The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connections
The ellipsoid body (EB) in the Drosophila brain is a central complex (CX) substructure that harbors circumferentially laminated ring (R) neuron axons and mediates multifaceted sensory integration and motor coordination functions. However, what regulates R axon lamination and how lamination affects R...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-06-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/25328 |
| _version_ | 1811181413408440320 |
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| author | Xiaojun Xie Masashi Tabuchi Matthew P Brown Sarah P Mitchell Mark N Wu Alex L Kolodkin |
| author_facet | Xiaojun Xie Masashi Tabuchi Matthew P Brown Sarah P Mitchell Mark N Wu Alex L Kolodkin |
| author_sort | Xiaojun Xie |
| collection | DOAJ |
| description | The ellipsoid body (EB) in the Drosophila brain is a central complex (CX) substructure that harbors circumferentially laminated ring (R) neuron axons and mediates multifaceted sensory integration and motor coordination functions. However, what regulates R axon lamination and how lamination affects R neuron function remain unknown. We show here that the EB is sequentially innervated by small-field and large-field neurons and that early developing EB neurons play an important regulatory role in EB laminae formation. The transmembrane proteins semaphorin-1a (Sema-1a) and plexin A function together to regulate R axon lamination. R neurons recruit both GABA and GABA-A receptors to their axon terminals in the EB, and optogenetic stimulation coupled with electrophysiological recordings show that Sema-1a-dependent R axon lamination is required for preventing the spread of synaptic inhibition between adjacent EB lamina. These results provide direct evidence that EB lamination is critical for local pre-synaptic inhibitory circuit organization. |
| first_indexed | 2024-04-11T09:17:21Z |
| format | Article |
| id | doaj.art-b384610d767a44a4b0a67bf884da1a2e |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:17:21Z |
| publishDate | 2017-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-b384610d767a44a4b0a67bf884da1a2e2022-12-22T04:32:18ZengeLife Sciences Publications LtdeLife2050-084X2017-06-01610.7554/eLife.25328The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connectionsXiaojun Xie0https://orcid.org/0000-0003-3459-6095Masashi Tabuchi1Matthew P Brown2Sarah P Mitchell3Mark N Wu4Alex L Kolodkin5https://orcid.org/0000-0001-7562-5513The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States; Howard Hughes Medical Institute, The Johns Hopkins University School of Medicine, Baltimore, United StatesDepartment of Neurology, The Johns Hopkins University School of Medicine, Baltimore, United StatesThe Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States; Howard Hughes Medical Institute, The Johns Hopkins University School of Medicine, Baltimore, United StatesThe Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States; Howard Hughes Medical Institute, The Johns Hopkins University School of Medicine, Baltimore, United StatesThe Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States; Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, United StatesThe Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States; Howard Hughes Medical Institute, The Johns Hopkins University School of Medicine, Baltimore, United StatesThe ellipsoid body (EB) in the Drosophila brain is a central complex (CX) substructure that harbors circumferentially laminated ring (R) neuron axons and mediates multifaceted sensory integration and motor coordination functions. However, what regulates R axon lamination and how lamination affects R neuron function remain unknown. We show here that the EB is sequentially innervated by small-field and large-field neurons and that early developing EB neurons play an important regulatory role in EB laminae formation. The transmembrane proteins semaphorin-1a (Sema-1a) and plexin A function together to regulate R axon lamination. R neurons recruit both GABA and GABA-A receptors to their axon terminals in the EB, and optogenetic stimulation coupled with electrophysiological recordings show that Sema-1a-dependent R axon lamination is required for preventing the spread of synaptic inhibition between adjacent EB lamina. These results provide direct evidence that EB lamination is critical for local pre-synaptic inhibitory circuit organization.https://elifesciences.org/articles/25328neural laminationsemaphorinellipsoid bodycentral complex |
| spellingShingle | Xiaojun Xie Masashi Tabuchi Matthew P Brown Sarah P Mitchell Mark N Wu Alex L Kolodkin The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connections eLife neural lamination semaphorin ellipsoid body central complex |
| title | The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connections |
| title_full | The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connections |
| title_fullStr | The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connections |
| title_full_unstemmed | The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connections |
| title_short | The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connections |
| title_sort | laminar organization of the drosophila ellipsoid body is semaphorin dependent and prevents the formation of ectopic synaptic connections |
| topic | neural lamination semaphorin ellipsoid body central complex |
| url | https://elifesciences.org/articles/25328 |
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