Identifying neural substrates of competitive interactions and sequence transitions during mechanosensory responses in Drosophila


Autoři: Jean-Baptiste Masson aff001;  Francois Laurent aff002;  Albert Cardona aff001;  Chloe Barre aff002;  Nicolas Skatchkovsky aff002;  Marta Zlatic aff001;  Tihana Jovanic aff001
Působiště autorů: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, United States of America aff001;  Decision and Bayesian Computation, USR 3756 (C3BI/DBC) & Neuroscience Department, Institut Pasteur & CNRS, Paris, France aff002;  Department of Physiology, Development, and Neuroscience, Cambridge University, Cambridge, United Kingdom aff003;  MRC Laboratory of Molecular Biology, Trumpington, Cambridge, United Kingdom aff004;  Department of Zoology, Cambridge University, Cambridge, United Kingdom aff005;  Université Paris-Saclay, CNRS, Institut des Neurosciences Paris Saclay, Gif-sur-Yvette, France aff006
Vyšlo v časopise: Identifying neural substrates of competitive interactions and sequence transitions during mechanosensory responses in Drosophila. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008589
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008589

Souhrn

Nervous systems have the ability to select appropriate actions and action sequences in response to sensory cues. The circuit mechanisms by which nervous systems achieve choice, stability and transitions between behaviors are still incompletely understood. To identify neurons and brain areas involved in controlling these processes, we combined a large-scale neuronal inactivation screen with automated action detection in response to a mechanosensory cue in Drosophila larva. We analyzed behaviors from 2.9x105 larvae and identified 66 candidate lines for mechanosensory responses out of which 25 for competitive interactions between actions. We further characterize in detail the neurons in these lines and analyzed their connectivity using electron microscopy. We found the neurons in the mechanosensory network are located in different regions of the nervous system consistent with a distributed model of sensorimotor decision-making. These findings provide the basis for understanding how selection and transition between behaviors are controlled by the nervous system.

Klíčová slova:

Decision making – Drosophila melanogaster – Electron microscopy – Larvae – Motor neurons – Nervous system – Neurons – Sensory neurons


Zdroje

1. Cisek P. Cortical mechanisms of action selection: the affordance competition hypothesis. Philosophical Transactions of the Royal Society B: Biological Sciences. 2007;362: 1585–1599. doi: 10.1098/rstb.2007.2054 17428779

2. Reyn von CR, Breads P, Peek MY, Zheng GZ, Williamson WR, Yee AL, et al. A spike-timing mechanism for action selection. Nat Neurosci. 2014;17: 962–970. doi: 10.1038/nn.3741 24908103

3. Cisek P, Kalaska JF. Neural Mechanisms for Interacting with a World Full of Action Choices. Annu Rev Neurosci. 2010;33: 269–298. doi: 10.1146/annurev.neuro.051508.135409 20345247

4. Gold JI, Shadlen MN. The neural basis of decision making. Annu Rev Neurosci. 2007;30: 535–574. doi: 10.1146/annurev.neuro.29.051605.113038 17600525

5. Gaudry Q, Kristan WB. Behavioral choice by presynaptic inhibition of tactile sensory terminals. Nat Neurosci. 2009;12: 1450–1457. doi: 10.1038/nn.2400 19801989

6. Kristan WB. Neuronal Decision-Making Circuits. Current Biology. 2008;18: R928–R932. doi: 10.1016/j.cub.2008.07.081 18957243

7. Lebedev MA, Wise SP. Insights into seeing and grasping: distinguishing the neural correlates of perception and action. Behav Cogn Neurosci Rev. 2002;1: 108–129. doi: 10.1177/1534582302001002002 17715589

8. Livant WP. George A. Miller, Eugene Galanter, and Karl H Pribram, Plans and the structure of behavior. New York: Henry Holt, 1960. Syst Res. 2007;5: 341–342. doi: 10.1002/bs.3830050409

9. Miller GA, Galanter E, Pribram KH. Plans and the Structure of Behavior. Holt R, Winston, editors. New York; 1960.

10. Jovanic T, Schneider-Mizell CM, Shao M, Masson J-B, Denisov G, Fetter RD, et al. Competitive Disinhibition Mediates Behavioral Choice and Sequences in Drosophila. Cell. Elsevier; 2016;167: 858–870.e19. doi: 10.1016/j.cell.2016.09.009 27720450

11. Lasley KS. The problem of serial order in behavior. Jeffress LA, editor. New York: Wiley; 1951 pp. 112–131.

12. Seeds AM, Ravbar P, Chung P, Hampel S, Midgley FM, Mensh BD, et al. A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila. eLife. 2014;3: e02951. doi: 10.7554/eLife.02951 25139955

13. Long MA, Jin DZ, Fee MS. Support for a synaptic chain model of neuronal sequence generation. Nature. 2010;468: 394–399. doi: 10.1038/nature09514 20972420

