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

Maartje S Spetter, Cees de Graaf, Monica Mars, Max A Viergever, Paul A M Smeets, Maartje S Spetter, Cees de Graaf, Monica Mars, Max A Viergever, Paul A M Smeets

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.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Experimental design.
Figure 1. Experimental design.
A: Flow diagram. B: Timeline of events during one fMRI run (total duration 35 min). Every block represents one 4.5-min time bin. At all illustrated time points (t = min) blood was drawn and fullness, desire to eat and anxiety were rated.*During this time bin chocolate milk was infused or ingested, or water was infused.
Figure 2. Effect of gastric infusion of…
Figure 2. Effect of gastric infusion of water and chocolate milk on brain activity compared to baseline.
Left panel: T-map of the increased response to chocolate milk and water infusion versus baseline overlaid onto the mean anatomical scan, thresholded at P

Figure 3. Changes in brain activity after…

Figure 3. Changes in brain activity after treatment for the three conditions. Left panel: T-map…

Figure 3. Changes in brain activity after treatment for the three conditions. Left panel: T-map of the increased response to oral chocolate milk stimulation after administration versus baseline overlaid onto the mean anatomical scan, thresholded at P
Right panel: Mean parameter estimates (a.u. ± SEM) over time from selected significant clusters. Area under the curve was greater for the oral condition in all brain areas, and for the control condition in the putamen (all P

Figure 4. Correlation between fullness and insulin…

Figure 4. Correlation between fullness and insulin changes (from baseline) and changes in brain activity…

Figure 4. Correlation between fullness and insulin changes (from baseline) and changes in brain activity in corresponding time bins during the gastric condition (n = 14, 5 time bins per subject, T-maps are thresholded at P
Left pane: T-map of selected significant correlations overlaid onto the mean anatomical scan. A: Correlation T-map and scatter plot showing the parameter estimates of the ACC peak voxel at MNI (−6, −16, 30) against fullness changes. B: Correlation T-map and scatter plot showing the parameter estimates of the putamen peak voxel (34, 0, 6) against insulin changes. C: Correlation T-map and scatter plot of the parameter estimates of the insula peak voxel at MNI (−38, 0, 2) plotted against insulin changes.
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References
    1. World Health Organization (2000) Obesity: preventing and managing the global epidemic. World Health Organ Tech Rep Ser 894: 1–253. - PubMed
    1. Westerterp KR (2010) Physical activity, food intake, and body weight regulation: insights from doubly labeled water studies. Nutr Rev 68: 148–154. - PubMed
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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.
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Figure 3. Changes in brain activity after…
Figure 3. Changes in brain activity after treatment for the three conditions. Left panel: T-map of the increased response to oral chocolate milk stimulation after administration versus baseline overlaid onto the mean anatomical scan, thresholded at P
Right panel: Mean parameter estimates (a.u. ± SEM) over time from selected significant clusters. Area under the curve was greater for the oral condition in all brain areas, and for the control condition in the putamen (all P

Figure 4. Correlation between fullness and insulin…

Figure 4. Correlation between fullness and insulin changes (from baseline) and changes in brain activity…

Figure 4. Correlation between fullness and insulin changes (from baseline) and changes in brain activity in corresponding time bins during the gastric condition (n = 14, 5 time bins per subject, T-maps are thresholded at P
Left pane: T-map of selected significant correlations overlaid onto the mean anatomical scan. A: Correlation T-map and scatter plot showing the parameter estimates of the ACC peak voxel at MNI (−6, −16, 30) against fullness changes. B: Correlation T-map and scatter plot showing the parameter estimates of the putamen peak voxel (34, 0, 6) against insulin changes. C: Correlation T-map and scatter plot of the parameter estimates of the insula peak voxel at MNI (−38, 0, 2) plotted against insulin changes.
Figure 4. Correlation between fullness and insulin…
Figure 4. Correlation between fullness and insulin changes (from baseline) and changes in brain activity in corresponding time bins during the gastric condition (n = 14, 5 time bins per subject, T-maps are thresholded at P
Left pane: T-map of selected significant correlations overlaid onto the mean anatomical scan. A: Correlation T-map and scatter plot showing the parameter estimates of the ACC peak voxel at MNI (−6, −16, 30) against fullness changes. B: Correlation T-map and scatter plot showing the parameter estimates of the putamen peak voxel (34, 0, 6) against insulin changes. C: Correlation T-map and scatter plot of the parameter estimates of the insula peak voxel at MNI (−38, 0, 2) plotted against insulin changes.

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