Serotonergic modulation of visual neurons in Drosophila melanogaster
Autoři:
Maureen M. Sampson aff001; Katherine M. Myers Gschweng aff001; Ben J. Hardcastle aff004; Shivan L. Bonanno aff001; Tyler R. Sizemore aff005; Rebecca C. Arnold aff001; Fuying Gao aff003; Andrew M. Dacks aff005; Mark A. Frye aff004; David E. Krantz aff001
Působiště autorů:
UCLA, Hatos Center for Neuropharmacology, Los Angeles, CA, United States of America
aff001; UCLA, Molecular Toxicology Interdepartmental Program, Los Angeles, CA, United States of America
aff002; UCLA, Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, David Geffen School of Medicine, Los Angeles, CA, United States of America
aff003; UCLA, Department of Integrative Biology and Physiology, Los Angeles, CA, United States of America
aff004; Department of Biology, West Virginia University, Morgantown, WV, United States of America
aff005
Vyšlo v časopise:
Serotonergic modulation of visual neurons in Drosophila melanogaster. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1009003
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009003
Souhrn
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.
Klíčová slova:
Drosophila melanogaster – Neurons – Neuropil – Receptor physiology – Serotonin – Serotonin receptors – Vision – Optic lobes
Zdroje
1. Kupfermann I. Modulatory actions of neurotransmitters. Annual review of neuroscience. 1979;2:447–65. doi: 10.1146/annurev.ne.02.030179.002311 44174
2. Marder E. Neuromodulation of neuronal circuits: back to the future. Neuron. 2012;76(1):1–11. doi: 10.1016/j.neuron.2012.09.010 23040802
3. Marder E, O'Leary T, Shruti S. Neuromodulation of circuits with variable parameters: single neurons and small circuits reveal principles of state-dependent and robust neuromodulation. Annual review of neuroscience. 2014;37:329–46. doi: 10.1146/annurev-neuro-071013-013958 25032499
4. Nadim F, Bucher D. Neuromodulation of neurons and synapses. Current opinion in neurobiology. 2014;29:48–56. doi: 10.1016/j.conb.2014.05.003 24907657
5. Katz PS. Beyond Neurotransmission: Neuromodulation and its Importance for Information Processing. Oxford; New York: Oxford University Press; 1999. xiii, 391 p. p.
6. Moreau AW, Amar M, Le Roux N, Morel N, Fossier P. Serotoninergic fine-tuning of the excitation-inhibition balance in rat visual cortical networks. Cereb cortex. 2010;20(2):456–67. doi: 10.1093/cercor/bhp114 19520765
7. Arechiga H, Banuelos E, Frixione E, Picones A, Rodriguez-Sosa L. Modulation of crayfish retinal sensitivity by 5-hydroxytryptamine. The Journal of experimental biology. 1990;150:123–43. 2355208
8. Seillier L, Lorenz C, Kawaguchi K, Ott T, Nieder A, Pourriahi P, et al. Serotonin Decreases the Gain of Visual Responses in Awake Macaque V1. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2017;37(47):11390–405.
9. Kloppenburg P, Ferns D, Mercer AR. Serotonin enhances central olfactory neuron responses to female sex pheromone in the male sphinx moth manduca sexta. The Journal of neuroscience: the official journal of the Society for Neuroscience. 1999;19(19):8172–81.
10. Dacks AM, Christensen TA, Hildebrand JG. Modulation of olfactory information processing in the antennal lobe of Manduca sexta by serotonin. Journal of neurophysiology. 2008;99(5):2077–85. doi: 10.1152/jn.01372.2007 18322001
11. Lottem E, Lorincz ML, Mainen ZF. Optogenetic Activation of Dorsal Raphe Serotonin Neurons Rapidly Inhibits Spontaneous But Not Odor-Evoked Activity in Olfactory Cortex. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2016;36(1):7–18.
12. Brunert D, Tsuno Y, Rothermel M, Shipley MT, Wachowiak M. Cell-Type-Specific Modulation of Sensory Responses in Olfactory Bulb Circuits by Serotonergic Projections from the Raphe Nuclei. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2016;36(25):6820–35.
13. Petzold GC, Hagiwara A, Murthy VN. Serotonergic modulation of odor input to the mammalian olfactory bulb. Nature neuroscience. 2009;12(6):784–91. doi: 10.1038/nn.2335 19430472
14. Papesh MA, Hurley LM. Modulation of auditory brainstem responses by serotonin and specific serotonin receptors. Hearing research. 2016;332:121–36. doi: 10.1016/j.heares.2015.11.014 26688176
15. Fotowat H, Harvey-Girard E, Cheer JF, Krahe R, Maler L. Subsecond Sensory Modulation of Serotonin Levels in a Primary Sensory Area and Its Relation to Ongoing Communication Behavior in a Weakly Electric Fish. eNeuro. 2016;3(5).
