Calcium-stores mediate adaptation in axon terminals of olfactory receptor neurons in Drosophila.
BACKGROUND
In vertebrates and invertebrates, sensory neurons adapt to variable ambient conditions, such as the duration or repetition of a stimulus, a physiological mechanism considered as a simple form of non-associative learning and neuronal plasticity. Although various signaling pathways, as cAMP, cGMP, and the inositol 1,4,5-triphosphate receptor (InsP3R) play a role in adaptation, their precise mechanisms of action at the cellular level remain incompletely understood. Recently, in Drosophila, we reported that odor-induced Ca2+-response in axon terminals of olfactory receptor neurons (ORNs) is related to odor duration. In particular, a relatively long odor stimulus (such as 5 s) triggers the induction of a second component involving intracellular Ca2+-stores.


RESULTS
We used a recently developed in-vivo bioluminescence imaging approach to quantify the odor-induced Ca2+-activity in the axon terminals of ORNs. Using either a genetic approach to target specific RNAs, or a pharmacological approach, we show that the second component, relying on the intracellular Ca2+-stores, is responsible for the adaptation to repetitive stimuli. In the antennal lobes (a region analogous to the vertebrate olfactory bulb) ORNs make synaptic contacts with second-order neurons, the projection neurons (PNs). These synapses are modulated by GABA, through either GABAergic local interneurons (LNs) and/or some GABAergic PNs. Application of GABAergic receptor antagonists, both GABAA or GABAB, abolishes the adaptation, while RNAi targeting the GABABR (a metabotropic receptor) within the ORNs, blocks the Ca2+-store dependent component, and consequently disrupts the adaptation. These results indicate that GABA exerts a feedback control. Finally, at the behavioral level, using an olfactory test, genetically impairing the GABABR or its signaling pathway specifically in the ORNs disrupts olfactory adapted behavior.


CONCLUSIONS
Taken together, our results indicate that a relatively long lasting form of adaptation occurs within the axon terminals of the ORNs in the antennal lobes, which depends on intracellular Ca2+-stores, attributable to a positive feedback through the GABAergic synapses.
Imagerie Cérébrale Fonctionnelle et Comportements, Neurobiologie et Développement, CNRS, UPR-3294, 1 Avenue de la Terrasse, Gif-sur-Yvette Cedex, France.
Meena S
MS
Murmu
Jacques
J
Stinnakre
Eléonore
E
Réal
Jean-René
JR
Martin
D000222:Adaptation, Physiological / Q000502:physiology*; D000818:Animals; D030801:Animals, Genetically Modified; D001369:Axons / Q000502:physiology; D002118:Calcium / Q000378:metabolism* / Q000502:physiology; D020013:Calcium Signaling / Q000502:physiology*; D004331:Drosophila melanogaster / Q000235:genetics / Q000502:physiology*; D005260:Female; D018034:Olfactory Receptor Neurons / Q000166:cytology / Q000502:physiology*; D017729:Presynaptic Terminals / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology
D002118:Calcium