Calcium-stores mediate adaptation in axon terminals of Olfactory Receptor Neurons in Drosophila
<p>Abstract</p> <p>Background</p> <p>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...
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| Format: | Article |
| Language: | English |
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BMC
2011-10-01
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| Series: | BMC Neuroscience |
| Online Access: | http://www.biomedcentral.com/1471-2202/12/105 |
| _version_ | 1818066191967584256 |
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| author | Murmu Meena S Stinnakre Jacques Réal Eléonore Martin Jean-René |
| author_facet | Murmu Meena S Stinnakre Jacques Réal Eléonore Martin Jean-René |
| author_sort | Murmu Meena S |
| collection | DOAJ |
| description | <p>Abstract</p> <p>Background</p> <p>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 (InsP<sub>3</sub>R) play a role in adaptation, their precise mechanisms of action at the cellular level remain incompletely understood. Recently, in <it>Drosophila</it>, we reported that odor-induced Ca<sup>2+</sup>-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 Ca<sup>2+</sup>-stores.</p> <p>Results</p> <p>We used a recently developed <it>in-vivo </it>bioluminescence imaging approach to quantify the odor-induced Ca<sup>2+</sup>-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 Ca<sup>2+</sup>-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 GABA<sub>A </sub>or GABA<sub>B</sub>, abolishes the adaptation, while RNAi targeting the GABAB<sub>R </sub>(a metabotropic receptor) within the ORNs, blocks the Ca<sup>2+</sup>-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 GABA<sub>B</sub>R or its signaling pathway specifically in the ORNs disrupts olfactory adapted behavior.</p> <p>Conclusion</p> <p>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 Ca<sup>2+</sup>-stores, attributable to a positive feedback through the GABAergic synapses.</p> |
| first_indexed | 2024-12-10T15:03:52Z |
| format | Article |
| id | doaj.art-f0b8e8da102d4c37b13086b3d1e26b52 |
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| issn | 1471-2202 |
| language | English |
| last_indexed | 2024-12-10T15:03:52Z |
| publishDate | 2011-10-01 |
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| spelling | doaj.art-f0b8e8da102d4c37b13086b3d1e26b522022-12-22T01:44:06ZengBMCBMC Neuroscience1471-22022011-10-0112110510.1186/1471-2202-12-105Calcium-stores mediate adaptation in axon terminals of Olfactory Receptor Neurons in DrosophilaMurmu Meena SStinnakre JacquesRéal EléonoreMartin Jean-René<p>Abstract</p> <p>Background</p> <p>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 (InsP<sub>3</sub>R) play a role in adaptation, their precise mechanisms of action at the cellular level remain incompletely understood. Recently, in <it>Drosophila</it>, we reported that odor-induced Ca<sup>2+</sup>-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 Ca<sup>2+</sup>-stores.</p> <p>Results</p> <p>We used a recently developed <it>in-vivo </it>bioluminescence imaging approach to quantify the odor-induced Ca<sup>2+</sup>-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 Ca<sup>2+</sup>-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 GABA<sub>A </sub>or GABA<sub>B</sub>, abolishes the adaptation, while RNAi targeting the GABAB<sub>R </sub>(a metabotropic receptor) within the ORNs, blocks the Ca<sup>2+</sup>-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 GABA<sub>B</sub>R or its signaling pathway specifically in the ORNs disrupts olfactory adapted behavior.</p> <p>Conclusion</p> <p>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 Ca<sup>2+</sup>-stores, attributable to a positive feedback through the GABAergic synapses.</p>http://www.biomedcentral.com/1471-2202/12/105 |
| spellingShingle | Murmu Meena S Stinnakre Jacques Réal Eléonore Martin Jean-René Calcium-stores mediate adaptation in axon terminals of Olfactory Receptor Neurons in Drosophila BMC Neuroscience |
| title | Calcium-stores mediate adaptation in axon terminals of Olfactory Receptor Neurons in Drosophila |
| title_full | Calcium-stores mediate adaptation in axon terminals of Olfactory Receptor Neurons in Drosophila |
| title_fullStr | Calcium-stores mediate adaptation in axon terminals of Olfactory Receptor Neurons in Drosophila |
| title_full_unstemmed | Calcium-stores mediate adaptation in axon terminals of Olfactory Receptor Neurons in Drosophila |
| title_short | Calcium-stores mediate adaptation in axon terminals of Olfactory Receptor Neurons in Drosophila |
| title_sort | calcium stores mediate adaptation in axon terminals of olfactory receptor neurons in drosophila |
| url | http://www.biomedcentral.com/1471-2202/12/105 |
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