16. Andres M, Seifert M, Spalthoff C, Warren B, Weiss L, Giraldo D, et al. Auditory Efferent System Modulates Mosquito Hearing. Current biology: CB. 2016;26(15):2028–36. doi: 10.1016/j.cub.2016.05.077 27476597
17. Watakabe A, Komatsu Y, Sadakane O, Shimegi S, Takahata T, Higo N, et al. Enriched expression of serotonin 1B and 2A receptor genes in macaque visual cortex and their bidirectional modulatory effects on neuronal responses. Cereb cortex. 2009;19(8):1915–28. doi: 10.1093/cercor/bhn219 19056862
18. Gagolewicz PJ, Dringenberg HC. Age-Dependent Switch of the Role of Serotonergic 5-HT1A Receptors in Gating Long-Term Potentiation in Rat Visual Cortex In Vivo. Neural plast. 2016;2016:6404082. doi: 10.1155/2016/6404082 27247804
19. Lombaert N, Hennes M, Gilissen S, Schevenels G, Aerts L, Vanlaer R, et al. 5-HTR2A and 5-HTR3A but not 5-HTR1A antagonism impairs the cross-modal reactivation of deprived visual cortex in adulthood. Mol brain. 2018;11(1):65. doi: 10.1186/s13041-018-0404-5 30400993
20. Gu Q, Singer W. Involvement of serotonin in developmental plasticity of kitten visual cortex. Eur J Neurosci. 1995;7(6):1146–53. doi: 10.1111/j.1460-9568.1995.tb01104.x 7582087
21. Wang Y, Gu Q, Cynader MS. Blockade of serotonin-2C receptors by mesulergine reduces ocular dominance plasticity in kitten visual cortex. Exp brain res. 1997;114(2):321–8. doi: 10.1007/pl00005640 9166921
22. Shimegi S, Kimura A, Sato A, Aoyama C, Mizuyama R, Tsunoda K, et al. Cholinergic and serotonergic modulation of visual information processing in monkey V1. Journal of physiology, Paris. 2016;110(1–2):44–51. doi: 10.1016/j.jphysparis.2016.09.001 27619519
23. Zhou X, Zhang R, Zhang S, Wu J, Sun X. Activation of 5-HT1A receptors promotes retinal ganglion cell function by inhibiting the cAMP-PKA pathway to modulate presynaptic GABA release in chronic glaucoma. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2018.
24. Trakhtenberg EF, Pita-Thomas W, Fernandez SG, Patel KH, Venugopalan P, Shechter JM, et al. Serotonin receptor 2C regulates neurite growth and is necessary for normal retinal processing of visual information. Developmental neurobiology. 2017;77(4):419–37. doi: 10.1002/dneu.22391 26999672
25. Borst A, Helmstaedter M. Common circuit design in fly and mammalian motion vision. Nature neuroscience. 2015;18(8):1067–76. doi: 10.1038/nn.4050 26120965
26. Cheng KY, Frye MA. Neuromodulation of insect motion vision. Journal of comparative physiology A, Neuroethology, sensory, neural, and behavioral physiology. 2019.
27. Meinertzhagen IA, O'Neil SD. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. The Journal of comparative neurology. 1991;305(2):232–63. doi: 10.1002/cne.903050206 1902848
28. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A. ON and OFF pathways in Drosophila motion vision. Nature. 2010;468(7321):300–4. doi: 10.1038/nature09545 21068841
29. Strother JA, Nern A, Reiser MB. Direct observation of ON and OFF pathways in the Drosophila visual system. Current biology: CB. 2014;24(9):976–83. doi: 10.1016/j.cub.2014.03.017 24704075
30. Clark DA, Bursztyn L, Horowitz MA, Schnitzer MJ, Clandinin TR. Defining the computational structure of the motion detector in Drosophila. Neuron. 2011;70(6):1165–77. doi: 10.1016/j.neuron.2011.05.023 21689602
31. Yang HH, St-Pierre F, Sun X, Ding X, Lin MZ, Clandinin TR. Subcellular Imaging of Voltage and Calcium Signals Reveals Neural Processing In Vivo. Cell. 2016;166(1):245–57. doi: 10.1016/j.cell.2016.05.031 27264607
32. Zheng L, de Polavieja GG, Wolfram V, Asyali MH, Hardie RC, Juusola M. Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila. The Journal of general physiology. 2006;127(5):495–510. doi: 10.1085/jgp.200509470 16636201
33. Behnia R, Desplan C. Visual circuits in flies: beginning to see the whole picture. Current opinion in neurobiology. 2015;34:125–32. doi: 10.1016/j.conb.2015.03.010 25881091
34. Bahl A, Serbe E, Meier M, Ammer G, Borst A. Neural Mechanisms for Drosophila Contrast Vision. Neuron. 2015;88(6):1240–52. doi: 10.1016/j.neuron.2015.11.004 26673659
