Dystrophin is required for normal synaptic gain in the Drosophila olfactory circuit

Salinee Jantrapirom, De Shou Cao, Jing W. Wang, Huey Hing, Christopher J. Tabone, Kathryn Lantz, J.S. de Belle, Yu Tong Qiu, Hans M. Smid, Masamitsu Yamaguchi, Lee G. Fradkin, Jasprina N. Noordermeer, Saranyapin Potikanond*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

The Drosophila olfactory system provides an excellent model to elucidate the neural circuits that control behaviors elicited by environmental stimuli. Despite significant progress in defining olfactory circuit components and their connectivity, little is known about the mechanisms that transfer the information from the primary antennal olfactory receptor neurons to the higher order brain centers. Here, we show that the Dystrophin Dp186 isoform is required in the olfactory system circuit for olfactory functions. Using two-photon calcium imaging, we found the reduction of calcium influx in olfactory receptor neurons (ORNs) and also the defect of GABA A mediated inhibitory input in the projection neurons (PNs) in Dp186 mutation. Moreover, the Dp186 mutant flies which display a decreased odor avoidance behavior were rescued by Dp186 restoration in the Drosophila olfactory neurons in either the presynaptic ORNs or the postsynaptic PNs. Therefore, these results revealed a role for Dystrophin, Dp 186 isoform in gain control of the olfactory synapse via the modulation of excitatory and inhibitory synaptic inputs to olfactory projection neurons.

Original languageEnglish
Pages (from-to)158-166
Number of pages9
JournalBrain Research
Volume1712
DOIs
Publication statusPublished - 1 Jun 2019

Fingerprint

Dystrophin
Olfactory Receptor Neurons
Drosophila
Neurons
Protein Isoforms
Avoidance Learning
Calcium
Presynaptic Receptors
Behavior Control
Photons
Diptera
Synapses
gamma-Aminobutyric Acid
Mutation
Brain

Keywords

  • Antennal lobe
  • Behavior
  • Drosophila melanogaster
  • Dystrophin
  • Olfaction
  • Olfactory receptor neurons
  • Projection neurons

Cite this

Jantrapirom, S., Cao, D. S., Wang, J. W., Hing, H., Tabone, C. J., Lantz, K., ... Potikanond, S. (2019). Dystrophin is required for normal synaptic gain in the Drosophila olfactory circuit. Brain Research, 1712, 158-166. https://doi.org/10.1016/j.brainres.2019.01.039
Jantrapirom, Salinee ; Cao, De Shou ; Wang, Jing W. ; Hing, Huey ; Tabone, Christopher J. ; Lantz, Kathryn ; de Belle, J.S. ; Qiu, Yu Tong ; Smid, Hans M. ; Yamaguchi, Masamitsu ; Fradkin, Lee G. ; Noordermeer, Jasprina N. ; Potikanond, Saranyapin. / Dystrophin is required for normal synaptic gain in the Drosophila olfactory circuit. In: Brain Research. 2019 ; Vol. 1712. pp. 158-166.
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abstract = "The Drosophila olfactory system provides an excellent model to elucidate the neural circuits that control behaviors elicited by environmental stimuli. Despite significant progress in defining olfactory circuit components and their connectivity, little is known about the mechanisms that transfer the information from the primary antennal olfactory receptor neurons to the higher order brain centers. Here, we show that the Dystrophin Dp186 isoform is required in the olfactory system circuit for olfactory functions. Using two-photon calcium imaging, we found the reduction of calcium influx in olfactory receptor neurons (ORNs) and also the defect of GABA A mediated inhibitory input in the projection neurons (PNs) in Dp186 mutation. Moreover, the Dp186 mutant flies which display a decreased odor avoidance behavior were rescued by Dp186 restoration in the Drosophila olfactory neurons in either the presynaptic ORNs or the postsynaptic PNs. Therefore, these results revealed a role for Dystrophin, Dp 186 isoform in gain control of the olfactory synapse via the modulation of excitatory and inhibitory synaptic inputs to olfactory projection neurons.",
keywords = "Antennal lobe, Behavior, Drosophila melanogaster, Dystrophin, Olfaction, Olfactory receptor neurons, Projection neurons",
author = "Salinee Jantrapirom and Cao, {De Shou} and Wang, {Jing W.} and Huey Hing and Tabone, {Christopher J.} and Kathryn Lantz and {de Belle}, J.S. and Qiu, {Yu Tong} and Smid, {Hans M.} and Masamitsu Yamaguchi and Fradkin, {Lee G.} and Noordermeer, {Jasprina N.} and Saranyapin Potikanond",
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Jantrapirom, S, Cao, DS, Wang, JW, Hing, H, Tabone, CJ, Lantz, K, de Belle, JS, Qiu, YT, Smid, HM, Yamaguchi, M, Fradkin, LG, Noordermeer, JN & Potikanond, S 2019, 'Dystrophin is required for normal synaptic gain in the Drosophila olfactory circuit', Brain Research, vol. 1712, pp. 158-166. https://doi.org/10.1016/j.brainres.2019.01.039

