The sum of its parts--effects of gastric distention, nutrient content and sensory stimulation on brain activation

PLoS One. 2014 Mar 10;9(3):e90872. doi: 10.1371/journal.pone.0090872. eCollection 2014.

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 registration: ClinicalTrials.gov NCT01644539.

Publication types

  • Randomized Controlled Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Weight
  • Brain / physiology*
  • Brain Mapping*
  • Gastric Dilatation / metabolism*
  • Hormones / metabolism
  • Humans
  • Infusion Pumps
  • Insulin / metabolism
  • Male
  • Milk
  • Physical Stimulation
  • Sensation*
  • Water
  • Young Adult

Substances

  • Hormones
  • Insulin
  • Water

Associated data

  • ClinicalTrials.gov/NCT01644539

Grant support

This work was financed by the Dutch Technology Foundation STW (http://www.stw.nl/en/) under grant nr. 07438. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.