35. Rivera-Alba M, Vitaladevuni SN, Mishchenko Y, Lu Z, Takemura SY, Scheffer L, et al. Wiring economy and volume exclusion determine neuronal placement in the Drosophila brain. Current biology: CB. 2011;21(23):2000–5. doi: 10.1016/j.cub.2011.10.022 22119527
36. Takemura SY, Lu Z, Meinertzhagen IA. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. The Journal of comparative neurology. 2008;509(5):493–513. doi: 10.1002/cne.21757 18537121
37. Takemura SY, Bharioke A, Lu Z, Nern A, Vitaladevuni S, Rivlin PK, et al. A visual motion detection circuit suggested by Drosophila connectomics. Nature. 2013;500(7461):175–81. doi: 10.1038/nature12450 23925240
38. Takemura SY, Xu CS, Lu Z, Rivlin PK, Parag T, Olbris DJ, et al. Synaptic circuits and their variations within different columns in the visual system of Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(44):13711–6. doi: 10.1073/pnas.1509820112 26483464
39. Takemura SY, Nern A, Chklovskii DB, Scheffer LK, Rubin GM, Meinertzhagen IA. The comprehensive connectome of a neural substrate for 'ON' motion detection in. Elife. 2017;6.
40. Shinomiya K, Huang G, Lu Z, Parag T, Xu CS, Aniceto R, et al. Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain. Elife. 2019;8.
41. Wasserman SM, Aptekar JW, Lu P, Nguyen J, Wang AL, Keles MF, et al. Olfactory neuromodulation of motion vision circuitry in Drosophila. Current biology: CB. 2015;25(4):467–72. doi: 10.1016/j.cub.2014.12.012 25619767
42. Strother JA, Wu ST, Rogers EM, Eliason JLM, Wong AM, Nern A, et al. Behavioral state modulates the ON visual motion pathway of Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2018;115(1):E102–E11. doi: 10.1073/pnas.1703090115 29255026
43. Cheng KY, Colbath RA, Frye MA. Olfactory and Neuromodulatory Signals Reverse Visual Object Avoidance to Approach in Drosophila. Current biology: CB. 2019;29(12):2058–65 e2. doi: 10.1016/j.cub.2019.05.010 31155354
44. Hevers W, Hardie RC. Serotonin modulates the voltage dependence of delayed rectifier and Shaker potassium channels in Drosophila photoreceptors. Neuron. 1995;14:845–56. doi: 10.1016/0896-6273(95)90228-7 7718246
45. Kloppenburg P, Erber J. The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.) II. Electrophysiological analysis of motion-sensitive neurons in the lobula. Journal of comparative physiology A, Neuroethology, sensory, neural, and behavioral physiology. 1995;176:119–29.
46. Suver MP, Mamiya A, Dickinson MH. Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Current biology: CB. 2012;22(24):2294–302. doi: 10.1016/j.cub.2012.10.034 23142045
47. Leitinger G, Pabst MA, Kral K. Serotonin-immunoreactive neurones in the visual system of the praying mantis: an immunohistochemical, confocal laser scanning and electron microscopic study. Brain res. 1999;823(1–2):11–23. doi: 10.1016/s0006-8993(98)01339-0 10095007
48. Nässel DR, Meyer EP, Klemm N. Mapping and ultrastructure of serotonin-immunoreactive neurons in the optic lobes of three insect species. The Journal of comparative neurology. 1985;232(2):190–204. doi: 10.1002/cne.902320205 3973090
49. Nässel DR, Ohlsson L, Sivasubramanian P. Postembryonic differentiation of serotonin-immunoreactive neurons in fleshfly optic lobes developing in situ or cultured in vivo without eye discs. The Journal of comparative neurology. 1987;255(3):327–40. doi: 10.1002/cne.902550302 3546409
50. Valles AM, White K. Serotonin-containing neurons in Drosophila melanogaster: development and distribution. The Journal of comparative neurology. 1988;268(3):414–28. doi: 10.1002/cne.902680310 3129459
51. Hamanaka Y, Kinoshita M, Homberg U, Arikawa K. Immunocytochemical localization of amines and GABA in the optic lobe of the butterfly, Papilio xuthus. PloS one. 2012;7(7):e41109. doi: 10.1371/journal.pone.0041109 22844431
52. Schafer S, Bicker G. Common projection areas of 5-HT- and GABA-like immunoreactive fibers in the visual system of the honeybee. Brain res. 1986;380(2):368–70. doi: 10.1016/0006-8993(86)90237-4 3530374
53. Chen B, Meinertzhagen IA, Shaw SR. Circadian rhythms in light-evoked responses of the fly's compound eye, and the effects of neuromodulators 5-HT and the peptide PDF. J comp physiol [A]. 1999;185:393–404.
