Long-lasting deficits in hedonic and nucleus accumbens reactivity to sweet rewards by sugar overconsumption during adolescence

• Published in: The European journal of neuroscience Vol. 43; no. 5; pp. 671 - 680
• Main Authors: Naneix, Fabien, Darlot, Florence, Coutureau, Etienne, Cador, Martine
• Format: Journal Article
• Language: English
• Published: France Blackwell Publishing Ltd 01-03-2016
• Subjects: Animals; c-Fos; Feeding Behavior; liking; limbic system; Male; Nucleus Accumbens - drug effects; Nucleus Accumbens - growth & development; Nucleus Accumbens - physiology; palatability; Proto-Oncogene Proteins c-fos - genetics; Proto-Oncogene Proteins c-fos - metabolism; rat; Rats; Rats, Wistar; Reward; Self Administration; Sucrose - administration & dosage; Sucrose - adverse effects; Taste Perception; c-Fos; liking; limbic system; rat; palatability
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.13149

Adolescence is a critical period characterized by major neurobiological changes. Chronic stimulation of the reward system might constitute an important factor in vulnerability to pathological development. In spite of the dramatic increase in the consumption of sweet palatable foods during adolescence in our modern societies, the long‐term consequences of such exposure on brain reward processing remain poorly understood. Here, we investigated in rats the long‐lasting effects of sugar overconsumption during their adolescence on their adult reactivity to the hedonic properties of sweet rewards. Adolescent rats with continuous access to 5% sucrose solution (from postnatal day 30–46) showed escalating intake. At adulthood (post‐natal day 70), using two‐bottle free choice tests, sucrose‐exposed rats showed lower intake than non‐exposed rats suggesting decreased sensitivity to the rewarding properties of sucrose. In Experiment 1, we tested their hedonic‐related orofacial reactions to intraoral infusion of tasty solutions. We showed that sucrose‐exposed rats presented less hedonic reactions in response to sweet tastes leaving the reactivity to water or quinine unaltered. Hence, in Experiment 2, we observed that this hedonic deficit is associated with lower c‐Fos expression levels in the nucleus accumbens, a brain region known to play a central role in hedonic processing. These findings demonstrate that a history of high sucrose intake during the critical period of adolescence induces long‐lasting deficits in hedonic treatment that may contribute to reward‐related disorders.
Adolescence is an important period of vulnerability to psychiatric diseases. Here we report that the overconsumption of sucrose during adolescence induces a decrease in the intake of sweet solutions and in orofacial hedonic reactions to sweet tastes at adulthood. This hedonic deficit is associated with lower c‐Fos levels in the nucleus accumbens demonstrating that sugar overconsmption during adolescence leads to long‐lasting alterations of reward‐related circuits.