Elsevier

Physiology & Behavior

Volume 176, 1 July 2017, Pages 149-158
Physiology & Behavior

Diet choice patterns in rodents depend on novelty of the diet, exercise, species, and sex

https://doi.org/10.1016/j.physbeh.2017.02.045Get rights and content

Highlights

  • Wheel running induced diet avoidance is affected by species.

  • Diet novelty is critical for wheel running induced diet avoidance.

  • Wheel running reduced intake to a familiar HF diet in male and female rats.

  • Sex differences in diet choice were seen in sedentary and wheel running conditions.

Abstract

Prolonged consumption of a palatable, high fat (HF) diet paired with a lack of physical activity can exacerbate the development of obesity. Exercise can facilitate the maintenance of a healthy body weight, possibly though mediating changes in diet preference. Using a two-diet choice and wheel running (WR) paradigm, our laboratory previously demonstrated that WR induces HF diet avoidance with different persistency in male and female rats when HF diet and WR are introduced simultaneously. The aims of this study were to examine whether this behavior is species dependent and to what extent the novelty of the diet affects WR induced HF diet avoidance. Experiment 1 utilized male C57BL6 mice in a two-diet choice and WR paradigm. Results show that all mice preferred HF to chow diet regardless of exercise and the order in which exercise and HF diet were presented. Experiment 2A (diet novelty) utilized Sprague-Dawley rats that were first habituated to a 45% HF diet prior to the simultaneous introduction of WR and a novel high-carbohydrate, low-fat (DK) diet. All rats avoided the novel high-carbohydrate diet and neither male nor female wheel running rats exhibited reduction in HF diet intake or HF diet avoidance. After all rats were returned to a sedentary condition, female rats consumed significantly more of the DK diet than the male rats. In Experiment 2B (diet familiarity), rats remained sedentary and were re-habituated to the DK diet until intake stabilized. Subsequently, a 60% HF diet was introduced for all rats and for running rats, access to the running wheels were provided simultaneously. Consistent with our previous findings, HF diet intake and preference was significantly reduced in all wheel running rats. These data suggest that exercise induced HF diet avoidance is affected by species and the novelty of the diet.

Introduction

The lack of physical activity and increased consumption of palatable, calorie dense foods exacerbates the development of obesity, which is quickly becoming a global epidemic [26], [31], [38]. Regular adequate levels of exercise can be both preventive and therapeutic for multiple health issues [37], [56], [73], [76]. In humans, exercise can prevent the manifestation of comorbid conditions associated with obesity including Type II Diabetes Mellitus [12], [18], [33], [37], [47] by increasing insulin sensitivity and decreasing adiposity [18], [37]. In rats, acute wheel running (WR) leads to suppressed body weight gain and food intake [1], [14]. Rats with prolonged access to WR increase food intake but continue to maintain lower body weights compared to sedentary controls [68]. Furthermore, WR can prevent genetically [5], [6], [17], [50] and diet [24], [35], [36], [42], [43], [44], [53] induced obesity in both rats and mice. Taken together, these data indicate that exercise can facilitate the maintenance of a healthy body weight [12], [22], [26], [37], [56], [66], [75].

Data from the National Weight Control Registry found that individuals who are able to maintain weight loss  13.6 kg for at least one year engaged in regular physical activity and consumed diets low in calories and fat [8], [32], [62], [75]. The effects of exercise on palatable diet preference in rats parallel the human data. Studies using a two-diet choice WR paradigm (HF vs. chow) found that upon WR access, rats immediately decreased HF diet intake and preference regardless of the familiarity of the palatable diet [44], [59], [60], [61]. When WR and a novel HF diet are introduced at the same time, male rats completely avoided HF diet [49]. Here, avoidance is not simply the lack of preference for the palatable diet but rather the total lack of consumption of the palatable diet when presented with wheel running and diet choice simultaneously. These results demonstrate that exercise can affect energy balance through changes in diet choice and preference.