54. Ichikawa T. Light suppresses the activity of serotonin-immunoreactive neurons in the optic lobe of the swallowtail butterfly. Neurosci lett. 1994;172(1–2):115–8. doi: 10.1016/0304-3940(94)90675-0 8084513
55. Nichols CD. 5-HT2 receptors in Drosophila are expressed in the brain and modulate aspects of circadian behaviors. Developmental neurobiology. 2007;67(6):752–63. doi: 10.1002/dneu.20370 17443822
56. Yuan Q, Lin F, Zheng X, Sehgal A. Serotonin modulates circadian entrainment in Drosophila. Neuron. 2005;47(1):115–27. doi: 10.1016/j.neuron.2005.05.027 15996552
57. Helfrich-Forster C. Light input pathways to the circadian clock of insects with an emphasis on the fruit fly Drosophila melanogaster. Journal of comparative physiology A, Neuroethology, sensory, neural, and behavioral physiology. 2020;206(2):259–72. doi: 10.1007/s00359-019-01379-5 31691095
58. Helfrich-Forster C, Winter C, Hofbauer A, Hall JC, Stanewsky R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron. 2001;30(1):249–61. doi: 10.1016/s0896-6273(01)00277-x 11343659
59. Pyza E, Meinertzhagen IA. Neurotransmitters regulate rhythmic size changes amongst cells in the fly's optic lobe. Journal of comparative physiology A, Sensory, neural, and behavioral physiology. 1996;178(1):33–45. doi: 10.1007/BF00189588 8568723
60. Tomioka K, Ikeda M, Nagao T, Tamotsu S. Involvement of serotonin in the circadian rhythm of an insect visual system. Naturwissenschaften. 1993;80(3):137–9.
61. Nichols DE, Nichols CD. Serotonin receptors. Chemical reviews. 2008;108(5):1614–41. doi: 10.1021/cr078224o 18476671
62. McCorvy JD, Roth BL. Structure and function of serotonin G protein-coupled receptors. Pharmacology & therapeutics. 2015;150:129–42.
63. Maroteaux L, Bechade C, Roumier A. Dimers of serotonin receptors: Impact on ligand affinity and signaling. Biochimie. 2019;161:23–33. doi: 10.1016/j.biochi.2019.01.009 30685449
64. Araneda R, Andrade R. 5-Hydroxytryptamine2 and 5-hydroxytryptamine 1A receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience. 1991;40(2):399–412. doi: 10.1016/0306-4522(91)90128-b 1851255
65. Celada P, Puig MV, Artigas F. Serotonin modulation of cortical neurons and networks. Frontiers in integrative neuroscience. 2013;7:25. doi: 10.3389/fnint.2013.00025 23626526
66. Elliott MC, Tanaka PM, Schwark RW, Andrade R. Serotonin Differentially Regulates L5 Pyramidal Cell Classes of the Medial Prefrontal Cortex in Rats and Mice. eNeuro. 2018;5(1).
67. Llado-Pelfort L, Santana N, Ghisi V, Artigas F, Celada P. 5-HT1A receptor agonists enhance pyramidal cell firing in prefrontal cortex through a preferential action on GABA interneurons. Cereb cortex. 2012;22(7):1487–97. doi: 10.1093/cercor/bhr220 21893679
68. Gao M, Der-Ghazarian TS, Li S, Qiu S, Neisewander JL, Wu J. Dual Effect of 5-HT1B/1D Receptors on Dopamine Neurons in Ventral Tegmental Area: Implication for the Functional Switch After Chronic Cocaine Exposure. Biol psychiatry. 2020.
69. Del Rosario JS, Yudin Y, Su S, Hartle CM, Mirshahi T, Rohacs T. Gi-coupled receptor activation potentiates Piezo2 currents via Gbetagamma. EMBO Rep. 2020;21(5):e49124. doi: 10.15252/embr.201949124 32227462
70. Davis FP, Nern A, Picard S, Reiser MB, Rubin GM, Eddy SR, et al. A genetic, genomic, and computational resource for exploring neural circuit function. Elife. 2020;9.
