Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly

The fruit fly Drosophila melanogaster responds behaviorally to sound, gravity, and wind. Johnston’s organ (JO) at the antennal base serves as a sensory organ in the fruit fly to detect these mechanosensory stimuli. Among the five anatomically defined subgroups of sensory neurons in JO, subgroups A a...

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Main Authors: Eriko eMatsuo, Daichi eYamada, Yuki eIshikawa, Tomonori eAsai, Hiroshi eIshimoto, Azusa eKamikouchi
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-05-01
Series:Frontiers in Physiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fphys.2014.00179/full
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author Eriko eMatsuo
Daichi eYamada
Yuki eIshikawa
Tomonori eAsai
Hiroshi eIshimoto
Azusa eKamikouchi
Azusa eKamikouchi
author_facet Eriko eMatsuo
Daichi eYamada
Yuki eIshikawa
Tomonori eAsai
Hiroshi eIshimoto
Azusa eKamikouchi
Azusa eKamikouchi
author_sort Eriko eMatsuo
collection DOAJ
description The fruit fly Drosophila melanogaster responds behaviorally to sound, gravity, and wind. Johnston’s organ (JO) at the antennal base serves as a sensory organ in the fruit fly to detect these mechanosensory stimuli. Among the five anatomically defined subgroups of sensory neurons in JO, subgroups A and B detect sound vibrations and subgroups C and E respond to static deflections, such as gravity and wind. The functions of subgroup-D JO neurons, however, remain unknown. In this study, we used molecular-genetic methods to explore the physiologic properties of subgroup-D JO neurons. Both vibrations and static deflection of the antennal receiver activated subgroup-D JO neurons. This finding clearly revealed that zone D in the antennal mechanosensory and motor center (AMMC), the projection target of subgroup-D JO neurons, is a primary center for antennal vibrations and deflection in the fly brain. We anatomically identified two types of interneurons downstream of subgroup-D JO neurons, AMMC LNs and AMMC D1 neurons. AMMC LNs are local neurons whose projections are confined within the AMMC, connecting zones B and D. On the other hand, AMMC D1 neurons have both local dendritic arborizations within the AMMC and descending projections to the thoracic ganglia, suggesting that AMMC D1 neurons are likely to relay information of the antennal movement detected by subgroup-D JO neurons from the AMMC directly to the thorax. Together, these findings provide a neural basis for how JO and its brain targets encode information of complex movements of the fruit fly antenna.
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spelling doaj.art-92919c57880b4bce885c6bf4950dd8782022-12-21T20:36:51ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2014-05-01510.3389/fphys.2014.0017976433Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit flyEriko eMatsuo0Daichi eYamada1Yuki eIshikawa2Tomonori eAsai3Hiroshi eIshimoto4Azusa eKamikouchi5Azusa eKamikouchi6Graduate School of Science, Nagoya UniversityGraduate School of Science, Nagoya UniversityGraduate School of Science, Nagoya UniversityGraduate School of Science, Nagoya UniversityGraduate School of Science, Nagoya UniversityGraduate School of Science, Nagoya UniversityPrecursory Research for Embryonic Science and Technology, Japan Science and Technology AgencyThe fruit fly Drosophila melanogaster responds behaviorally to sound, gravity, and wind. Johnston’s organ (JO) at the antennal base serves as a sensory organ in the fruit fly to detect these mechanosensory stimuli. Among the five anatomically defined subgroups of sensory neurons in JO, subgroups A and B detect sound vibrations and subgroups C and E respond to static deflections, such as gravity and wind. The functions of subgroup-D JO neurons, however, remain unknown. In this study, we used molecular-genetic methods to explore the physiologic properties of subgroup-D JO neurons. Both vibrations and static deflection of the antennal receiver activated subgroup-D JO neurons. This finding clearly revealed that zone D in the antennal mechanosensory and motor center (AMMC), the projection target of subgroup-D JO neurons, is a primary center for antennal vibrations and deflection in the fly brain. We anatomically identified two types of interneurons downstream of subgroup-D JO neurons, AMMC LNs and AMMC D1 neurons. AMMC LNs are local neurons whose projections are confined within the AMMC, connecting zones B and D. On the other hand, AMMC D1 neurons have both local dendritic arborizations within the AMMC and descending projections to the thoracic ganglia, suggesting that AMMC D1 neurons are likely to relay information of the antennal movement detected by subgroup-D JO neurons from the AMMC directly to the thorax. Together, these findings provide a neural basis for how JO and its brain targets encode information of complex movements of the fruit fly antenna.http://journal.frontiersin.org/Journal/10.3389/fphys.2014.00179/fullBrainDrosophilainsectmechanosensoryneural circuitcalcium imaging
spellingShingle Eriko eMatsuo
Daichi eYamada
Yuki eIshikawa
Tomonori eAsai
Hiroshi eIshimoto
Azusa eKamikouchi
Azusa eKamikouchi
Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly
Frontiers in Physiology
Brain
Drosophila
insect
mechanosensory
neural circuit
calcium imaging
title Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly
title_full Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly
title_fullStr Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly
title_full_unstemmed Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly
title_short Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly
title_sort identification of novel vibration and deflection sensitive neuronal subgroups in johnston s organ of the fruit fly
topic Brain
Drosophila
insect
mechanosensory
neural circuit
calcium imaging
url http://journal.frontiersin.org/Journal/10.3389/fphys.2014.00179/full
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