Elsevier

Neuroscience

Volume 192, 29 September 2011, Pages 459-474
Neuroscience

Cognitive, Behavioral, and Systems Neuroscience
Research Paper
Sucrose modifies c-fos mRNA expression in the brain of rats maintained on feeding schedules

https://doi.org/10.1016/j.neuroscience.2011.06.033Get rights and content

Abstract

Food intake is regulated according to circadian activity, metabolic needs and the hedonic value of food. Rodents placed on a fixed feeding schedule show behavioral and physiological anticipation of mealtime referred to as food-anticipatory activity (FAA). FAA is driven by the food-entrainable oscillator (FEO), whose anatomical substrate is not yet known. Recent data have shown that restricted feeding schedules for regular chow and daily limited access to palatable food in free-feeding rats activate distinct brain regions during FAA. The combination of a deprivation regimen and scheduled access to palatable food may give rise to a more global anticipatory mechanism because the temporal cycles of energy balance would be strongly modulated by the incentive properties of palatable food; however, the neuronal response to this combined treatment is not yet known. The present study investigated how adding palatable sucrose to feeding schedules affects the pattern of brain c-fos mRNA expression during FAA (0–3 h) and 1 h following feeding. The rats maintained on scheduled chow access increased their daily chow intake, while the rats maintained on scheduled sucrose and chow mainly increased their daily sucrose intake. Adding sucrose to scheduled feeding displaced c-fos mRNA expression from the dorsomedial and paraventricular hypothalamic nuclei and posterior lateral hypothalamus (LH) to the prefrontal cortex, lateral septum, nucleus accumbens and anterior LH. During refeeding, the rats on scheduled sucrose demonstrated higher activation of the nucleus of the solitary tract. The present results suggest that palatable sucrose combined with restricted feeding schedules activate a distinct neuronal network compared to neuronal activation produced by scheduled access to regular chow. These data provide evidence that the brain may contain different food-oscillatory systems and that food palatability may shift the neuronal activity from the medial hypothalamus to the limbic and reward-related areas even at the negative metabolic state.

Highlights

▶Scheduled feeding induces neuronal c-fos mRNA expression during FAA. ▶Feeding schedules on chow affect medial hypothalamus. ▶Adding sucrose displaces the neuronal activation from the medial hypothalamus. ▶Sucrose anticipation stimulates the limbic and reward-related brain areas. ▶Brain contains different food-related oscillatory systems.

Section snippets

Animals and housing conditions

Male Wistar rats (n=76), aged 6 weeks, were purchased from the Canadian Breeding Laboratories (St.-Constant, QC, Canada). Animals were housed individually in plastic cages lined with wood shavings and maintained on a 12:12-h dark–light cycle [light-on between 06h00 (Zeitgeber time 0—ZT0) and 18h00 (ZT12)], with ambient temperature of 23±1 °C, free access to tap water, and the standard laboratory rat diet (Rat/Mouse/Hamster chow; 1000 Formula; 12.9 kJ/g; Agway Prolab), unless otherwise

Food intake, energy intake, and body weight

Ad-libitum-fed rats showed a slow gradual increase of their daily chow intake over the 3 weeks of the experiment (for 1.34 times over 3 weeks from 23.52±0.86 g on the first day to 31.59±1.35 g on the last, 21st day of the experiment; P=0.001). The increase in the daily chow intake of rats maintained on scheduled access to chow was also sustained and gradual. In total, the SC rats increased their chow intake by 16 times over the 3 weeks (from 1.68±0.31 g on the first day to 25.19±1.36 g on the

Discussion

The present data provide evidence that adding sucrose to feeding schedules alters the pattern of neuronal activation during food anticipation and following feeding. We recently described the pattern of induction of c-fos mRNA expression in the brains of rats maintained on scheduled daily access to chow (Poulin and Timofeeva, 2008). This treatment led to the activation of the DMH, PVTa, and SHi as early as 3 h before the expected meal, the time when the animals start to express FAA. As the time

Conclusion

The present results have demonstrated that adding sucrose to daily scheduled feeding displaced neuronal anticipatory activity from the medial and lateral tuberal hypothalamus to the lateral anterior hypothalamus as well as to the prefrontal cortex and the ventral striatum. The dorsomedial paraventricular thalamus, which interconnects the hypothalamic and limbic regions, was similarly activated by both treatments. The present data provide evidence that the dorsomedial thalamo-hypothalamic loop

Acknowledgments

This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and Canadian Institutes of Health Research. E.T. is a scholar of Fonds de la Recherche en Santé du Québec (FRSQ) and A.M. is a scholar of the Medicine Faculty of Laval University. We thank Julie Plamondon and Pierre Samson for technical assistance.

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