71. Konstantinides N, Kapuralin K, Fadil C, Barboza L, Satija R, Desplan C. Phenotypic Convergence: Distinct Transcription Factors Regulate Common Terminal Features. Cell. 2018;174(3):622–35 e13. doi: 10.1016/j.cell.2018.05.021 29909983
72. Colas JF, Launay JM, Kellermann O, Rosay P, Maroteaux L. Drosophila 5-HT2 serotonin receptor: coexpression with fushi-tarazu during segmentation. Proceedings of the National Academy of Sciences of the United States of America. 1995;92(12):5441–5. doi: 10.1073/pnas.92.12.5441 7777527
73. Gasque G, Conway S, Huang J, Rao Y, Vosshall LB. Small molecule drug screening in Drosophila identifies the 5HT2A receptor as a feeding modulation target. Scientific reports. 2013;3:srep02120. doi: 10.1038/srep02120 23817146
74. Saudou F, Boschert U, Amlaiky N, Plassat JL, Hen R. A family of Drosophila serotonin receptors with distinct intracellular signalling properties and expression patterns. The EMBO journal. 1992;11(1):7–17. 1310937
75. Witz P, Amlaiky N, Plassat JL, Maroteaux L, Borrelli E, Hen R. Cloning and characterization of a Drosophila serotonin receptor that activates adenylate cyclase. Proceedings of the National Academy of Sciences of the United States of America. 1990;87(22):8940–4. doi: 10.1073/pnas.87.22.8940 2174167
76. Blenau W, Daniel S, Balfanz S, Thamm M, Baumann A. Dm5-HT2B: Pharmacological Characterization of the Fifth Serotonin Receptor Subtype of Drosophila melanogaster. Front syst neurosci. 2017;11:28. doi: 10.3389/fnsys.2017.00028 28553207
77. Gnerer JP, Venken KJ, Dierick HA. Gene-specific cell labeling using MiMIC transposons. Nucleic acids research. 2015;43(8):e56. doi: 10.1093/nar/gkv113 25712101
78. Venken KJ, Schulze KL, Haelterman NA, Pan H, He Y, Evans-Holm M, et al. MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nature methods. 2011;8(9):737–43. doi: 10.1038/nmeth.1662 21985007
79. Diao F, Ironfield H, Luan H, Shropshire WC, Ewer J, Marr E, et al. Plug-and-play genetic access to drosophila cell types using exchangeable exon cassettes. Cell rep. 2015;10(8):1410–21. doi: 10.1016/j.celrep.2015.01.059 25732830
80. Fischbach KF, Dittrich APM. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild type structure. Cell tissue res. 1989;258:441–75.
81. Sanes JR, Zipursky SL. Design principles of insect and vertebrate visual systems. Neuron. 2010;66(1):15–36. doi: 10.1016/j.neuron.2010.01.018 20399726
82. Nern A, Pfeiffer BD, Rubin GM. Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(22):E2967–76. doi: 10.1073/pnas.1506763112 25964354
83. Edwards TN, Meinertzhagen IA. The functional organisation of glia in the adult brain of Drosophila and other insects. Progress in neurobiology. 2010;90(4):471–97. doi: 10.1016/j.pneurobio.2010.01.001 20109517
84. DeSalvo MK, Hindle SJ, Rusan ZM, Orng S, Eddison M, Halliwill K, et al. The Drosophila surface glia transcriptome: evolutionary conserved blood-brain barrier processes. Front neurosci. 2014;8:346. doi: 10.3389/fnins.2014.00346 25426014
85. Nässel DR. Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Progress in neurobiology. 1988;30(1):1–85. doi: 10.1016/0301-0082(88)90002-0 3275407
86. Xu L, He J, Kaiser A, Graber N, Schlager L, Ritze Y, et al. A Single Pair of Serotonergic Neurons Counteracts Serotonergic Inhibition of Ethanol Attraction in Drosophila. PloS one. 2016;11(12):e0167518. doi: 10.1371/journal.pone.0167518 27936023
87. Pooryasin A, Fiala A. Identified Serotonin-Releasing Neurons Induce Behavioral Quiescence and Suppress Mating in Drosophila. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2015;35(37):12792–812.
88. Sitaraman D, Zars M, Laferriere H, Chen YC, Sable-Smith A, Kitamoto T, et al. Serotonin is necessary for place memory in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(14):5579–84. doi: 10.1073/pnas.0710168105 18385379
89. Alekseyenko OV, Chan YB, Okaty BW, Chang Y, Dymecki SM, Kravitz EA. Serotonergic Modulation of Aggression in Drosophila Involves GABAergic and Cholinergic Opposing Pathways. Current biology: CB. 2019;29(13):2145–56 e5. doi: 10.1016/j.cub.2019.05.070 31231050
90. Tuthill JC, Nern A, Holtz SL, Rubin GM, Reiser MB. Contributions of the 12 neuron classes in the fly lamina to motion vision. Neuron. 2013;79(1):128–40. doi: 10.1016/j.neuron.2013.05.024 23849200
91. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nature protocols. 2008;3(6):1101–8. doi: 10.1038/nprot.2008.73 18546601
92. Deng B, Li Q, Liu X, Cao Y, Li B, Qian Y, et al. Chemoconnectomics: Mapping Chemical Transmission in Drosophila. Neuron. 2019;101(5):876–93 e4. doi: 10.1016/j.neuron.2019.01.045 30799021
93. Qian Y, Cao Y, Deng B, Yang G, Li J, Xu R, et al. Sleep homeostasis regulated by 5HT2b receptor in a small subset of neurons in the dorsal fan-shaped body of drosophila. Elife. 2017;6.
