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Asymmetric neurotransmitter release enables rapid odour lateralization in Drosophila

Abstract

In Drosophila, most individual olfactory receptor neurons (ORNs) project bilaterally to both sides of the brain1,2. Having bilateral rather than unilateral projections may represent a useful redundancy. However, bilateral ORN projections to the brain should also compromise the ability to lateralize odours. Nevertheless, walking or flying Drosophila reportedly turn towards the antenna that is more strongly stimulated by odour3,4,5. Here we show that each ORN spike releases approximately 40% more neurotransmitter from the axon branch ipsilateral to the soma than from the contralateral branch. As a result, when an odour activates the antennae asymmetrically, ipsilateral central neurons begin to spike a few milliseconds before contralateral neurons, and at a 30 to 50% higher rate than contralateral neurons. We show that a walking fly can detect a 5% asymmetry in total ORN input to its left and right antennal lobes, and can turn towards the odour in less time than it requires the fly to complete a stride. These results demonstrate that neurotransmitter release properties can be tuned independently at output synapses formed by a single axon onto two target cells with identical functions and morphologies. Our data also show that small differences in spike timing and spike rate can produce reliable differences in olfactory behaviour.

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Figure 1: Drosophila can lateralize odours based on bilateral receptor-neuron input to a single pair of glomeruli.
Figure 2: Lateralized odours produce an asymmetry in spike latency and spike rate in antennal lobe PNs.
Figure 3: The asymmetry arises at the level of ORN–PN synapses.
Figure 4: The asymmetry in ORN–PN synapses has a presynaptic origin.

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Acknowledgements

We are grateful to M. Dickinson, V. Jayaraman, L. Luo, D. Tracey and L. Vosshall for gifts of fly stocks. A. Baker helped construct and improve the spherical treadmill apparatus. Members of the Wilson laboratory provided feedback on the manuscript. This work was supported by a research project grant from the National Institutes of Health (R01DC008174). R.I.W. is an HHMI Early Career Scientist. B.L.d.B. and J.K. were supported by the Rowland Junior Fellows Program.

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Contributions

Q.G. and R.I.W. designed the experiments. Q.G. carried out all of the experiments, except for the calcium imaging, which was performed by Q.G. and E.J.H., and the synaptobrevin imaging, which was performed by R.I.W. Q.G. analysed the data. J.K. and B.L.d.B. helped to design and build the spherical treadmill apparatus. Q.G. and R.I.W. wrote the manuscript.

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Correspondence to Rachel I. Wilson.

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The authors declare no competing financial interests.

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Gaudry, Q., Hong, E., Kain, J. et al. Asymmetric neurotransmitter release enables rapid odour lateralization in Drosophila. Nature 493, 424–428 (2013). https://doi.org/10.1038/nature11747

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