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Featured ArticleResearch Articles, Systems/Circuits

Nonsynaptic Transmission Mediates Light Context-Dependent Odor Responses in Drosophila melanogaster

Kazuaki Ikeda, Masaki Kataoka and Nobuaki K. Tanaka
Journal of Neuroscience 16 November 2022, 42 (46) 8621-8628; DOI: https://doi.org/10.1523/JNEUROSCI.1106-22.2022
Kazuaki Ikeda
1Division of Biology, Department of Biological Sciences, School of Science, Hokkaido University, Sapporo, 060-0810, Japan
2Graduate School of Life Sciences, Hokkaido University, Sapporo, 060-0810, Japan
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Masaki Kataoka
1Division of Biology, Department of Biological Sciences, School of Science, Hokkaido University, Sapporo, 060-0810, Japan
2Graduate School of Life Sciences, Hokkaido University, Sapporo, 060-0810, Japan
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Nobuaki K. Tanaka
1Division of Biology, Department of Biological Sciences, School of Science, Hokkaido University, Sapporo, 060-0810, Japan
2Graduate School of Life Sciences, Hokkaido University, Sapporo, 060-0810, Japan
3Faculty of Science, Hokkaido University, Sapporo, 060-0810, Japan
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Abstract

Recent connectome analyses of the entire synaptic circuit in the nervous system have provided tremendous insights into how neural processing occurs through the synaptic relay of neural information. Conversely, the extent to which ephaptic transmission which does not depend on the synapses contributes to the relay of neural information, especially beyond a distance between adjacent neurons and to neural processing remains unclear. We show that ephaptic transmission mediated by extracellular potential changes in female Drosophila melanogaster can reach >200 µm, equivalent to the depth of its brain. Furthermore, ephaptic transmission driven by retinal photoreceptor cells mediates light-evoked firing rate increases in olfactory sensory neurons. These results indicate that ephaptic transmission contributes to sensory responses that can change momentarily in a context-dependent manner.

SIGNIFICANCE STATEMENT Although extracellular field potential activities are commonly observed in many nervous systems, this activity has been generally considered as a side effect of synchronized spiking of neurons. This study, however, shows that field potential changes in retinae evoked by a sensory stimulus can control the excitability of distant neurons in vivo and mediates multimodal sensory integration in Drosophila melanogaster. As such ephaptic transmission is more effective at a short distance, the ephaptic transmission from the retinae may contribute significantly to firing rate changes in downstream neurons of the photoreceptor cells in the optic lobe.

  • electric field
  • ephaptic
  • field potential
  • multimodal sensory integration
  • olfaction
  • vision

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The Journal of Neuroscience: 42 (46)
Journal of Neuroscience
Vol. 42, Issue 46
16 Nov 2022
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Nonsynaptic Transmission Mediates Light Context-Dependent Odor Responses in Drosophila melanogaster
Kazuaki Ikeda, Masaki Kataoka, Nobuaki K. Tanaka
Journal of Neuroscience 16 November 2022, 42 (46) 8621-8628; DOI: 10.1523/JNEUROSCI.1106-22.2022

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Nonsynaptic Transmission Mediates Light Context-Dependent Odor Responses in Drosophila melanogaster
Kazuaki Ikeda, Masaki Kataoka, Nobuaki K. Tanaka
Journal of Neuroscience 16 November 2022, 42 (46) 8621-8628; DOI: 10.1523/JNEUROSCI.1106-22.2022
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Keywords

  • electric field
  • ephaptic
  • field potential
  • multimodal sensory integration
  • olfaction
  • vision

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