14. James W. The Principles of Psychology. London: Macmillan; 1890.

15. Adams J, (null). Learning of movement sequences. Psychological Bulletin. 1984;93: 3–28.

16. Manning A. The Sexual Behaviour of Two Sibling Drosophila Species. Behaviour. Brill; 1959;15: 123–145.

17. Manoli DS, Baker BS. Median bundle neurons coordinate behaviours during Drosophila male courtship. Nature. Nature Publishing Group; 2004;430: 564–569. doi: 10.1038/nature02713 15282607

18. McKellar CE, Lillvis JL, Bath DE, Fitzgerald JE, Cannon JG, Simpson JH, et al. Threshold-Based Ordering of Sequential Actions during Drosophila Courtship. Curr Biol. 2019;29: 426–434.e6. doi: 10.1016/j.cub.2018.12.019 30661796

19. Jenett A, Rubin GM, Ngo T-TB, 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

20. Li H-H, Kroll JR, Lennox SM, Ogundeyi O, Jeter J, Depasquale G, et al. A GAL4 driver resource for developmental and behavioral studies on the larval CNS of Drosophila. Cell Rep. 2014;8: 897–908. doi: 10.1016/j.celrep.2014.06.065 25088417

21. 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

22. Schneider-Mizell CM, Gerhard S, Longair M, Kazimiers T, Li F, Zwart MF, et al. Quantitative neuroanatomy for connectomics in Drosophila. eLife. 2016;5: 1133. doi: 10.7554/eLife.12059 26990779

23. Heckscher ES, Lockery SR, Doe CQ. Characterization of Drosophila larval crawling at the level of organism, segment, and somatic body wall musculature. J Neurosci. Society for Neuroscience; 2012;32: 12460–12471. doi: 10.1523/JNEUROSCI.0222-12.2012 22956837

24. Zwart MF, Pulver SR, Truman JW, Fushiki A, Fetter RD, Cardona A, et al. Selective Inhibition Mediates the Sequential Recruitment of Motor Pools. Neuron. 2016;91: 615–628. doi: 10.1016/j.neuron.2016.06.031 27427461

25. Eichler K, Li F, Litwin-Kumar A, Park Y, Andrade I, Schneider-Mizell CM, et al. The complete connectome of a learning and memory centre in an insect brain. Nature. 2017;548: 175–182. doi: 10.1038/nature23455 28796202

26. Kohsaka H, Zwart MF, Fushiki A, Fetter RD, Truman JW, Cardona A, et al. Regulation of forward and backward locomotion through intersegmental feedback circuits in Drosophila larvae. Nat Commun. Nature Publishing Group; 2019;10: 2654–11. doi: 10.1038/s41467-019-10695-y 31201326

27. Fushiki A, Zwart MF, Kohsaka H, Fetter RD, Cardona A, Nose A, et al. A circuit mechanism for the propagation of waves of muscle contraction in Drosophila. eLife. eLife Sciences Publications Limited; 2016;5: e13253. doi: 10.7554/eLife.13253 26880545

28. 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. eLife Sciences Publications Limited; 2018;7: 57. doi: 10.7554/eLife.38554 30070205

29. Zarin AA, Mark B, Cardona A, Litwin-Kumar A, Doe CQ. A Drosophila larval premotor/motor neuron connectome generating two behaviors via distinct spatio-temporal muscle activity. bioRxiv. Cold Spring Harbor Laboratory; 2019;9: 617977. doi: 10.1101/617977

30. Burgos A, Honjo K, Ohyama T, Qian CS, Shin GJ-E, Gohl DM, et al. Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila. eLife. eLife Sciences Publications Limited; 2018;7: 1557. doi: 10.7554/eLife.26016 29528286

31. Ohyama T, Jovanic T, Denisov G, Dang TC, Hoffmann D, Kerr RA, et al. High-Throughput Analysis of Stimulus-Evoked Behaviors in Drosophila Larva Reveals Multiple Modality-Specific Escape Strategies. Brembs B, editor. PLoS ONE. Public Library of Science; 2013;8: e71706. doi: 10.1371/journal.pone.0071706 23977118

32. Bodmer R, Jan Y-N. Morphological differentiation of the embryonic peripheral neurons in Drosophila. Rouxs Arch Dev Biol. Springer-Verlag; 1987;196: 69–77. doi: 10.1007/BF00402027 28305460

33. Grueber WB, Ye B, Yang C-H, Younger S, Borden K, Jan LY, et al. Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development. The Company of Biologists Limited; 2007;134: 55–64. doi: 10.1242/dev.02666 17164414

34. Merritt DJ, Whitington PM. Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, soma position, and proneural gene function. J Neurosci. Society for Neuroscience; 1995;15: 1755–1767.