94. Macpherson LJ, Zaharieva EE, Kearney PJ, Alpert MH, Lin TY, Turan Z, et al. Dynamic labelling of neural connections in multiple colours by trans-synaptic fluorescence complementation. Nat commun. 2015;6:10024. doi: 10.1038/ncomms10024 26635273
95. Trueta C, De-Miguel FF. Extrasynaptic exocytosis and its mechanisms: a source of molecules mediating volume transmission in the nervous system. Frontiers in physiology. 2012;3:319. doi: 10.3389/fphys.2012.00319 22969726
96. Bunin MA, Wightman RM. Paracrine neurotransmission in the CNS: involvement of 5-HT. Trends neurosci. 1999;22(9):377–82. doi: 10.1016/s0166-2236(99)01410-1 10441294
97. Vizi ES, Fekete A, Karoly R, Mike A. Non-synaptic receptors and transporters involved in brain functions and targets of drug treatment. British journal of pharmacology. 2010;160(4):785–809. doi: 10.1111/j.1476-5381.2009.00624.x 20136842
98. Fuxe K, Dahlstrom AB, Jonsson G, Marcellino D, Guescini M, Dam M, et al. The discovery of central monoamine neurons gave volume transmission to the wired brain. Progress in neurobiology. 2010;90(2):82–100. doi: 10.1016/j.pneurobio.2009.10.012 19853007
99. Liu C, Meng Z, Wiggin TD, Yu J, Reed ML, Guo F, et al. A Serotonin-Modulated Circuit Controls Sleep Architecture to Regulate Cognitive Function Independent of Total Sleep in Drosophila. Current biology: CB. 2019;29(21):3635–46 e5. doi: 10.1016/j.cub.2019.08.079 31668619
100. Zhang X, Gaudry Q. Functional integration of a serotonergic neuron in the Drosophila antennal lobe. Elife. 2016;5.
101. Hoyer D, Hannon JP, Martin GR. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol biochem behav. 2002;71(4):533–54. doi: 10.1016/s0091-3057(01)00746-8 11888546
102. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature. 2013;499(7458):295–300. doi: 10.1038/nature12354 23868258
103. Narahashi T. Tetrodotoxin: a brief history. Proc Jpn Acad ser B Phys biol sci. 2008;84(5):147–54. doi: 10.2183/pjab.84.147 18941294
104. Narahashi T, Moore JW, Scott WR. Tetrodotoxin Blockage of Sodium Conductance Increase in Lobster Giant Axons. The Journal of general physiology. 1964;47:965–74. doi: 10.1085/jgp.47.5.965 14155438
105. Polter AM, Li X. 5-HT1A receptor-regulated signal transduction pathways in brain. Cell signal. 2010;22(10):1406–12. doi: 10.1016/j.cellsig.2010.03.019 20363322
106. Cao G, Platisa J, Pieribone VA, Raccuglia D, Kunst M, Nitabach MN. Genetically targeted optical electrophysiology in intact neural circuits. Cell. 2013;154(4):904–13. doi: 10.1016/j.cell.2013.07.027 23932121
107. Laughlin SB, Osorio D. Mechanisms for Neural Signal Enhancement in the Blowfly Compound Eye. Journal of experimental biology. 1989;144(1):113–46.
108. Reiff DF, Plett J, Mank M, Griesbeck O, Borst A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nature neuroscience. 2010;13(8):973–8. doi: 10.1038/nn.2595 20622873
109. Fisher YE, Yang HH, Isaacman-Beck J, Xie M, Gohl DM, Clandinin TR. FlpStop, a tool for conditional gene control in Drosophila. Elife. 2017;6.
110. Kolodziejczyk A, Sun X, Meinertzhagen IA, Nassel DR. Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PloS one. 2008;3(5):e2110. doi: 10.1371/journal.pone.0002110 18464935
111. Hong CS, Ganetzky B. Spatial and temporal expression patterns of two sodium channel genes in Drosophila. The Journal of neuroscience: the official journal of the Society for Neuroscience. 1994;14(9):5160–9.
