Abstract
During food consumption the brain integrates multiple interrelated neural and hormonal signals involved in the regulation of food intake. Factors influencing the decision to stop eating include the foods' sensory properties, macronutrient content, and volume, which in turn affect gastric distention and appetite hormone responses. So far, the contributions of gastric distention and oral stimulation by food on brain activation have not been studied. The primary objective of this study was to assess the effect of gastric distention with an intra-gastric load and the additional effect of oral stimulation on brain activity after food administration. Our secondary objective was to study the correlations between hormone responses and appetite-related ratings and brain activation. Fourteen men completed three functional magnetic resonance imaging sessions during which they either received a naso-gastric infusion of water (stomach distention), naso-gastric infusion of chocolate milk (stomach distention + nutrients), or ingested chocolate-milk (stomach distention + nutrients + oral exposure). Appetite ratings and blood parameters were measured at several time points. During gastric infusion, brain activation was observed in the midbrain, amygdala, hypothalamus, and hippocampus for both chocolate milk and water, i.e., irrespective of nutrient content. The thalamus, amygdala, putamen and precuneus were activated more after ingestion than after gastric infusion of chocolate milk, whereas infusion evoked greater activation in the hippocampus and anterior cingulate. Moreover, areas involved in gustation and reward were activated more after oral stimulation. Only insulin responses following naso-gastric infusion of chocolate milk correlated with brain activation, namely in the putamen and insula. In conclusion, we show that normal (oral) food ingestion evokes greater activation than gastric infusion in stomach distention and food intake-related brain areas. This provides neural evidence for the importance of sensory stimulation in the process of satiation.Trial RegistrationClinicalTrials.gov NCT01644539.
Highlights
Obesity prevalence has increased dramatically the last decades [1], as a result of overconsumption [2]
When food enters the stomach, neural signals from the gastrointestinal tract travel via the vagus nerve to the brainstem and thalamus, which projects to the rest of the brain in particular the hypothalamus, amygdala and primary sensory cortices [22]
We have no valid data of the brain activity during ingestion of chocolate milk, due to movement artefacts associated with swallowing
Summary
Obesity prevalence has increased dramatically the last decades [1], as a result of overconsumption [2]. Satiation refers to the process which leads to meal termination [3]. It is a complex process which is determined by many different factors, including the foods’ sensory properties, macronutrient content, and volume, which influence hormone levels and gastric distention [4]. Satiety is the ensuing state of satisfaction after the meal and is related to the post-ingestive consequences of consumption, such as digestion and hormone signaling. Gastric [5,6] as well as oral [7,8,9,10] stimulation contribute separately and in conjunction with meal termination [11]. Higher viscosity leads to decreased intake [12], and increased oro-sensory exposure can lower the intake of sweet drinks [13]
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