Cargando…

Serotonergic modulation of visual neurons in Drosophila melanogaster

Sensory systems rely on neuromodulators, such as serotonin, to provide flexibility for information processing as stimuli vary, such as light intensity throughout the day. Serotonergic neurons broadly innervate the optic ganglia of Drosophila melanogaster, a widely used model for studying vision. It...

Descripción completa

Detalles Bibliográficos
Autores principales: Sampson, Maureen M., Myers Gschweng, Katherine M., Hardcastle, Ben J., Bonanno, Shivan L., Sizemore, Tyler R., Arnold, Rebecca C., Gao, Fuying, Dacks, Andrew M., Frye, Mark A., Krantz, David E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7485980/
https://www.ncbi.nlm.nih.gov/pubmed/32866139
http://dx.doi.org/10.1371/journal.pgen.1009003
_version_ 1783581254922272768
author Sampson, Maureen M.
Myers Gschweng, Katherine M.
Hardcastle, Ben J.
Bonanno, Shivan L.
Sizemore, Tyler R.
Arnold, Rebecca C.
Gao, Fuying
Dacks, Andrew M.
Frye, Mark A.
Krantz, David E.
author_facet Sampson, Maureen M.
Myers Gschweng, Katherine M.
Hardcastle, Ben J.
Bonanno, Shivan L.
Sizemore, Tyler R.
Arnold, Rebecca C.
Gao, Fuying
Dacks, Andrew M.
Frye, Mark A.
Krantz, David E.
author_sort Sampson, Maureen M.
collection PubMed
description Sensory systems rely on neuromodulators, such as serotonin, to provide flexibility for information processing as stimuli vary, such as light intensity throughout the day. Serotonergic neurons broadly innervate the optic ganglia of Drosophila melanogaster, a widely used model for studying vision. It remains unclear whether serotonin modulates the physiology of interneurons in the optic ganglia. To address this question, we first mapped the expression patterns of serotonin receptors in the visual system, focusing on a subset of cells with processes in the first optic ganglion, the lamina. Serotonin receptor expression was found in several types of columnar cells in the lamina including 5-HT2B in lamina monopolar cell L2, required for spatiotemporal luminance contrast, and both 5-HT1A and 5-HT1B in T1 cells, whose function is unknown. Subcellular mapping with GFP-tagged 5-HT2B and 5-HT1A constructs indicated that these receptors localize to layer M2 of the medulla, proximal to serotonergic boutons, suggesting that the medulla neuropil is the primary site of serotonergic regulation for these neurons. Exogenous serotonin increased basal intracellular calcium in L2 terminals in layer M2 and modestly decreased the duration of visually induced calcium transients in L2 neurons following repeated dark flashes, but otherwise did not alter the calcium transients. Flies without functional 5-HT2B failed to show an increase in basal calcium in response to serotonin. 5-HT2B mutants also failed to show a change in amplitude in their response to repeated light flashes but other calcium transient parameters were relatively unaffected. While we did not detect serotonin receptor expression in L1 neurons, they, like L2, underwent serotonin-induced changes in basal calcium, presumably via interactions with other cells. These data demonstrate that serotonin modulates the physiology of interneurons involved in early visual processing in Drosophila.
format Online
Article
Text
id pubmed-7485980
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-74859802020-09-21 Serotonergic modulation of visual neurons in Drosophila melanogaster Sampson, Maureen M. Myers Gschweng, Katherine M. Hardcastle, Ben J. Bonanno, Shivan L. Sizemore, Tyler R. Arnold, Rebecca C. Gao, Fuying Dacks, Andrew M. Frye, Mark A. Krantz, David E. PLoS Genet Research Article Sensory systems rely on neuromodulators, such as serotonin, to provide flexibility for information processing as stimuli vary, such as light intensity throughout the day. Serotonergic neurons broadly innervate the optic ganglia of Drosophila melanogaster, a widely used model for studying vision. It remains unclear whether serotonin modulates the physiology of interneurons in the optic ganglia. To address this question, we first mapped the expression patterns of serotonin receptors in the visual system, focusing on a subset of cells with processes in the first optic ganglion, the lamina. Serotonin receptor expression was found in several types of columnar cells in the lamina including 5-HT2B in lamina monopolar cell L2, required for spatiotemporal luminance contrast, and both 5-HT1A and 5-HT1B in T1 cells, whose function is unknown. Subcellular mapping with GFP-tagged 5-HT2B and 5-HT1A constructs indicated that these receptors localize to layer M2 of the medulla, proximal to serotonergic boutons, suggesting that the medulla neuropil is the primary site of serotonergic regulation for these neurons. Exogenous serotonin increased basal intracellular calcium in L2 terminals in layer M2 and modestly decreased the duration of visually induced calcium transients in L2 neurons following repeated dark flashes, but otherwise did not alter the calcium transients. Flies without functional 5-HT2B failed to show an increase in basal calcium in response to serotonin. 5-HT2B mutants also failed to show a change in amplitude in their response to repeated light flashes but other calcium transient parameters were relatively unaffected. While we did not detect serotonin receptor expression in L1 neurons, they, like L2, underwent serotonin-induced changes in basal calcium, presumably via interactions with other cells. These data demonstrate that serotonin modulates the physiology of interneurons involved in early visual processing in Drosophila. Public Library of Science 2020-08-31 /pmc/articles/PMC7485980/ /pubmed/32866139 http://dx.doi.org/10.1371/journal.pgen.1009003 Text en © 2020 Sampson et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Sampson, Maureen M.
Myers Gschweng, Katherine M.
Hardcastle, Ben J.
Bonanno, Shivan L.
Sizemore, Tyler R.
Arnold, Rebecca C.
Gao, Fuying
Dacks, Andrew M.
Frye, Mark A.
Krantz, David E.
Serotonergic modulation of visual neurons in Drosophila melanogaster
title Serotonergic modulation of visual neurons in Drosophila melanogaster
title_full Serotonergic modulation of visual neurons in Drosophila melanogaster
title_fullStr Serotonergic modulation of visual neurons in Drosophila melanogaster
title_full_unstemmed Serotonergic modulation of visual neurons in Drosophila melanogaster
title_short Serotonergic modulation of visual neurons in Drosophila melanogaster
title_sort serotonergic modulation of visual neurons in drosophila melanogaster
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7485980/
https://www.ncbi.nlm.nih.gov/pubmed/32866139
http://dx.doi.org/10.1371/journal.pgen.1009003
work_keys_str_mv AT sampsonmaureenm serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT myersgschwengkatherinem serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT hardcastlebenj serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT bonannoshivanl serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT sizemoretylerr serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT arnoldrebeccac serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT gaofuying serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT dacksandrewm serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT fryemarka serotonergicmodulationofvisualneuronsindrosophilamelanogaster
AT krantzdavide serotonergicmodulationofvisualneuronsindrosophilamelanogaster