Decreased caudate response to milkshake is associated with higher body mass index and greater impulsivity

Abstract

Previous investigations consistently report a negative association between body mass index (BMI) and response in the caudate nucleus during the consumption of palatable and energy dense food. Since this response has also been linked to weight gain, we sought to replicate this finding and determine if the reduced response is associated with measures of impulsivity or food reward. Two studies were conducted in which fMRI was used to measure brain response to milkshake and a tasteless control solution. In Study 1 (n=25) we also assessed self-reported impulsivity, willingness to work for food, and subjective experiences of the pleasantness of milkshake taste and aroma. Replicating prior work, we report a negative association between BMI and brain response to milkshake vs. tasteless in the caudate nucleus. The opposite pattern was observed in the ventral putamen, with greater response observed in the 13 overweight compared to the 12 healthy weight subjects. Regression of brain response against impulsivity and food reward measures revealed one significant association: in the overweight but not healthy weight group self-reported impulsivity was negatively associated with caudate response to milkshake. In Study 2 (n=14), in addition to assessing brain response to milkshake and tasteless solutions subjects completed a go/no-go task outside the scanner. As predicted, we identified an inverse relationship between caudate response to milkshake vs. tasteless and failure to inhibit responses on the no-go trials. We conclude that the inverse correlation between BMI and caudate response to milkshake is associated with impulsivity but not food reward. These findings suggest that response to milkshake in the dorsal striatum may be related to weight gain by promoting impulsive eating behavior.

Keywords: BIS-11; BMI; Caudate; Habit; Impulsivity; Reward.

Figure 1

The protocol/paradigm used for the scanning and mock session. The timeline depicts the series of events for the delivery of (A) FO+ / milkshake and (B) FO− / tasteless solution. Following the audible instructions “3, 2, 1, Sniff,” either the FO+ or FO− is delivered for three seconds. This is then followed by a 1–7 second rest period, and then either milkshake or tasteless solution, respectively. Another 1–7 second rest period precedes the delivery of a rinse. Finally, 4–11 seconds pass before the next trial.

Figure 2

Effect of BMI on response to milkshake vs. tasteless in the striatum. (A) Axial section showing that BMI is negatively correlated with activation in the right caudate nucleus to milkshake vs. tasteless. For this and all future figures, the SPM is thresholded at p > 0.005; k = 5. The color bar represents t-values. The scatter plot shows average parameter estimates (PE) extracted from the peak voxel (y axis) plotted against BMI (x-axis). (B) Graph showing the time course of BOLD response to milkshake (solid lines) and tasteless (dotted lines) for each of the groups (red = OW and blue = HW) extracted from the peak voxel isolated in the contrast of milkshake vs. tasteless in HW vs. OW. (C) Coronal sections and bar graphs depicting the opposing effect of BMI on response in the caudate and putamen. The left brain image shows significantly greater response in HW vs. OW in the right caudate nucleus whereas the right brain images show significantly greater response in OW vs. HW in the left putamen. Bar graphs show the average contrast estimate (CE) extracted from peak voxel in HW vs. OW.

Figure 3

Axial sections depicting the correlation of BIS-11 total and subscale scores with caudate activation to milkshake in the overweight group. (A) BIS-11 total score (bilateral), (B) motor impulsivity (BIS-2), and (C) non-planning impulsivity (BIS-3). All correlations are p<0.05, FDR-corrected. Color bars represent t-values. Scatterplots show parameter estimates (P.E. – y-axis) plotted against BIS-11 score (x-axis).

Figure 4

Axial sections depicting correlations between caudate activation to milkshake vs. tasteless and performance on the Go/No-Go Task in study 2. Scatter plots show that activation (P.E. = parameter estimates on the y - axis) in the caudate is positively correlated with accuracy rate (A), and negatively correlated with false alarm rate (B) on the x-axis. Both effects are significant at p<0.05, FDR-corrected. Color bars represent t-values.