Altered reward processing following sucrose bingeing in male and female mice

ABSTRACT

Objectives: Binge eating disorder (BED) is the most prevalent eating disorder associated with multiple adverse health effects, especially mental health issues, including substance use disorders and mood and anxiety disorders. Given these high comorbidities, the objective of our study was to examine whether bingeing behavior would lead to altered perception of reinforcing properties of EtOH and changes in well-being. Methods: We used a sucrose bingeing model based on an intermittent access paradigm with a two-bottle choice, without fasting, in male and female mice. We examined the effect of 2-week sucrose paradigm on ethanol-reinforcing properties using a conditioned place preference test (CPP). Well-being, anxiety- and depressive-like behavioral tests were performed to assess emotional state following 2 and 8-week sucrose bingeing paradigm. Results: Mice with intermittent access to sucrose developed a binge-like behavior assessed by higher sucrose intake and escalation rate during the 1st hour of access, in comparison with mice with a continuous sucrose access. We show for the first time that sucrose bingeing in mice modifies positive reinforcing effect of EtOH in a CPP paradigm without marked alteration of emotional state. Interestingly, prolonging sucrose access for 8 weeks revealed an exacerbated bingeing behavior in female mice, and some signs of emotional state alterations in female with continuous access. Discussion: In sum, our findings broaden the understanding of behavioral alterations associated with bingeing, highlighting the need to investigate addictive-like properties of palatable food both in male and female mice.

KEYWORDS:

• Binge eating
• sucrose
• CPP
• well-being
• emotional state
• sex
• ethanol
• reward

Acknowledgement

We are thankful to Audrey Faesser for her help in setting behavioral tests and to Victor Mathis for fruitful discussions.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

All the data supporting the findings of this study can be provided upon request from the corresponding author.

Additional information

Funding

This project was supported by the Université de Strasbourg, Centre National de la Recherche Scientifique (CNRS), Programme International de Cooperation Scientifique (PICS CNRS), the French National Research Agency (ANR) through the Programme d’Investissement d’Avenir (ANR- 17-EURE-0022, Euridol, Graduate school of pain),Institut National du Cancer and IReSP (Institut pour la Recherche en Santé Publique, IReSP/INCa-21-Addiction), and the Natural Sciences and Engineering Research Council of Canada (NSERC). Gaëlle Awad received a PhD fellowship from the French Ministère de l’Enseignement Supérieur et de la Recherche. Anne-Sophie Aubry received a PhD fellowhip from Euridol, Graduate school of pain.

Notes on contributors

Gaëlle Awad

Gaëlle Awad was a PhD student in the Laboratory of Neuroscience and Cognitives Adaptations (LNCA). She defended her PhD in 2022 and pursued as a post-doctoral fellow at the University of Lausanne in Switzerland, in Dr I Décosterd team (Centre Hospitalo Universitaire Vaudois, Department of Fundamental Neurosciences).

Anne-Sophie Aubry

Anne-Sophie Aubry was a PhD student in the Laboratory of Neuroscience and Cognitives Adaptations (LNCA). She defended her PhD in 2023 and is now working in Paris as a consultant in innovation financing.

Mary C. Olmstead

Mary C. Olmstead is a professor of psychology and neuroscience at Queen's University in Kingston, Canada. She completed her training at the University of Toronto (BSc), McGill University (MSc, PhD), and University of Cambridge UK (Postdoctoral Fellow).

Katia Befort

Katia Befort is a CNRS researcher at the University of Strasbourg, France. She completed her training at the University Louis Pasteur Strasbourg (MSc & PhD) and Harvard Medical School (Postdoctoral Fellow).