Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in Drosophila
Startle-induced locomotion is commonly used in Drosophila research to monitor locomotor reactivity and its progressive decline with age or under various neuropathological conditions. A widely used paradigm is startle-induced negative geotaxis (SING), in which flies entrapped in a narrow column react...
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| Format: | Article |
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Frontiers Media S.A.
2018-03-01
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| Series: | Frontiers in Systems Neuroscience |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fnsys.2018.00006/full |
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| author | Jun Sun An Qi Xu Julia Giraud Haiko Poppinga Thomas Riemensperger André Fiala Serge Birman |
| author_facet | Jun Sun An Qi Xu Julia Giraud Haiko Poppinga Thomas Riemensperger André Fiala Serge Birman |
| author_sort | Jun Sun |
| collection | DOAJ |
| description | Startle-induced locomotion is commonly used in Drosophila research to monitor locomotor reactivity and its progressive decline with age or under various neuropathological conditions. A widely used paradigm is startle-induced negative geotaxis (SING), in which flies entrapped in a narrow column react to a gentle mechanical shock by climbing rapidly upwards. Here we combined in vivo manipulation of neuronal activity and splitGFP reconstitution across cells to search for brain neurons and putative circuits that regulate this behavior. We show that the activity of specific clusters of dopaminergic neurons (DANs) afferent to the mushroom bodies (MBs) modulates SING, and that DAN-mediated SING regulation requires expression of the DA receptor Dop1R1/Dumb, but not Dop1R2/Damb, in intrinsic MB Kenyon cells (KCs). We confirmed our previous observation that activating the MB α'β', but not αβ, KCs decreased the SING response, and we identified further MB neurons implicated in SING control, including KCs of the γ lobe and two subtypes of MB output neurons (MBONs). We also observed that co-activating the αβ KCs antagonizes α'β' and γ KC-mediated SING modulation, suggesting the existence of subtle regulation mechanisms between the different MB lobes in locomotion control. Overall, this study contributes to an emerging picture of the brain circuits modulating locomotor reactivity in Drosophila that appear both to overlap and differ from those underlying associative learning and memory, sleep/wake state and stress-induced hyperactivity. |
| first_indexed | 2024-12-21T05:44:23Z |
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| institution | Directory Open Access Journal |
| issn | 1662-5137 |
| language | English |
| last_indexed | 2024-12-21T05:44:23Z |
| publishDate | 2018-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Systems Neuroscience |
| spelling | doaj.art-02f07db3da7e4b1e93238878d68c3dbb2022-12-21T19:14:09ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372018-03-011210.3389/fnsys.2018.00006311299Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in DrosophilaJun Sun0An Qi Xu1Julia Giraud2Haiko Poppinga3Thomas Riemensperger4André Fiala5Serge Birman6Genes Circuits Rhythms and Neuropathology, Brain Plasticity Unit, Centre National de la Recherche Scientifique, PSL Research University, ESPCI Paris, Paris, FranceGenes Circuits Rhythms and Neuropathology, Brain Plasticity Unit, Centre National de la Recherche Scientifique, PSL Research University, ESPCI Paris, Paris, FranceGenes Circuits Rhythms and Neuropathology, Brain Plasticity Unit, Centre National de la Recherche Scientifique, PSL Research University, ESPCI Paris, Paris, FranceDepartment of Molecular Neurobiology of Behavior, Johann-Friedrich-Blumenbach-Institute for Zoology and Anthropology, University of Göttingen, Göttingen, GermanyDepartment of Molecular Neurobiology of Behavior, Johann-Friedrich-Blumenbach-Institute for Zoology and Anthropology, University of Göttingen, Göttingen, GermanyDepartment of Molecular Neurobiology of Behavior, Johann-Friedrich-Blumenbach-Institute for Zoology and Anthropology, University of Göttingen, Göttingen, GermanyGenes Circuits Rhythms and Neuropathology, Brain Plasticity Unit, Centre National de la Recherche Scientifique, PSL Research University, ESPCI Paris, Paris, FranceStartle-induced locomotion is commonly used in Drosophila research to monitor locomotor reactivity and its progressive decline with age or under various neuropathological conditions. A widely used paradigm is startle-induced negative geotaxis (SING), in which flies entrapped in a narrow column react to a gentle mechanical shock by climbing rapidly upwards. Here we combined in vivo manipulation of neuronal activity and splitGFP reconstitution across cells to search for brain neurons and putative circuits that regulate this behavior. We show that the activity of specific clusters of dopaminergic neurons (DANs) afferent to the mushroom bodies (MBs) modulates SING, and that DAN-mediated SING regulation requires expression of the DA receptor Dop1R1/Dumb, but not Dop1R2/Damb, in intrinsic MB Kenyon cells (KCs). We confirmed our previous observation that activating the MB α'β', but not αβ, KCs decreased the SING response, and we identified further MB neurons implicated in SING control, including KCs of the γ lobe and two subtypes of MB output neurons (MBONs). We also observed that co-activating the αβ KCs antagonizes α'β' and γ KC-mediated SING modulation, suggesting the existence of subtle regulation mechanisms between the different MB lobes in locomotion control. Overall, this study contributes to an emerging picture of the brain circuits modulating locomotor reactivity in Drosophila that appear both to overlap and differ from those underlying associative learning and memory, sleep/wake state and stress-induced hyperactivity.http://journal.frontiersin.org/article/10.3389/fnsys.2018.00006/fulldopaminemushroom bodiesstartle-induced negative geotaxisneural circuitsDrosophila melanogaster |
| spellingShingle | Jun Sun An Qi Xu Julia Giraud Haiko Poppinga Thomas Riemensperger André Fiala Serge Birman Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in Drosophila Frontiers in Systems Neuroscience dopamine mushroom bodies startle-induced negative geotaxis neural circuits Drosophila melanogaster |
| title | Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in Drosophila |
| title_full | Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in Drosophila |
| title_fullStr | Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in Drosophila |
| title_full_unstemmed | Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in Drosophila |
| title_short | Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in Drosophila |
| title_sort | neural control of startle induced locomotion by the mushroom bodies and associated neurons in drosophila |
| topic | dopamine mushroom bodies startle-induced negative geotaxis neural circuits Drosophila melanogaster |
| url | http://journal.frontiersin.org/article/10.3389/fnsys.2018.00006/full |
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