35. Tsubouchi A, Caldwell JC, Tracey WD. Dendritic filopodia, Ripped Pocket, NOMPC, and NMDARs contribute to the sense of touch in Drosophila larvae. Curr Biol. 2012;22: 2124–2134. doi: 10.1016/j.cub.2012.09.019 23103192

36. 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. 2013;493: 221–225. doi: 10.1038/nature11685 23222543

37. Kernan M, Cowan D, Zuker C. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron. 1994;12: 1195–1206. doi: 10.1016/0896-6273(94)90437-5 8011334

38. Jovanic T, Winding M, Cardona A, Truman JW, Gershow M, Zlatic M. Neural Substrates of Drosophila Larval Anemotaxis. Curr Biol. 2019;29: 554–566.e4. doi: 10.1016/j.cub.2019.01.009 30744969

39. 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

40. Nern A, Pfeiffer BD, Rubin GM. Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proc Natl Acad Sci USA. National Acad Sciences; 2015;112: E2967–76. doi: 10.1073/pnas.1506763112 25964354

41. Gerhard S, Andrade I, Fetter RD, Cardona A, Schneider-Mizell CM. Conserved neural circuit structure across Drosophila larval development revealed by comparative connectomics. eLife. eLife Sciences Publications Limited; 2017;6: 2452. doi: 10.7554/eLife.29089 29058674

42. Rosenbaum DA, Cohen RG, Jax SA, Weiss DJ, van der Wel R. The problem of serial order in behavior: Lashley’s legacy. Human Movement Science. 2007;26: 525–554. doi: 10.1016/j.humov.2007.04.001 17698232

43. Cisek P. Making decisions through a distributed consensus. Current Opinion in Neurobiology. Elsevier Current Trends; 2012;22: 927–936. doi: 10.1016/j.conb.2012.05.007 22683275

44. Briggman KL, Kristan WB. Imaging dedicated and multifunctional neural circuits generating distinct behaviors. The Journal of neuroscience. 2006.

45. Ledberg A, Bressler SL, Ding M, Coppola R, Nakamura R. Large-scale visuomotor integration in the cerebral cortex. Cereb Cortex. 2007;17: 44–62. doi: 10.1093/cercor/bhj123 16452643

46. Pezzulo G, Castelfranchi C. Thinking as the control of imagination: a conceptual framework for goal-directed systems. Psychol Res. 2009;73: 559–577. doi: 10.1007/s00426-009-0237-z 19347359

47. Berck ME, Khandelwal A, Claus L, Hernandez-Nunez L, Si G, Tabone CJ, et al. The wiring diagram of a glomerular olfactory system. 2016 Jan. Report No.: http://dx.doi.org/10.1101/037721. doi: 10.1101/037721

48. Heckscher ES, Zarin AA, Faumont S, Clark MQ, Manning L, Fushiki A, et al. Even-Skipped(+) Interneurons Are Core Components of a Sensorimotor Circuit that Maintains Left-Right Symmetric Muscle Contraction Amplitude. Neuron. 2015;88: 314–329. doi: 10.1016/j.neuron.2015.09.009 26439528

49. Schlegel P, Texada MJ, Miroschnikow A, Schoofs A, Hückesfeld S, Peters M, et al. Synaptic transmission parallels neuromodulation in a central food-intake circuit. eLife. eLife Sciences Publications Limited; 2016;5: 462. doi: 10.7554/eLife.16799 27845623

50. Pfeiffer BD, Jenett A, Hammonds AS, Ngo T-TB, Misra S, Murphy C, et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci USA. National Acad Sciences; 2008;105: 9715–9720. doi: 10.1073/pnas.0803697105 18621688

51. Zhang W, Yan Z, Jan LY, Jan Y-N. Sound response mediated by the TRP channels NOMPC, NANCHUNG, and INACTIVE in chordotonal organs of Drosophila larvae. Proc Natl Acad Sci USA. National Acad Sciences; 2013;110: 13612–13617. doi: 10.1073/pnas.1312477110 23898199

52. Kwon Y, Shen WL, Shim H-S, Montell C. Fine thermotactic discrimination between the optimal and slightly cooler temperatures via a TRPV channel in chordotonal neurons. J Neurosci. Society for Neuroscience; 2010;30: 10465–10471. doi: 10.1523/JNEUROSCI.1631-10.2010 20685989

53. 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

54. Saalfeld S, Cardona A, Hartenstein V, Tomancak P. CATMAID: collaborative annotation toolkit for massive amounts of image data. Bioinformatics. Oxford University Press; 2009;25: 1984–1986. doi: 10.1093/bioinformatics/btp266 19376822

55. Swierczek NA, Giles AC, Rankin CH, Kerr RA. High-throughput behavioral analysis in C. elegans. Nat Methods. 2011;8: 592–598. doi: 10.1038/nmeth.1625 21642964

56. Kabra M, Robie AA, Rivera-Alba M, Branson S, Branson K. JAABA: interactive machine learning for automatic annotation of animal behavior. Nat Methods. 2012;10: 64–67. doi: 10.1038/nmeth.2281 23202433

57. Bishop C. Pattern recognition and machine learning. Springer; 2006.

58. Schulze A, Gomez-Marin A, Rajendran VG, Lott G, Musy M, Ahammad P, et al. Dynamical feature extraction at the sensory periphery guides chemotaxis. eLife. eLife Sciences Publications Limited; 2015;4: 1129. doi: 10.7554/eLife.06694 26077825

59. Vogelstein JT, Park Y, Ohyama T, Kerr RA, Truman JW, Priebe CE, et al. Discovery of brainwide neural-behavioral maps via multiscale unsupervised structure learning. Science. 2014;344: 386–392. doi: 10.1126/science.1250298 24674869

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 2

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×