Elsevier

Neuroscience

Volume 139, Issue 3, 2006, Pages 813-820
Neuroscience

Behavioural neuroscience
Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response

https://doi.org/10.1016/j.neuroscience.2005.12.037Get rights and content

Abstract

Drinking a sugar solution on an intermittent schedule can promote sugar bingeing and cause signs of dependence while releasing dopamine repeatedly like a drug of abuse. It is hypothesized that sweet taste alone is sufficient for this effect in sucrose bingeing rats. On the theory that acetylcholine in the nucleus accumbens plays a role in satiety, it is further hypothesized that purging the stomach contents will delay acetylcholine release. Rats with gastric fistulas and nucleus accumbens guide shafts for microdialysis were fed 12 h each day. During the first hour, fistulas were open for the sham-feeding group and closed for the real-feeding group, and 10% sucrose was the only food source. For the remaining 11 h, liquid rodent diet was available as well as the 10% sucrose to provide a balanced diet. In microdialysis tests during the first sugar meal on days 1, 2 and 21, extracellular dopamine increased at least 30% each day in both groups. Acetylcholine also increased during the sugar meals for the real-feeding animals, but not during sham feeding. In conclusion, the taste of sugar can increase extracellular dopamine in the nucleus accumbens without fail in animals on a dietary regimen that causes bingeing and sugar dependency. During sham feeding, the acetylcholine satiation signal is eliminated, and the animals drink more. These findings support the hypothesis that dopamine is released repeatedly in response to taste when bingeing on sweet food, and the acetylcholine satiety effect is greatly reduced by purging; this may be relevant to bulimia nervosa in humans.

Section snippets

Subjects

Male Sprague–Dawley rats weighing between 250 and 350 g were obtained from the Princeton University vivarium from a stock originating from Taconic Farms (Germantown, NY, USA). The rats were housed individually on a reversed 12-h light/dark cycle with ad libitum access to water and LabDiet rodent chow (PMI Nutrition International, St. Louis, MO, USA) prior to surgery. All procedures were carried out in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory

Daily intake of sucrose escalates more during sham feeding than real feeding

Both groups of rats had daily, 12-h access to sucrose, and both significantly escalated their intake over the course of the experiment (F(17,170)=5.0, P<0.01, data from the 18 days that microdialysis was not conducted). Rats that sham fed for the first hour each day consumed larger amounts of sucrose in the first hour than the real-feeding rats (group effect: F(1,90)=167.7, P<0.01). Fig. 1 shows the sucrose intakes for 1 h during microdialysis on days 1, 2 and 21. Post hoc analyses show there

Accumbens DA and bingeing

The repeated increase in extracellular DA that occurred in the NAc during sham feeding suggests that taste alone can be sufficient to release DA in sucrose-bingeing rats. This finding, coupled with previous work (Hoebel et al 1999, Colantuoni et al 2001, Colantuoni et al 2002, Avena and Hoebel 2003, Avena et al 2004, Avena et al 2005, Spangler et al 2004, Rada et al 2005), supports the theory that repeated, excessive sugar bingeing produces a neural process qualitatively like that caused by

Conclusions

The present results show that both sham feeding and real feeding by sugar-dependent rats cause extracellular DA to increase in the NAc. This increase in DA release occurs repeatedly in association with intake of a palatable solution and resembles the pattern of persistent DA release, albeit smaller in magnitude, seen after administration of most drugs of abuse. This suggests that intermittent, short-term food deprivation, combined with recurrent DA release due to the taste of sweet food, might

Acknowledegments

Appreciation is extended to Dr. Nori Geary for training in the fistula technique and to Maida Rada for microdialysis probes. This research was supported by USPHS grant MH-65024 and DA-016458 (fellowship to N.M.A.). Abstracts of this work have been presented previously (Society for Neuroscience Annual Meeting 2003 Program No. 929.2, International Behavioral Neuroscience Society Annual Meeting 2004, and Society for the Study of Ingestive Behavior Annual Meeting 2004).

References (38)

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