Increased feeding and food hoarding following food deprivation are associated with activation of dopamine and orexin neurons in male Brandt's voles.

Xue-Ying Zhang,Hui-Di Yang,Qiang Zhang,De-Hua Wang,Zuoxin Wang

doi:10.1371/journal.pone.0026408

Xue-Ying Zhang, Hui-Di Yang + Show 3 more

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https://doi.org/10.1371/journal.pone.0026408

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Abstract

Small mammals usually face energetic challenges, such as food shortage, in the field. They have thus evolved species-specific adaptive strategies for survival and reproductive success. In the present study, we examined male Brandt's voles (Lasiopodomys brandtii) for their physiological, behavioral, and neuronal responses to food deprivation (FD) and subsequent re-feeding. Although 48 hr FD induced a decrease in body weight and the resting metabolic rate (RMR), such decreases did not reach statistical significance when compared to the control males that did not experience FD. During the first 2 hr of re-feeding following 48 hr FD, voles showed higher levels of feeding than controls. However, when permitted to hoard food, FD voles showed an increase in food hoarding, rather than feeding, compared to the controls. Further, both feeding and food hoarding induced an increase in neuronal activation, measured by Fos-ir, in a large number of brain areas examined. Interestingly, feeding and food hoarding also induced an increase in the percentage of tyrosine hydroxylase immunoreactive (TH-ir) cells that co-expressed Fos-ir in the ventral tegmental area (VTA), whereas both FD and feeding induced an increase in the percentage of orexin-ir cells that co-expressed Fos-ir in the lateral hypothalamus (LH). Food hoarding also increased orexin-ir/Fos-ir labeling in the LH. Together, our data indicate that food-deprived male Brandt's voles display enhanced feeding or food hoarding dependent upon an environmental setting. In addition, changes in central dopamine and orexin activities in selected brain areas are associated with feeding and hoarding behaviors following FD and subsequent re-feeding.

Highlights

Food availability is an important environmental cue that affects animal fitness, such as body weight, development, survival, and reproduction [1]
In the food deprivation (FD)-refeeding group, one or two days of FD resulted in significant decreases in body weight compared to the baseline levels, and body weight completely recovered within 2 weeks after refeeding
We found that food-deprived male Brandt’s voles increased feeding or food hoarding after re-feeding and this effect was dependent upon environmental setting

Summary

Introduction

Food availability is an important environmental cue that affects animal fitness, such as body weight, development, survival, and reproduction [1]. When faced with limited food availability, many small mammals, such as rats, mice, voles, and gerbils, with relatively high metabolic rates can engage in several behaviors to lower energy expenditure They can decrease resting metabolic rate (RMR) and non-shivering thermogenesis (NST) [2,3,4], reduce physical activity [5], or even enter torpor [6] to conserve energy. Other species, such as Siberian hamsters (Phodopus sungorus) and Syrian hamsters (Mesocricetus auratus), were reported to increase hoarding rather than feeding when given access to food following food shortage [9,10] These compensatory increases in feeding or food hoarding to restore energy balance may be a ‘‘hard-wired’’, evolutionarily conserved mechanism to ensure animal’s survival and reproductive fitness [1]. We still know very little about the neuromechanisms underlying these behaviors

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