Elsevier

Current Opinion in Neurobiology

Volume 29, December 2014, Pages 57-63
Current Opinion in Neurobiology

Feeding regulation in Drosophila

https://doi.org/10.1016/j.conb.2014.05.008Get rights and content

Highlights

  • Signals from peripheral tissues and circulating nutrients report nutritional status.

  • Multiple cues signal hunger and satiety.

  • Subprograms of feeding behavior are under independent modulatory control.

Neuromodulators play a key role in adjusting animal behavior based on environmental cues and internal needs. Here, we review the regulation of Drosophila feeding behavior to illustrate how neuromodulators achieve behavioral plasticity. Recent studies have made rapid progress in determining molecular and cellular mechanisms that translate the metabolic needs of the fly into changes in neuroendocrine and neuromodulatory states. These neuromodulators in turn promote or inhibit discrete feeding behavioral subprograms. This review highlights the links between physiological needs, neuromodulatory states, and feeding decisions.

Introduction

Animals have evolved diverse behavioral repertoires to facilitate survival. Many of these behaviors are plastic and subject to modulation by environmental cues and internal needs. Neuromodulators, such as biogenic amines and neuropeptides, play a critical role in achieving behavioral plasticity. Work in invertebrates, particularly in the crustacean stomatogastric ganglion and Caenorhabditis elegans, has provided detailed insight into how neuromodulators alter biophysical properties of individual neurons and reconfigure circuits [1, 2]. Here, we will examine how these lessons apply to establishing flexibility in a complex innate behavior by reviewing recent findings on neuromodulation in the fruit fly feeding circuit.

The basic challenge in food intake regulation is to maintain energetic homeostasis by balancing food consumption with energy expenditure. Recent studies of Drosophila feeding illustrate several principles of how neuromodulatory systems link physiological needs to flexible expression of adaptive behaviors. This review focuses on how metabolic changes are translated into neuroendocrine and neuromodulatory states and how these in turn impinge on central circuits to regulate feeding decisions.

Section snippets

Structure and plasticity in Drosophila feeding behavior

Drosophila feeding behavior is composed of a series of behavioral modules or subprograms (Figure 1). In a food-deprived state, an adult fruit fly will forage for potential food sources (panel a) [3, 4]. Chemosensory detection of a palatable food leads to cessation of locomotion (panel b), meal initiation (panel c), and consumption (panel d) [5, 6]. Post-ingestive signals generated during consumption cause meal termination (panel e) and disengagement from the food source (f) by reactivating

Nutritional status is converted into neuromodulatory states

The central nervous system monitors systemic energy balance and alters feeding probability based on internal nutritional state. Remarkably, recent studies reveal that a small number of specialized central brain neurons directly sense specific circulating macronutrients and modify feeding. Behavioral evidence that flies have internal nutrient sensors came from studies showing that flies can distinguish sugars based solely on caloric content in the absence of sweet taste detection [7•, 8, 9•, 10

Converting neuromodulatory states into feeding decisions

A dozen neuromodulatory systems in Drosophila have been implicated to date in food intake regulation. Many of the signaling systems appear to be functionally conserved throughout evolution, including orthologs for mammalian peptidergic signals tachykinin, cholecystokinin, neuropeptide Y, Neuromedin U and insulin [21, 30•, 31, 32, 33]. Although our understanding of how neuromodulators sway feeding decisions is far from complete, recent studies serve to illustrate conserved functions of

Conclusions

Recent work in Drosophila and other model systems has revealed how neuromodulators respond to changes in nutrient availability to adjust discrete aspects of feeding. Systemic signals from peripheral tissues and circulating nutrients report nutritional status to the brain. Central effector pathways release neuromodulators to independently promote or inhibit discrete feeding behavioral subprograms. Recent studies have made rapid progress by identifying and characterizing key signals that regulate

Conflict of interest

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

KS is supported by a grant from the NIH (DK098747) and an HHMI Early Career Scientist award.

A-HP was supported by a predoctoral grant from Boehringer Ingelheim Fonds. We would like to thank Dr. Christoph Scheper for help with Figure 1 and Dr. Brendan Mullaney for comments.

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