributes to the physiological organization of brain-body states and that irritable bowel syndrome may involve altered functional interpretation of visceral signals despite preserved gastric-brain coupling dynamics.
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