A pair of ascending neurons in the subesophageal zone mediates aversive sensory inputs-evoked backward locomotion in Drosophila larvae

English version

Autoři: Natsuko Omamiuda-Ishikawa ^aff001; Moeka Sakai ^aff001; Kazuo Emoto ^aff001
Působiště autorů: Department of Biological Sciences, Graduate School of Science, The University of Tokyo ^aff001; International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo ^aff002
Vyšlo v časopise: A pair of ascending neurons in the subesophageal zone mediates aversive sensory inputs-evoked backward locomotion in Drosophila larvae. PLoS Genet 16(11): e1009120. doi:10.1371/journal.pgen.1009120
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009120

Souhrn

Animals typically avoid unwanted situations with stereotyped escape behavior. For instance, Drosophila larvae often escape from aversive stimuli to the head, such as mechanical stimuli and blue light irradiation, by backward locomotion. Responses to these aversive stimuli are mediated by a variety of sensory neurons including mechanosensory class III da (C3da) sensory neurons and blue-light responsive class IV da (C4da) sensory neurons and Bolwig’s organ (BO). How these distinct sensory pathways evoke backward locomotion at the circuit level is still incompletely understood. Here we show that a pair of cholinergic neurons in the subesophageal zone, designated AMBs, evoke robust backward locomotion upon optogenetic activation. Anatomical and functional analysis shows that AMBs act upstream of MDNs, the command-like neurons for backward locomotion. Further functional analysis indicates that AMBs preferentially convey aversive blue light information from C4da neurons to MDNs to elicit backward locomotion, whereas aversive information from BO converges on MDNs through AMB-independent pathways. We also found that, unlike in adult flies, MDNs are dispensable for the dead end-evoked backward locomotion in larvae. Our findings thus reveal the neural circuits by which two distinct blue light-sensing pathways converge on the command-like neurons to evoke robust backward locomotion, and suggest that distinct but partially redundant neural circuits including the command-like neurons might be utilized to drive backward locomotion in response to different sensory stimuli as well as in adults and larvae.

Klíčová slova:

Optogenetics – Behavior – Biological locomotion – Larvae – Neural pathways – Neurons – Sensory neurons – Sensory perception

Zdroje

1. Kristan WB, Calabrese RL, Friesen WO. Neuronal control of leech behavior. Prog Neurobiol. 2005;76: 279–327. doi: 10.1016/j.pneurobio.2005.09.004 16260077

2. Edwards DH, Heitler WJ, Krasne FB. Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci. 1999;22: 153–161. doi: 10.1016/s0166-2236(98)01340-x 10203852

3. Korn H, Faber DS. The Mauthner cell half a century later: A neurobiological model for decision-making? Neuron. 2005;47: 13–28. doi: 10.1016/j.neuron.2005.05.019 15996545

4. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci. 1985;5: 956–964. 3981252 doi: 10.1523/JNEUROSCI.05-04-00956.1985 3981252

5. Deliagina TG, Musienko PE, Zelenin P V. Nervous mechanisms of locomotion in different directions. Curr Opin Physiol. 2019;8: 7–13. doi: 10.1016/j.cophys.2018.11.010 31468024

6. Bidaye SS, Machacek C, Wu Y, Dickson BJ. Neuronal Control of Drosophila Walking Direction. Science (80-). 2014;344: 97–101. doi: 10.1126/science.1249964 24700860

7. Carreira-Rosario A, Zarin AA, Clark MQ, Manning L, Fetter RD, Cardona A, et al. MDN brain descending neurons coordinately activate backward and inhibit forward locomotion. Elife. 2018;7: e38554. doi: 10.7554/eLife.38554 30070205

8. Sen R, Wu M, Branson K, Robie A, Rubin GM, Dickson BJ. Moonwalker Descending Neurons Mediate Visually Evoked Retreat in Drosophila. Curr Biol. 2017;27: 766–771. doi: 10.1016/j.cub.2017.02.008 28238656

9. Sen R, Wang K, Dickson BJ. TwoLumps Ascending Neurons Mediate Touch-Evoked Reversal of Walking Direction in Drosophila. Curr Biol. 2019;29: 4337–4344.e5. doi: 10.1016/j.cub.2019.11.004 31813606

10. Sawin-McCormack EP, Sokolowski MB, Campos AR. Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. J Neurogenet. 1995;10: 119–135. Available: http://www.ncbi.nlm.nih.gov/pubmed/8592272 doi: 10.3109/01677069509083459 8592272

11. Mazzoni EO, Desplan C, Blau J. Circadian Pacemaker Neurons Transmit and Modulate Visual Information to Control a Rapid Behavioral Response. Neuron. 2005;45: 293–300. doi: 10.1016/j.neuron.2004.12.038 15664180

12. Shibuya K, Onodera S, Hori M. Toxic wavelength of blue light changes as insects grow. Singh A, editor. PLoS One. 2018;13: e0199266. doi: 10.1371/journal.pone.0199266 29920536

