Multimodal perception of sugar modulates cerebral blood flow in the hedonic circuit differently than independent oral or intestinal perception - Archive ouverte HAL Accéder directement au contenu
Communication Dans Un Congrès Année : 2016

Multimodal perception of sugar modulates cerebral blood flow in the hedonic circuit differently than independent oral or intestinal perception

Résumé

Objectives: The characterization of brain networks contributing to the processing of oral and/or intestinal sugar signals in a relevant animal model might help to understand the neural mechanisms related to the control of food intake inhumans and suggest potential causes for impaired eating behaviours. The aims of this study were 1) to investigate whether the combination or dissociation between oral and post-oral sucrose perception influence the brain activity in reward-related brain structures, and 2) to determine whether duodenal infusion of sucrose in the absence of sweet taste, and conversely, induce specific activity in the brain reward circuit. Methods: Seven growing pigs underwent four brain single photon emission computed tomography to assess cerebral bloodflow (CBF) modifications further to oral stimulation with neutral or sucrose artificial saliva paired with saline or sucrose infusion in the duodenum. For each brain imaging session, animals were anaesthetised after an overnight fasting and the injection of 99Tc-HMPAO (740 MBq) was synchronized with the oral stimulation, 50 min after the duodenal infusion (timeline corresponding to the peak of glycemia after sucrose duodenal infusion). CBF changes were investigated via SVC analyses using SPM8 in several regions of interest including cortical and subcortical areas of the hedonic/limbic circuit. An uncorrected value of P=0.01 was set as threshold for the clusters’ peak and clusters comprising a minimum of 25 contiguous voxels were considered significant. Results: Oral and/or duodenal sucrose sensing induced differential CBF changes in brain regions known to be involved in memory, reward processes and hedonic (i.e. pleasure) evaluation of sensory stimuli, including the dorsal striatum,prefrontal cortex, cingulate cortex, insular cortex, hippocampus, and parahippocampus cortex. Sucrose duodenal infusion only and combined sucrose stimulation induced similar activity patterns in the putamen, ventral anterior cingulate cortex and hippocampus. Some brain deactivations in the prefrontal and insular cortices were onlydetected in the presence of oral sucrose stimulation.Finally, activation of the right insular cortex was only induced by combined oral and duodenal sucrose stimulation, while specific activity patterns were detected in the hippocampus and parahippocampal cortex with oral sucrose dissociated from caloric load. Conclusions: We demonstrated that oral, duodenal and the bimodal perception of sucrose induced different patterns of brain metabolism in structures involved in memory, reward processes and hedonic evaluation of sensory stimuli. Using controlled conditions in a pertinent animal model for human nutrition and nutrient sensing, we managed to demonstrate that some CBF changes are specific to oralor duodenal sucrose sensing, and that bimodal sucrose stimulation can even have a synergetic effect in some brain areas. We identified brain areas that are probably involved in the congruence between the sweet oral perceptionand internal state. All these results have important implications for discussions related to caloric vs. non-caloric sweeteners consumption and impact of sugars on the brain hedonic circuits and motivational processes.

Dates et versions

hal-01527063 , version 1 (23-05-2017)

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Citer

David Val-Laillet, Caroline Clouard, Marie-Christine Meunier-Salaün, Paul Meurice, Charles-Henri Malbert. Multimodal perception of sugar modulates cerebral blood flow in the hedonic circuit differently than independent oral or intestinal perception. 27th International Symposium on Cerebral Blood Flow, Metabolism and Function / 12th International Conference on Quantification of Brain Function with PET, Jun 2015, Vancouver, Canada. ⟨10.1177/0271678X16639009⟩. ⟨hal-01527063⟩
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