Representation in the human brain of food texture and oral fat

Abstract

Important factors that influence food palatability are its texture and fat content. We investigated their representation in the human brain using event-related functional magnetic resonance imaging. It was shown that the viscosity of oral stimuli is represented in the (primary) taste cortex in the anterior insula, in which activation was proportional to the log of the viscosity of a cellulose stimulus (carboxymethyl cellulose), and was also produced by sucrose. Oral viscosity was also represented in a mid-insular region that was posterior to the taste cortex. Third, it was found that oral delivery of fatty vegetable oil activates both of these insular cortex regions, the hypothalamus, and the dorsal midanterior cingulate cortex. Fourth, it was found that the ventral anterior cingulate cortex, where it borders the medial orbitofrontal cortex, was activated by oral fat independently of its viscosity and was also activated by sucrose taste. This ventral anterior cingulate region thus represents two indicators of the energy content and palatability of foods. These are the first investigations of the oral sensory representation of food texture and fat in the human brain, and they start to reveal brain mechanisms that may be important in texture-related sensory properties of foods that make them palatable and that may accordingly play a role in the hedonic responses to foods, the control of food intake, and obesity.

Figure 1.

Brain areas where activation (as indicated by the BOLD signal) was correlated with stimulus viscosity. Top row, Left, Activations shown bilaterally in a midposterior region of the insular cortex. The sagittal slice shows the anteroposterior extent of the left hemisphere activation marked by the crosshairs. Top row, Right, Scatter plot showing the BOLD signal (percentage change) in this region with respect to viscosity produced by the CMC series. Bottom row, Left, Activations in the anterior insula. The sagittal slice shows the anteroposterior extent of the left hemisphere activation marked by the crosshairs. Bottom row, Right, Scatter plot showing the BOLD signal (percentage change) in this region as a function of oral viscosity produced by the CMC series. The image was thresholded at p < 0.001, uncorrected to show the extent of the activation. R, Right.

Figure 2.

Top, Anterior insula activation by (CMC at 1000 cP – control) and (sucrose – control), as revealed by conjunction analysis. The sagittal slice on the right shows the anteroposterior extent of this activation. Bottom, Average time courses (across trials and subjects) for CMC at 1000 cP and sucrose from the anterior insula voxel indicated by the crosshairs. The time course data reveal a robust response for both types of stimuli (i.e., unimodal oral somatosensory and unimodal taste) in this part of the human insula. The image was thresholded at p < 0.0001, uncorrected to show the extent of the activation. R, Right.

Figure 3.

Responses to the oral delivery of fat as assessed by the comparison (fat – control). Activations were observed in the mid-insula and hypothalamus (Hy) (top row, left), anterior insula (top row, middle), and anterior cingulate cortex (top row, right). The average time course data (across trials and subjects) from the mid-insular cortex (from the voxels marked by the crosshairs in the top row, left) are shown in the bottom row for the conditions fat and CMC at 50 cP. R, Right.

Figure 4.

Top, Rostral anterior cingulate cortex activation by (fat – control) and (sucrose – control), as revealed by conjunction analysis. Bottom, The corresponding average time course data (across trials and subjects) from the voxel marked by the crosshairs are shown.

Figure 5.

Activations correlating with stimulus fat content but independent of viscosity. Left, The main cluster of activation was observed in a rostral part of the anterior cingulate cortex, close to its transition zone with the medial orbitofrontal cortex. The parameter estimate for fat is 2.42 ± 0.92, for CMC at 50 cP is 1.6 ± 0.86, and for CMC at 1000 cP is –0.14 ± 0.31. Right, In a region of interest analysis, activations were also observed in the ventral part of the left striatum. The parameter estimate for fat is 1.13 ± 0.97, for CMC at 50 cP is 0.73 ± 0.62, and for CMC at 1000 cP is –0.13 ± 0.85. R, Right.