13. Takagi S, Cocanougher BT, Niki S, Miyamoto D, Kohsaka H, Kazama H, et al. Divergent Connectivity of Homologous Command-like Neurons Mediates Segment-Specific Touch Responses in Drosophila. Neuron. 2017;96: 1373–1387.e6. doi: 10.1016/j.neuron.2017.10.030 29198754

14. Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN. Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature. 2010;468: 921–926. doi: 10.1038/nature09576 21068723

15. Steller H, Fischbach K-F, Rubin GM. disconnected: A Locus Required for Neuronal Pathway Formation in the Visual System of Drosophila. Cell. 1987;50: 1139–1153. doi: 10.1016/0092-8674(87)90180-2 3113740

16. Sprecher SG, Pichaud F, Desplan C. Adult and larval photoreceptors use different mechanisms to specify the same Rhodopsin fates. Genes Dev. 2007;21: 2182–2195. doi: 10.1101/gad.1565407 17785526

17. Salcedo E, Huber A, Henrich S, Chadwell L V, Chou WH, Paulsen R, et al. Blue- and green-absorbing visual pigments of Drosophila: ectopic expression and physiological characterization of the R8 photoreceptor cell-specific Rh5 and Rh6 rhodopsins. J Neurosci. 1999;19: 10716–10726. doi: 10.1523/JNEUROSCI.19-24-10716.1999 10594055

18. Hwang RY, Zhong L, Xu Y, Johnson T, Zhang F, Deisseroth K, et al. Nociceptive Neurons Protect Drosophila Larvae from Parasitoid Wasps. Curr Biol. 2007;17: 2105–2116. doi: 10.1016/j.cub.2007.11.029 18060782

19. Grueber WB, Jan LY, Jan YN. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development. 2002;129: 2867–2878. 12050135

20. Emoto K, He Y, Ye B, Grueber WB, Adler PN, Jan LY, et al. Control of Dendritic Branching and Tiling by the Tricornered-Kinase/Furry Signaling Pathway in Drosophila Sensory Neurons. Cell. 2004;119: 245–256. doi: 10.1016/j.cell.2004.09.036 15479641

21. Emoto K. Signaling mechanisms that coordinate the development and maintenance of dendritic fields. Curr Opin Neurobiol. 2012;22: 805–811. doi: 10.1016/j.conb.2012.04.005 22575709

22. Yoshino J, Morikawa RK, Hasegawa E, Emoto K. Neural Circuitry that Evokes Escape Behavior upon Activation of Nociceptive Sensory Neurons in Drosophila Larvae. Curr Biol. 2017;27: 2499–2504.e3. doi: 10.1016/j.cub.2017.06.068 28803873

23. Ohyama T, Schneider-Mizell CM, Fetter RD, Aleman JV, Franconville R, Rivera-Alba M, et al. A multilevel multimodal circuit enhances action selection in Drosophila. Nature. 2015;520: 633–639. doi: 10.1038/nature14297 25896325

24. Morikawa RK, Kanamori T, Yasunaga K, Emoto K. Different levels of the Tripartite motif protein, Anomalies in sensory axon patterning (Asap), regulate distinct axonal projections of Drosophila sensory neurons. Proc Natl Acad Sci U S A. 2011;108: 19389–19394. doi: 10.1073/pnas.1109843108 22084112

25. Burgos A, Honjo K, Ohyama T, Qian CS, Shin GJ, Gohl DM, et al. Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila. Elife. 2018;7: e26016. doi: 10.7554/eLife.26016 29528286

26. Hu C, Petersen M, Hoyer N, Spitzweck B, Tenedini F, Wang D, et al. Sensory integration and neuromodulatory feedback facilitate Drosophila mechanonociceptive behavior. Nat Neurosci. 2017;20: 1085–1095. doi: 10.1038/nn.4580 28604684

27. Jenett A, Rubin GM, Ngo TTB, Shepherd D, Murphy C, Dionne H, et al. A GAL4-Driver Line Resource for Drosophila Neurobiology. Cell Rep. 2012;2: 991–1001. doi: 10.1016/j.celrep.2012.09.011 23063364

28. Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A, Cho YK, et al. Independent optical excitation of distinct neural populations. Nat Methods. 2014;11: 338–346. doi: 10.1038/nmeth.2836 24509633

29. Gordon MD, Scott K. Motor Control in a Drosophila Taste Circuit. Neuron. 2009;61: 373–384. doi: 10.1016/j.neuron.2008.12.033 19217375

30. Bohm RA, Welch WP, Goodnight LK, Cox LW, Henry LG, Gunter TC, et al. A genetic mosaic approach for neural circuit mapping in Drosophila. Proc Natl Acad Sci. 2010;107: 16378–16383. doi: 10.1073/pnas.1004669107 20810922

