Expression of neural markers of gustatory signaling are differentially altered by continuous and intermittent feeding patterns
Introduction
The overconsumption of highly palatable, high fat foods has been linked to an increase in the prevalence of obesity and multiple studies propose that the timing or pattern in which these energy dense meals are consumed may contribute to weight gain and increase metabolic risks [1], [2], [3]. Eating patterns (e.g. how much, how often, macronutrient composition) are regulated by signals from the gustatory neural circuit, a complex neural network that begins at the tongue and continues to homeostatic and hedonic brain regions involved in feeding and reward. Taste is an important modulator of fat intake and fat preference and initiates a cascade of neural events that leads to changes in food intake [4], [5], [6], [7], [8]. Recent studies have demonstrated that expression levels of lingual fat sensors are related to obesity in clinical populations and animal models [7], [8], [9], [10], [11], [12]. Therefore, patterns of fat intake may affect the expression of lingual fat sensors, which in turn, may alter downstream neural targets and play a role in the preference for and consumption of dietary fat.
CD36 is a lingual fat sensor that regulates fat intake, is expressed primarily on the circumvallate papillae (CV) of the tongue and is considered the fat taste receptor [9], [13], [14], [15], [16], [17], [18], [19]. Studies investigating the role of lingual CD36 on fat intake and preference in models that differ in their susceptibility to develop obesity suggest that lingual CD36 mRNA expression is increased by short-term fat intake in obesity-prone rats, but that taste preference thresholds for linoleic acid are not altered, suggesting desensitization of the taste signal [13], [15], [18]. In another study, chronic consumption of a high fat diet (HFD) reduced CD36 mRNA expression levels compared to chow fed rats [20]. Overall, these studies suggest that dietary fat consumption leads to a dysregulation of fat sensing from the tongue and suggests that this dysregulation may alter the gustatory neural circuitry.
Lingual fat signaling via CD36 involves the regulation of serotonin (5-HT) in taste receptor cells and activation of gustatory afferent nerves [9]. Gustatory afferent nerves project to neural regions associated with eating behaviors, which are regulated by both homeostatic and hedonic mechanisms [21], [22], [23]. Studies suggest that a binge-like pattern of eating and obesity are consequences of overconsuming high fat, highly palatable foods and are due to a shift from homeostatic eating to hedonic, reward-driven eating [24], [25]. The goal of the current study was to investigate the short-term effects of multiple fat intake patterns on the expression of lingual markers of fat sensing and neural markers of homeostatic and hedonic eating.
Section snippets
Animals
Male Sprague-Dawley rats (8–10 weeks old) (Harlan/Envigo, Indianapolis, IN) were housed on a 12/12 h light/dark (on at 0700) cycle with food and water available ad libitum. Rats were randomly assigned to meal pattern condition. All procedures were approved by the LSU Health Sciences Center Institutional Animal Care and Use Committees.
Diet conditions
Animals were randomly divided into four groups. The Chow group (n = 14) received ad libitum access to standard lab chow. The Continuous group (n = 9) received ad
Results
Body weight was assessed weekly. Weight gain differed between groups (F = 3.1, p<.05) and rats in the Intermittent group gained the least amount of weight (Fig. 1A). Average daily kilocalories in the Daily and Intermittent groups were calculated from chow and vegetable shortening. Average daily food intake differed across groups (F = 13.9, p<.001; Fig. 1B). Rats fed HFD or given access to vegetable shortening consumed more kilocalories than Chow controls. Assessment of patterns of consumption
Discussion
The overconsumption of palatable high fat foods has been linked to an increase in the prevalence of obesity. Studies suggest that the meal timing or the pattern in which energy dense meals are consumed may contribute to weight gain and metabolic risks [1], [2], [3]. Food intake patterns (e.g. how much, how often, macronutrient composition) are regulated by signals from the gustatory neural circuit, a complex neural network that begins at the tongue and continues to homeostatic and hedonic brain
Acknowledgments
This research was supported by LSU Health Sciences Center to SDP. This work was partially supported by the Pennington/Louisiana NORC Center grant P30DK072476 and the COBRE center grant P30GM118430 from the National Institutes of Health.
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