Dystrophin is required for normal synaptic gain in the Drosophila olfactory circuit. / Jantrapirom, Salinee; Cao, De Shou; Wang, Jing W.; Hing, Huey; Tabone, Christopher J.; Lantz, Kathryn; de Belle, J.S.; Qiu, Yu Tong; Smid, Hans M.; Yamaguchi, Masamitsu; Fradkin, Lee G.; Noordermeer, Jasprina N.; Potikanond, Saranyapin.

In: Brain Research, Vol. 1712, 01.06.2019, p. 158-166.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Dystrophin is required for normal synaptic gain in the Drosophila olfactory circuit

AU - Jantrapirom, Salinee

AU - Cao, De Shou

AU - Wang, Jing W.

AU - Hing, Huey

AU - Tabone, Christopher J.

AU - Lantz, Kathryn

AU - de Belle, J.S.

AU - Qiu, Yu Tong

AU - Smid, Hans M.

AU - Yamaguchi, Masamitsu

AU - Fradkin, Lee G.

AU - Noordermeer, Jasprina N.

AU - Potikanond, Saranyapin

PY - 2019/6/1

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N2 - The Drosophila olfactory system provides an excellent model to elucidate the neural circuits that control behaviors elicited by environmental stimuli. Despite significant progress in defining olfactory circuit components and their connectivity, little is known about the mechanisms that transfer the information from the primary antennal olfactory receptor neurons to the higher order brain centers. Here, we show that the Dystrophin Dp186 isoform is required in the olfactory system circuit for olfactory functions. Using two-photon calcium imaging, we found the reduction of calcium influx in olfactory receptor neurons (ORNs) and also the defect of GABA A mediated inhibitory input in the projection neurons (PNs) in Dp186 mutation. Moreover, the Dp186 mutant flies which display a decreased odor avoidance behavior were rescued by Dp186 restoration in the Drosophila olfactory neurons in either the presynaptic ORNs or the postsynaptic PNs. Therefore, these results revealed a role for Dystrophin, Dp 186 isoform in gain control of the olfactory synapse via the modulation of excitatory and inhibitory synaptic inputs to olfactory projection neurons.

AB - The Drosophila olfactory system provides an excellent model to elucidate the neural circuits that control behaviors elicited by environmental stimuli. Despite significant progress in defining olfactory circuit components and their connectivity, little is known about the mechanisms that transfer the information from the primary antennal olfactory receptor neurons to the higher order brain centers. Here, we show that the Dystrophin Dp186 isoform is required in the olfactory system circuit for olfactory functions. Using two-photon calcium imaging, we found the reduction of calcium influx in olfactory receptor neurons (ORNs) and also the defect of GABA A mediated inhibitory input in the projection neurons (PNs) in Dp186 mutation. Moreover, the Dp186 mutant flies which display a decreased odor avoidance behavior were rescued by Dp186 restoration in the Drosophila olfactory neurons in either the presynaptic ORNs or the postsynaptic PNs. Therefore, these results revealed a role for Dystrophin, Dp 186 isoform in gain control of the olfactory synapse via the modulation of excitatory and inhibitory synaptic inputs to olfactory projection neurons.

KW - Antennal lobe

KW - Behavior

KW - Drosophila melanogaster

KW - Dystrophin

KW - Olfaction

KW - Olfactory receptor neurons

KW - Projection neurons

U2 - 10.1016/j.brainres.2019.01.039

DO - 10.1016/j.brainres.2019.01.039

M3 - Article

VL - 1712

SP - 158

EP - 166

JO - Brain Research

JF - Brain Research

SN - 0006-8993

ER -