Elsevier

Neuroscience

Volume 156, Issue 4, 28 October 2008, Pages 865-871
Neuroscience

Behavioural neuroscience
Underweight rats have enhanced dopamine release and blunted acetylcholine response in the nucleus accumbens while bingeing on sucrose

https://doi.org/10.1016/j.neuroscience.2008.08.017Get rights and content

Abstract

The present study tested whether rats release more accumbens dopamine (DA) during a sugar binge when they are underweight vs. normal weight. Since acetylcholine (ACh) in the nucleus accumbens (NAc) normally increases as a meal progresses and satiety ensues, we also tested whether ACh release is altered when an animal has lost weight. Rats were maintained on daily 8-h access to chow, with 10% sucrose solution available for the first 2 h. Microdialysis performed on day 21, at normal body weight, revealed an increase in extracellular DA to 122% of baseline in response to drinking sucrose. Extracellular ACh peaked at the end of the meal. Next, the rats were food and sucrose restricted so that by day 28 they were at 85% body weight. When retested, these animals released significantly more DA when drinking sucrose (179%), but ACh release failed to rise. A control group was tested in the same manner but given sugar only on days 1, 21 and 28. At normal body weight, control animals showed a non-significant rise in DA when drinking sucrose on day 21. On day 28, at 85% body weight, the controls showed a small increase (124%) in DA release; however, this was significantly lower than the 179% observed in the underweight rats with daily sugar access. These findings suggest that when an animal binges on sugar and then loses weight, the binge releases significantly more DA and less ACh than when animals are at a normal body weight.

Section snippets

Subjects and surgery

Male Sprague–Dawley rats (300–325 g) were obtained from Taconic Farms (Germantown, NY, USA) and housed individually on a reversed 12-h light/dark cycle. All procedures were approved by the Princeton University Institutional Animal Care and Use Committee and conformed to the National Institutes of Health guidelines on the ethical use of animals. Efforts were made to minimize the use of animals and their suffering. Water was continuously available except during the microdialysis tests.

All rats

DA release is enhanced by body-weight reduction in sugar-bingeing rats

At a normal body weight, rats with 2-h access to sugar every day increased their intake during the 21 days (F(20,230)=6.02, P<0.001, Fig. 1), and by day 21 they consumed significantly more than the control group that had access only on days 1 and 21 (t(16)=4.84, P<0.001; 16.2±1.5 kcal vs. 3.9±1 kcal, respectively).

Basal DA levels were as follows: 2-h daily sugar group at normal body weight (day 21)=0.75±0.18 fmol; 2-h daily sugar group at reduced body weight (day 28)=0.88±0.35 fmol; 2-h sugar

Sugar-induced DA release is enhanced in bingeing rats at a low body weight

The findings suggest that animals that binge eat a sugar solution, and then lose weight, show a greater percent increase in DA release in the NAc than at normal body weight, and more than non-bingeing animals at a low weight. In a prior study, when underweight rats were fed ordinary chow or given systemic amphetamine or morphine, enhanced DA release was not observed; however, when amphetamine was administered directly into the NAc, it did release significantly more DA, suggesting that vesicular

Conclusion

As reviewed elsewhere, it has been previously shown that sugar bingeing results in behaviors and neurochemical changes that are similar to those observed with drugs of abuse (Avena et al., 2008). The present findings suggest that in rats with a history of binge eating, access to a palatable food (sucrose) at a low body weight is associated with a simultaneous increase in DA and attenuated ACh release in the NAc. This may make the effect of sugar more like a substance of abuse. Binge eating on

Acknowledgments

This research was supported by MH-65024 (to B. T. Walsh at NY Psychiatric Inst./Columbia Univ. and B.G.H. et al.), DA-10608 (to B.G.H.) and DA-16458 and DK-79793 (fellowships to N.M.A.). We thank Miriam Bocarsly and Jacqueline Sullivan for their assistance preparing the manuscript. The data presented here have been discussed in a review paper (Avena, 2007).

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