Previous studies have shown that WR can serve as an unconditioned stimulus (US) to induce conditioned taste aversion (CTA) in rats at a hunger or satiated state [40], [41]. One study revealed that during a two-diet choice test following CTA conditioning, wheel running rats exhibited CTA to the novel but not familiar diet [63]. This study indicates the significance of diet novelty in WR induced diet avoidance. Therefore, when WR and a novel HF diet are presented together, it is unclear whether complete HF diet avoidance occurred due to the novelty of the diet or if exercise specifically causes avoidance to palatable, energy dense foods such as a HF diet. Moreover, it is unknown whether running induced HF diet avoidance is species dependent because the two-diet choice and WR procedures have not been applied to other species.

Accordingly, the present study aimed to further examine the interaction between exercise and diet choice patterns in both mice and rats. Experiment 1 examined whether C57BL6 mice would display exercise-mediated changes in diet preference that are similar to what has been observed in rats. Experiment 2 tested to what extent the novelty of the diet affects diet avoidance and whether there are any sex differences. Experiment 2A (diet novelty) examined whether HF diet avoidance in male and female Sprague-Dawley rats would still occur when the novel diet that is simultaneously introduced with wheel running was no longer the palatable diet. Thus, rats were first habituated to the HF diet for 4 days after which WR was introduced simultaneously with a novel, non-palatable high-carbohydrate diet. Experiment 2B (diet familiarity) examined whether running induced reduction in HF diet intake and preference would occur when the rats were re-habituated to the high-carbohydrate diet and then placed on a two-diet choice (the high-carbohydrate diet vs. a somewhat familiar HF diet) feeding schedule.

Section snippets

Animals

Twenty male C57BL6 mice (The Jackson Laboratory, ME) weighing 20–25 g at age 7–8 weeks upon arrival were the subjects of this experiment. The mice were individually housed in polyethylene tubs on a 12 h light/dark cycle (lights on at 0600 h). During habituation, mice had ad libitum access to tap water and a standard Harlan diet (chow; 3.1 kcal/g, 58% carbohydrate, 24% protein, and 18% fat; Harlan 2018, Harlan Laboratories, USA). All experimental procedures were approved by the Institutional Animal

Experiment 1

During the 14-day diet choice period, SedHF, HF_WR, and WRHF mice expressed the same diet intake pattern (Fig. 3A–C). No group differences in chow or HF diet intakes were observed. Three-way repeated measures ANOVA indicated that all mice consumed significantly more HF than chow diet [effects of diet, time, and diet × time: F(1,17) = 1609.51, F(13,221) = 21.32, and F(13,221) = 2.45, all p < 0.005] regardless of group [F(2, 17) = 2.71, p = 0.095]. In other words, both sedentary and wheel running mice

Discussion

The present study examined whether wheel running induced HF diet avoidance also occurs in mice (Experiment 1) and whether this avoidance occurs towards novel diets in general or specifically to energy dense, palatable foods (Experiment 2). First, we found that wheel running C57BL6 mice preferred HF to chow diet during the two-diet choice and running period regardless of the different testing procedures. Accordingly, we concluded that wheel running induced HF diet avoidance differs among rats

Acknowledgments

We thank Dr. Timothy H. Moran for early discussion about this project. The corresponding author (N-C. L.) deeply appreciates Dr. Moran's excellent mentorship during her postdoctoral training. This study was supported by the UIUC Psychology Department startup funds (to N-C. L.) and the Klarman Family Foundation (to T.H.M.).

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      Similar to humans, mice fed high-fat food develop diet-induced obesity which can be mitigated by exercise from running [14–32]. Reduced weight gain is thought to be due to increased energy expenditure, based on measures of indirect calorimetry [15,17,21,22,27,28] and since energy intake from food increases [14–16,21,26,27,30,31,33] or stays the same [17,18,20,23,24,28,32,34] with exercise. Such studies also provide a model for investigating factors like leptin, glucose, or insulin which might underlie the benefits of exercise on food intake and body weight [17,24,27,28,32].

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