The effects of overfeeding on the neuronal response to visual food cues in thin and reduced-obese individuals

Abstract

Background: The regulation of energy intake is a complex process involving the integration of homeostatic signals and both internal and external sensory inputs. The objective of this study was to examine the effects of short-term overfeeding on the neuronal response to food-related visual stimuli in individuals prone and resistant to weight gain.

Methodology/principal findings: 22 thin and 19 reduced-obese (RO) individuals were studied. Functional magnetic resonance imaging (fMRI) was performed in the fasted state after two days of eucaloric energy intake and after two days of 30% overfeeding in a counterbalanced design. fMRI was performed while subjects viewed images of foods of high hedonic value and neutral non-food objects. In the eucaloric state, food as compared to non-food images elicited significantly greater activation of insula and inferior visual cortex in thin as compared to RO individuals. Two days of overfeeding led to significant attenuation of not only insula and visual cortex responses but also of hypothalamus response in thin as compared to RO individuals.

Conclusions/significance: These findings emphasize the important role of food-related visual cues in ingestive behavior and suggest that there are important phenotypic differences in the interactions between external visual sensory inputs, energy balance status, and brain regions involved in the regulation of energy intake. Furthermore, alterations in the neuronal response to food cues may relate to the propensity to gain weight.

Figure 1. Neuronal response to visual foods cues in thin individuals in the eucaloric state.

The neuronal response in thin individuals to visual stimuli of foods of high hedonic value as compared to non-food objects in the eucaloric state is shown (EU:H>O). Robust activation is observed in the insula, sensory cortex, posterior cingulate, ventral striatum, posterior hippocampus, parietal cortex, and inferior temporal visual cortex. Statistical maps thresholded at an FDR corrected threshold of q<0.05 and overlaid onto the group average anatomical image. Data are shown in the radiological convention (right hemisphere on the left).

Figure 2. Neuronal response in thin as compared to reduced-obese individuals.

The difference in neuronal response in thin as compared to reduced-obese individuals to foods of high hedonic value in the eucaloric state is shown (EU:Thin>RO:H>O). Greater activation of the insula and visual cortex is noted in thin as compared to reduced-obese individuals. Statistical maps thresholded at p<0.01 for visualization and overlaid onto the group average anatomical image. Data are shown in the radiological convention (right hemisphere on the left).

Figure 3. Effects of overfeeding on the neuronal response in thin as compared to reduced-obese individuals.

The difference in neuronal response with overfeeding as compared to eucaloric feeding in thin as compared to reduced-obese individuals in response to foods of high hedonic value is shown (EU>OF:Thin>OF:H>O). A. Greater deactivation of the insula, hypothalamus and visual cortex is noted in thin as compared to reduced-obese individuals. Statistical maps thresholded at p<0.01 for visualization and overlaid onto the group average anatomical image. Data are shown in the radiological convention (right hemisphere on the left). B. Mean BOLD responses (± SEM) are shown for the insula and hypothalamus.