Roux-en-Y gastric bypass surgery changes food reward in rats

Abstract

Context: Roux-en-Y gastric bypass surgery (RYGB) is currently the most effective treatment for morbid obesity, and clinical studies suggest that RYGB patients change food preferences and the desire to eat.

Objective: To examine hedonic reactions to palatable foods and food choice behavior in an established rat model of RYGB.

Methods and design: Male Sprague-Dawley (SD) rats and selected line obesity-prone rats that were rendered obese on a high-fat diet underwent RYGB or sham surgery and were tested for 'liking' and 'wanting' of palatable foods at different caloric densities 4-6 months after surgery.

Results: Compared with sham-operated (obese) and age-matched lean control rats, RYGB rats of both models exhibited more positive orofacial responses to low concentrations of sucrose but fewer to high concentrations. These changes in 'liking' by RYGB rats were translated into a shift of the concentration-response curve in the brief access test, with more vigorous licking of low concentrations of sucrose and corn oil, but less licking of the highest concentrations. The changes in hedonic evaluation also resulted in lower long-term preference/acceptance of high-fat diets compared with sham-operated (obese) rats. Furthermore, the reduced 'wanting' of a palatable reward in the incentive runway seen in sham-operated obese SD rats was fully restored after RYGB to the level found in lean control rats.

Conclusions: The results suggest that RYGB leads to a shift in hedonic evaluation, favoring low over high calorie foods and restores obesity-induced alterations in 'liking' and 'wanting'. It remains to be determined whether these effects are simply due to weight loss or specific changes in gut-brain communication. Given the emerging evidence for modulation of cortico-limbic brain structures involved in reward mechanisms by gut hormones, RYGB-induced changes in the secretion of these hormones could potentially be mediating these effects.

Fig. 1

Body weight, body composition, and leptin levels after RYGB and sham surgery. A–C, G: Body weight (A), adiposity (B), percent lean mass (C), and plasma leptin levels (G), of outbred Sprague-Dawley rats with either Roux-en-Y gastric bypass surgery (RYGB, filled circles; n = 11) or sham surgery (sham, open circles; n = 11), and non-operated, chow-fed, lean controls (lean, open triangles; n = 10). Body weight in RYGB rats was significantly reduced at all time points after surgery compared with sham-operated controls, but was not significantly different from lean controls. D–F: Body weight (D), adiposity (E), and percent lean mass (F) of genetically select obesity-prone (CD–OP) rats with RYGB (n = 6) or sham-surgery (n = 5). Bars that do not share the same letter are significantly (P < 0.05) different from each other (based on ANOVA and Bonferroni adjusted multiple comparisons).

Fig. 2

Hedonic impact or ‘liking’ of sucrose as measured by the taste reactivity test. The number of positive hedonic reactions in response to tasting 3 different sucrose concentrations is shown. A: outbred Sprague-Dawley rats, either non-operated, chow-fed lean controls (lean, n = 9), sham-operated, obese (sham/obese, n = 11), or RYGB (n =11). B: Genetically select line of obesity-prone (CD–OP) rats, sham-operated, obese (n = 5), and RYGB (n = 5). Bars that do not share the same letter are significantly different from each other (p < 0.05, based on ANOVA and Bonferroni adjusted multiple comparisons).

Fig. 3

Motivation to obtain food or ‘wanting’ as measured in the incentive runway. Rats were required to run from a start box to a goal box where they were rewarded with a palatable treat (sweet tasting Fruit-Loops). A: Completion speed (based on time required to go from start to goal box) for non-operated, chow-fed lean controls (lean, n = 4), sham-operated, obese (sham/obese, n = 6), and RYGB (n = 4) outbred Sprague-Dawley rats. Completion speed (‘wanting’) is significantly suppressed in obese rats with sham-surgery compared with both RYGB (* p < 0.05) and lean rats (# p < 0.05). B: Net running speed is not different for the three groups. C: Obese, sham-operated rats spend significantly more time being distracted by latency to leave the start box, pauses, and reversals.

Fig. 4

Lickometer responding for different concentrations of sucrose (A,C) and corn oil (B,D) as a measure of combined taste-guided ‘liking’ and low-effort ‘wanting’. The number of licks/10s was measured in series of ascending concentrations of sucrose solutions and corn oil emulsions. A,B: Outbred Sprague-Dawley rats with either Roux-en-Y gastric bypass surgery (RYGB, filled circles; n = 9) or sham surgery (sham, open circles; n = 11), and non-operated, chow-fed, lean controls (lean, open triangles; n = 7). C,D: Genetically select obesity-prone (CD–OP) rats with RYGB (n = 4) or sham-surgery (n = 4). *p < 0.05, RYGB compared with sham/obese and, # p < 0.05, lean compared with sham/obese rats, based on ANOVA and Bonferroni adjusted multiple comparisons.

Fig. 5

Food choice of sham-operated (Sham, n = 6) and RYGB (n = 4) outbred Sprague-Dawley rats, 8 months after surgery. Two-choice diet (chow and high-fat) was available throughout postsurgical period. A: Intake of calories from chow and high-fat diet measured during 3 consecutive days. B: Fat preference in percent of total intake. * P < 0.01, RYGB compared with sham/obese, based on t-test.