Abstract

Recent studies provide evidence that high-fat diets (HF) trigger both i) a deficit of reward responses linked to a decrease of mesolimbic dopaminergic activity, and ii) a disorganization of circadian feeding behavior that switch from a structured meal-based schedule to a continuous snacking, even during periods normally devoted to rest. This feeding pattern has been shown to be a cause of HF-induced overweight and obesity. Our hypothesis deals with the eventual link between the rewarding properties of food and the circadian distribution of meals. We have investigated the effect of circadian feeding pattern on reward circuits by means of the conditioned-place preference (CPP) paradigm and we have characterized the rewarding properties of natural (food) and artificial (cocaine) reinforcers both in free-feeding ad libitum HF mice and in HF animals submitted to a re-organized feeding schedule based on the standard feeding behavior displayed by mice feeding normal chow (“forced synchronization”). We demonstrate that i) ad libitum HF diet attenuates cocaine and food reward in the CPP protocol, and ii) forced synchronization of feeding prevents this reward deficit. Our study provides further evidence that the rewarding impact of food with low palatability is diminished in mice exposed to a high-fat diet and strongly suggest that the decreased sensitivity to chow as a positive reinforcer triggers a disorganized feeding pattern which might account for metabolic disorders leading to obesity.

Highlights

  • Feeding behavior is driven by energy demands, termed ‘‘homeostatic’’ feeding, and by the hedonic gratification associated with eating a preferred food, referred to as ‘‘nonhomeostatic’’ feeding [1]

  • Dietary treatment with high-fat diets reduces food reward in the conditioned-place preference To evaluate the effect of HF diets on the perception of food as a positive reinforcer, we compared CPP induced by non-caloric neutral food (Figure 3A) and chocolate krispies (Figure 3B) in control and HF mice

  • In the current study we demonstrate that HF diets diminish food and cocaine reward in mice and this behavioral impairment is not observed in animals forced to adhere to a standard meal-based feeding behavior (‘‘forced-synchronization’’)

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Summary

Introduction

Feeding behavior is driven by energy demands, termed ‘‘homeostatic’’ feeding, and by the hedonic gratification associated with eating a preferred food, referred to as ‘‘nonhomeostatic’’ feeding [1]. The hedonic value of food is thought to contribute to its reinforcing properties [2]; [3]. Eating a preferred food has been shown to serve as a tool to manage anxiety and/or stress [4]. Adiposity positively correlates with the preference for high-fat diets (HF) in obese individuals [5,6] and excessive consumption of palatable food leads to compulsive-like eating [7]. Other studies provide evidence that rats exposed to HF exhibit attenuated behaviors in response to both palatable food and amphetamine [8]

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