112. Warmke JW, Reenan RA, Wang P, Qian S, Arena JP, Wang J, et al. Functional expression of Drosophila para sodium channels. Modulation by the membrane protein TipE and toxin pharmacology. The Journal of general physiology. 1997;110(2):119–33. doi: 10.1085/jgp.110.2.119 9236205
113. Mu L, Ito K, Bacon JP, Strausfeld NJ. Optic glomeruli and their inputs in Drosophila share an organizational ground pattern with the antennal lobes. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2012;32(18):6061–71.
114. Juusola M, Uusitalo RO, Weckstrom M. Transfer of graded potentials at the photoreceptor-interneuron synapse. The Journal of general physiology. 1995;105(1):117–48. doi: 10.1085/jgp.105.1.117 7537323
115. Uusitalo RO, Juusola M, Kouvalainen E, Weckstrom M. Tonic transmitter release in a graded potential synapse. Journal of neurophysiology. 1995;74(1):470–3. doi: 10.1152/jn.1995.74.1.470 7472349
116. Stenesen D, Moehlman AT, Schellinger JN, Rodan AR, Kramer H. The glial sodium-potassium-2-chloride cotransporter is required for synaptic transmission in the Drosophila visual system. Scientific reports. 2019;9(1):2475. doi: 10.1038/s41598-019-38850-x 30792494
117. Weckstrom M, Laughlin S. Extracellular potentials modify the transfer of information at photoreceptor output synapses in the blowfly compound eye. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2010;30(28):9557–66.
118. Nikolaev A, Zheng L, Wardill TJ, O'Kane CJ, de Polavieja GG, Juusola M. Network adaptation improves temporal representation of naturalistic stimuli in Drosophila eye: II mechanisms. PloS one. 2009;4(1):e4306. doi: 10.1371/journal.pone.0004306 19180195
119. Pyza E, Gorska-Andrzejak J. Involvement of glial cells in rhythmic size changes in neurons of the housefly's visual system. J neurobiol. 2004;59(2):205–15. doi: 10.1002/neu.10307 15085538
120. Benna C, Bonaccorsi S, Wulbeck C, Helfrich-Forster C, Gatti M, Kyriacou CP, et al. Drosophila timeless2 is required for chromosome stability and circadian photoreception. Current biology: CB. 2010;20(4):346–52. doi: 10.1016/j.cub.2009.12.048 20153199
121. Coates KE, Majot AT, Zhang X, Michael CT, Spitzer SL, Gaudry Q, et al. Identified Serotonergic Modulatory Neurons Have Heterogeneous Synaptic Connectivity within the Olfactory System of Drosophila. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2017;37(31):7318–31.
122. Gaspar P, Lillesaar C. Probing the diversity of serotonin neurons. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 2012;367(1601):2382–94. doi: 10.1098/rstb.2011.0378 22826339
123. Herve D, Pickel VM, Joh TH, Beaudet A. Serotonin axon terminals in the ventral tegmental area of the rat: fine structure and synaptic input to dopaminergic neurons. Brain res. 1987;435(1–2):71–83. doi: 10.1016/0006-8993(87)91588-5 2892580
124. Moukhles H, Bosler O, Bolam JP, Vallee A, Umbriaco D, Geffard M, et al. Quantitative and morphometric data indicate precise cellular interactions between serotonin terminals and postsynaptic targets in rat substantia nigra. Neuroscience. 1997;76(4):1159–71. doi: 10.1016/s0306-4522(96)00452-6 9027876
125. Nässel DR, Elekes K. Ultrastructural demonstration of serotonin-immunoreactivity in the nervous system of an insect (Calliphora erythrocephala). Neurosci lett. 1984;48(2):203–10. doi: 10.1016/0304-3940(84)90020-x 6384830
126. Zheng Z, Lauritzen JS, Perlman E, Robinson CG, Nichols M, Milkie D, et al. A Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster. Cell. 2018;174(3):730–43 e22. doi: 10.1016/j.cell.2018.06.019 30033368
127. Eckstein N, Bates AS, Du M, Hartenstein V, Jefferis GSXE, Funke J. Neurotransmitter Classification from Electron Microscopy Images at Synaptic Sites in Drosophila. BioRxiv. 2020:2020.06.12.148775.
