Spike Amplitude of Single-Unit Responses in Antennal Sensillae Is Controlled by the Drosophila Circadian Clock

Abstract

Circadian changes in membrane potential and spontaneous firing frequency have been observed in microbial systems, invertebrates, and mammals. Oscillators in olfactory sensory neurons (OSNs) from Drosophila are both necessary and sufficient to sustain rhythms in electroanntenogram (EAG) responses, suggesting that odorant receptors (ORs) and/or OR-dependent processes are under clock control. We measured single-unit responses in different antennal sensillae from wild-type, clock mutant, odorant-receptor mutant, and G protein-coupled receptor kinase 2 (Gprk2) mutant flies to examine the cellular and molecular mechanisms that drive rhythms in olfaction. Spontaneous spike amplitude, but not spontaneous or odor-induced firing frequency, is under clock control in ab1 and ab3 basiconic sensillae and T2 trichoid sensillae. Mutants lacking odorant receptors in dendrites display constant low spike amplitudes, and the reduction or increase of levels of GPRK2 in OSNs results in constant low or constant high spontaneous spike amplitudes, respectively. We conclude that spike amplitude is controlled by circadian clocks in basiconic and trichoid sensillae and requires GPRK2 expression and the presence of functional ORs in dendrites. These results argue that rhythms in GPRK2 levels control OR localization and OR-dependent ion channel activity and/or composition to mediate rhythms in spontaneous spike amplitude.

Post-eclosion odor experience modifies olfactory receptor neuron coding in Drosophila

“…These findings are paralleled by studies showing that olfactory sensilla undergo significant morphological changes that result from odor deprivation in Caenorhabditis elegans (30), and odor imprinting in zebrafish is correlated with changes in gene expression in their ORNs (31). In addition to plasticity resulting from imprinting or conditioning, other studies in Diptera indicate that odor coding may display circadian variation (32,33), and depend on age, sex, and hunger level (34). Furthermore, short-term priming by certain ketones and alde- Fig.…”

Blood meal-induced changes to antennal transcriptome profiles reveal shifts in odor sensitivities in Anopheles gambiae

“…The rhythmicity seen in these transcripts suggests that peripheral circadian clock genes may be involved in their regulation. It is well established that autonomous clocks operate in a number of peripheral insect tissues, including the antennae of Drosophila melanogaster (32,33) where odor sensitivity rhythms are affected by the circadian oscillator (34,35). Although differential expression analysis would not detect genes that cycle synchronously between Bf and nBf, the rhythmic pattern seen in cluster 13 is the result of a decoupling of diel rhythmicity between the Bf and nBf groups following blood feeding, possibly a result of the near doubling in the abundance of the clock ortholog (AGAP005711) within the Bf cohort (Fig.…”

Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits

“…Thus, a regulatory mechanism that modulates olfactory signaling and thereby allows the animal to respond differentially to odor sources at different situations should be advantageous. For instance, olfactory sensitivity in Drosophila is regulated by a circadian rhythm (Krishnan et al, 1999), which is sustained by oscillations in olfactory receptor neurons (Krishnan et al, 2008). Neuropeptides can act as neuromodulators and may affect target cells differentially in different physiological and behavioral contexts.…”