Editors' ChoiceCircadian Rhythms

Eating by the Clock

Sci. Signal.  09 Mar 2010:
Vol. 3, Issue 112, pp. ec74
DOI: 10.1126/scisignal.3112ec74

Drosophila feeding behavior, which depends not only on gustatory and olfactory cues but also on internal signals, is influenced by circadian clocks (see Krupp and Levine). Noting that the Drosophila proboscis (the main gustatory organ) contains circadian oscillators, Chatterjee et al. investigated circadian regulation of the Drosophila gustatory system. Recordings from individual sensillae (taste hairs) on the proboscis tip revealed that both gustatory receptor neurons (GRNs) responsive to sugar (S neurons) and GRNs responsive to bitter compounds showed diurnal and circadian rhythms in the electrophysiological response to stimuli (sucrose and caffeine, respectively). These variations in spike amplitude, duration, and frequency, which persisted in constant darkness and depended on clock components, were paralleled by fluctuations in the proboscis extension reflex (PrER, a taste-evoked response) to stimulatory (sucrose or trehalose) substances and in PrER inhibition by caffeine. Increasing sucrose concentration increased the minimal response to near-maximal levels, indicating circadian variation in taste sensitivity. Immunofluorescence analysis revealed rhythmic changes in GRN PDP1 (Par domain protein 1) abundance, indicating that the GRNs themselves contained circadian oscillators, and expression of a dominant-negative form of the clock component CYC (CYCDN) in S neurons abolished circadian variation in the PrER response to sucrose. Indeed, mutant flies with oscillator function only in S neurons showed circadian variations in PrER. G protein receptor kinase 2 (GPRK2) was present in GRNs, and its abundance in the proboscis varied antiphasically with the PrER response. Manipulation of either GPRK2 or gustatory receptor abundance abolished PrER rhythmicity: The PrER response to sugars was consistently high in mutant flies with little GPRK2 and consistently low in flies in which GPRK2 was overexpressed, whereas increases or decreases in gustatory receptor abundance, respectively, elicited nonrhythmic increases or decreases in PrER. Expression of CYCDN in neurons with the gustatory receptor that mediates responses to trehalose led to increased food consumption and locomotor activity, behavioral changes consistent with the response to starvation, and increased triglyceride and glycogen content. The authors thus conclude that local clocks in GRNs mediate rhythms in taste sensitivity and modulate feeding behavior in Drosophila.

A. Chatterjee, S. Tanoue, J. H. Houl, P. E. Hardin, Regulation of gustatory physiology and appetitive behavior by the Drosophila circadian clock. Curr. Biol. 20, 300–309 (2010). [PubMed]

J. J. Krupp, J. D. Levine, Biological rhythms: The taste-time continuum. Curr. Biol. 20, R147–R149 (2010). [PubMed]