128. Altieri SC, Garcia-Garcia AL, Leonardo ED, Andrews AM. Rethinking 5-HT1A receptors: emerging modes of inhibitory feedback of relevance to emotion-related behavior. ACS chem neurosci. 2013;4(1):72–83. doi: 10.1021/cn3002174 23336046
129. Andrade R, Huereca D, Lyons JG, Andrade EM, McGregor KM. 5-HT1A Receptor-Mediated Autoinhibition and the Control of Serotonergic Cell Firing. ACS chem neurosci. 2015;6(7):1110–5. doi: 10.1021/acschemneuro.5b00034 25913021
130. Courtney NA, Ford CP. Mechanisms of 5-HT1A receptor-mediated transmission in dorsal raphe serotonin neurons. J physiol. 2016;594(4):953–65. doi: 10.1113/JP271716 26634643
131. Freifeld L, Clark DA, Schnitzer MJ, Horowitz MA, Clandinin TR. GABAergic lateral interactions tune the early stages of visual processing in Drosophila. Neuron. 2013;78(6):1075–89. doi: 10.1016/j.neuron.2013.04.024 23791198
132. Keles MF, Hardcastle BJ, Stadele C, Xiao Q, Frye MA. Inhibitory Interactions and Columnar Inputs to an Object Motion Detector in Drosophila. Cell rep. 2020;30(7):2115–24 e5. doi: 10.1016/j.celrep.2020.01.061 32075756
133. Halberstadt AL. Recent advances in the neuropsychopharmacology of serotonergic hallucinogens. Behav Brain Res. 2015;277:99–120. doi: 10.1016/j.bbr.2014.07.016 25036425
134. Li YH, Xiang K, Xu X, Zhao X, Li Y, Zheng L, et al. Co-activation of both 5-HT1A and 5-HT7 receptors induced attenuation of glutamatergic synaptic transmission in the rat visual cortex. Neurosci lett. 2018;686:122–6. doi: 10.1016/j.neulet.2018.09.013 30205142
135. Sizemore TR, Dacks AM. Serotonergic Modulation Differentially Targets Distinct Network Elements within the Antennal Lobe of Drosophila melanogaster. Scientific reports. 2016;6:37119. doi: 10.1038/srep37119 27845422
136. Gordon MD, Scott K. Motor control in a Drosophila taste circuit. Neuron. 2009;61(3):373–84. doi: 10.1016/j.neuron.2008.12.033 19217375
137. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nature methods. 2012;9(7):676–82. doi: 10.1038/nmeth.2019 22743772
138. Tan L, Zhang KX, Pecot MY, Nagarkar-Jaiswal S, Lee PT, Takemura SY, et al. Ig Superfamily Ligand and Receptor Pairs Expressed in Synaptic Partners in Drosophila. Cell. 2015;163(7):1756–69. doi: 10.1016/j.cell.2015.11.021 26687360
139. Hu Y, Sopko R, Foos M, Kelley C, Flockhart I, Ammeux N, et al. FlyPrimerBank: an online database for Drosophila melanogaster gene expression analysis and knockdown evaluation of RNAi reagents. G3 (Bethesda). 2013;3(9):1607–16.
140. Picelli S, Bjorklund AK, Faridani OR, Sagasser S, Winberg G, Sandberg R. Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nature methods. 2013;10(11):1096–8. doi: 10.1038/nmeth.2639 24056875
141. Picelli S, Faridani OR, Bjorklund AK, Winberg G, Sagasser S, Sandberg R. Full-length RNA-seq from single cells using Smart-seq2. Nature protocols. 2014;9(1):171–81. doi: 10.1038/nprot.2014.006 24385147
142. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. doi: 10.1093/bioinformatics/bts635 23104886
143. Keles MF, Frye MA. Object-Detecting Neurons in Drosophila. Current biology: CB. 2017;27(5):680–7. doi: 10.1016/j.cub.2017.01.012 28190726
144. Stadele C, Keles MF, Mongeau JM, Frye MA. Non-canonical Receptive Field Properties and Neuromodulation of Feature-Detecting Neurons in Flies. Current biology: CB. 2020.
145. Weir PT, Dickinson MH. Functional divisions for visual processing in the central brain of flying Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(40):E5523–32. doi: 10.1073/pnas.1514415112 26324910
146. Wilson RI, Turner GC, Laurent G. Transformation of olfactory representations in the Drosophila antennal lobe. Science. 2004;303(5656):366–70. doi: 10.1126/science.1090782 14684826
147. Akin O, Zipursky SL. Frazzled promotes growth cone attachment at the source of a Netrin gradient in the Drosophila visual system. Elife. 2016;5.
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 8
- Proč se v Česku šíří několik „vymýcených“ infekcí najednou? Ptáme se odborníků
- ADHD jako evoluční výhoda? Výzkum se zaměřil na lovce a sběrače
- Není migréna jako migréna: Co pociťují ženy a co muži?
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Není statin jako statin aneb praktický přehled rozdílů jednotlivých molekul
Nejčtenější v tomto čísle
- Genomic imprinting: An epigenetic regulatory system
- Uptake of exogenous serine is important to maintain sphingolipid homeostasis in Saccharomyces cerevisiae
- A human-specific VNTR in the TRIB3 promoter causes gene expression variation between individuals
- Immediate activation of chemosensory neuron gene expression by bacterial metabolites is selectively induced by distinct cyclic GMP-dependent pathways in Caenorhabditis elegans