31. Luan H, Peabody NC, Vinson CRR, White BH. Refined Spatial Manipulation of Neuronal Function by Combinatorial Restriction of Transgene Expression. Neuron. 2006;52: 425–436. doi: 10.1016/j.neuron.2006.08.028 17088209

32. Nicolai LJJ, Ramaekers A, Raemaekers T, Drozdzecki A, Mauss AS, Yan J, et al. Genetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila. Proc Natl Acad Sci. 2010;107: 20553–20558. doi: 10.1073/pnas.1010198107 21059961

33. Fouquet W, Owald D, Wichmann C, Mertel S, Depner H, Dyba M, et al. Maturation of active zone assembly by Drosophila Bruchpilot. J Cell Biol. 2009;186: 129–145. doi: 10.1083/jcb.200812150 19596851

34. Feinberg EH, VanHoven MK, Bendesky A, Wang G, Fetter RD, Shen K, et al. GFP Reconstitution Across Synaptic Partners (GRASP) Defines Cell Contacts and Synapses in Living Nervous Systems. Neuron. 2008;57: 353–363. doi: 10.1016/j.neuron.2007.11.030 18255029

35. Shearin HK, Quinn CD, Mackin RD, Macdonald IS, Stowers RS. t-GRASP, a targeted GRASP for assessing neuronal connectivity. J Neurosci Methods. 2018;306: 94–102. doi: 10.1016/j.jneumeth.2018.05.014 29792886

36. Sweeney ST, Broadie K, Keane J, Niemann H, O’Kane CJ. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron. 1995;14: 341–351. doi: 10.1016/0896-6273(95)90290-2 7857643

37. White K, Tahaoglu E, Steller H. Cell killing by the Drosophila gene reaper. Science. 1996;271: 805–807. doi: 10.1126/science.271.5250.805 8628996

38. White K, Grether ME, Abrams JM, Young L, Farrell K, Steller H. Genetic control of programmed cell death in Drosophila. Science. 1994;264: 677–683. doi: 10.1126/science.8171319 8171319

39. Abbott MK, Lengyel JA. Embryonic head involution and rotation of male terminalia require the Drosophila locus head involution defective. Genetics. 1991;129: 783–789. 1752422

40. Yan Z, Zhang W, He Y, Gorczyca D, Xiang Y, Cheng LE, et al. Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature. 2012;493: 221–225. doi: 10.1038/nature11685 23222543

41. Berger-Müller S, Sugie A, Takahashi F, Tavosanis G, Hakeda-Suzuki S, Suzuki T. Assessing the Role of Cell-Surface Molecules in Central Synaptogenesis in the Drosophila Visual System. PLoS One. 2013;8: e83732. doi: 10.1371/journal.pone.0083732 24386266

42. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003;302: 1765–1768. doi: 10.1126/science.1089035 14657498

43. Kanamori T, Kanai MI, Dairyo Y, Yasunaga KI, Morikawa RK, Emoto K. Compartmentalized calcium transients trigger dendrite pruning in Drosophila sensory neurons. Science 2013; 340: 1475–1478. doi: 10.1126/science.1234879 23722427

44. Kanamori T, Yoshino J, Yasunaga KI, Dairyo Y, Emoto K. Local endocytosis triggers dendritic thinning and pruning in Drosophila sensory neurons. Nat Commun. 2015; 6: 6515. doi: 10.1038/ncomms7515 25761586

45. Pfeiffer BD, Ngo T-TB, Hibbard KL, Murphy C, Jenett A, Truman JW, et al. Refinement of tools for targeted gene expression in Drosophila. Genetics. 2010;186: 735–755. doi: 10.1534/genetics.110.119917 20697123

46. Park J, Kondo S, Tanimoto H, Kohsaka H, Nose A. Data-driven analysis of motor activity implicates 5-HT2A neurons in backward locomotion of larval Drosophila. Sci Rep. 2018;8: 10307. doi: 10.1038/s41598-018-28680-8 29985473

47. Kondo S, Ueda R, Phillis RW, Johnson-Schlitz DM, Benz WK. Highly improved gene targeting by germline-specific Cas9 expression in Drosophila. Genetics. 2013;195: 715–721. doi: 10.1534/genetics.113.156737 24002648

48. Röder L, Vola C, Kerridge S. The role of the teashirt gene in trunk segmental identity in Drosophila. Development. 1992;115: 1017–1033. 1360402

49. Fasano L, Röder L, Coré N, Alexandre E, Vola C, Jacq B, et al. The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs. Cell. 1991;64: 63–79. doi: 10.1016/0092-8674(91)90209-h 1846092

50. Mahr A, Aberle H. The expression pattern of the Drosophila vesicular glutamate transporter: A marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr Patterns. 2006;6: 299–309. doi: 10.1016/j.modgep.2005.07.006 16378756

51. Feng Y, Ueda A, Wu C. A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J Neurogenet. 2004;18: 377–402. doi: 10.1080/01677060490894522 15763995

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