High-Throughput Analysis of Stimulus-Evoked Behaviors in Drosophila Larva Reveals Multiple Modality-Specific Escape Strategies

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Ohyama, Tomoko ^a   Jovanic, Tihana ^a   Denisov, Gennady ^a   Dang, Tam C ^a   Hoffmann, Dominik ^a   Kerr, Rex A ^a   Zlatic, Marta ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; TRANSCRIPTION FACTOR GAL4;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL ACTIVATION; COMPUTER PROGRAM; CONTROLLED STUDY; DENDRITE; DROSOPHILA; EMBRYO; ESCAPE BEHAVIOR; EVOKED SOMATOSENSORY RESPONSE; HEAD MOVEMENT; HEAT SENSITIVITY; LARVAL STAGE; LOCOMOTION; NEUROMODULATION; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; OPTOGENETICS; PROCESS DEVELOPMENT; SOMATOSENSORY STIMULATION; VIBRATION SENSE;

AIR; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ESCAPE REACTION; HIGH-THROUGHPUT SCREENING ASSAYS; HOT TEMPERATURE; ION CHANNELS; LARVA; MUTATION; NEURONS; OPTOGENETICS; PHYSICAL STIMULATION; SOFTWARE; VIBRATION;

EID: 84882718493     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071706     Document Type: Article

References (54)

1. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C, et al. (2012) A GAL4-Driver Line Resource for Drosophila Neurobiology. Cell Rep 2: 991-1001.
2. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S, et al. (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci U S A 105: 9715-9720.
3. Boyan GS, Ball EE, (1993) The grasshopper, Drosophila and neuronal homology (advantages of the insect nervous system for the neuroscientist). Prog Neurobiol 41: 657-682.
4. Murphey RK, Possidente D, Pollack G, Merritt DJ, (1989) Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila. J Comp Neurol 290: 185-200.
5. Ladle D, Pechovrieseling E, Arber S, (2007) Assembly of Motor Circuits in the Spinal Cord: Driven to Function by Genetic and Experience-Dependent Mechanisms. Neuron 56: 270-283.
6. Grillner S, Jessell TM, (2009) Measured motion: searching for simplicity in spinal locomotor networks. Current opinion in neurobiology 19: 572-586.
7. Heckscher ES, Lockery SR, Doe CQ, (2012) Characterization of Drosophila larval crawling at the level of organism, segment, and somatic body wall musculature. J Neurosci 32: 12460-12471.
8. Berni J, Pulver SR, Griffith LC, Bate M, (2012) Autonomous circuitry for substrate exploration in freely moving Drosophila larvae. Curr Biol 22: 1861-1870.
9. Tracey WD Jr, Wilson RI, Laurent G, Benzer S, (2003) painless, a Drosophila gene essential for nociception. Cell 113: 261-273.
10. Kernan M, Cowan D, Zuker C, (1994) Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12: 1195-1206.
11. Wu Z, Sweeney LB, Ayoob JC, Chak K, Andreone BJ, et al. (2011) A combinatorial semaphorin code instructs the initial steps of sensory circuit assembly in the Drosophila CNS. Neuron 70: 281-298.
12. Bharadwaj R, Roy M, Ohyama T, Sivan-Loukianova E, Delannoy M, et al. (2013) Cbl-associated protein regulates assembly and function of two tension-sensing structures in Drosophila. Development 140: 627-638.
13. Hwang RY, Zhong L, Xu Y, Johnson T, Zhang F, et al. (2007) Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr Biol 17: 2105-2116.
14. Caldwell JC, Miller MM, Wing S, Soll DR, Eberl DF, (2003) Dynamic analysis of larval locomotion in Drosophila chordotonal organ mutants. Proc Natl Acad Sci U S A 100: 16053-16058.
15. Hughes C, Thomas J, (2007) A sensory feedback circuit coordinates muscle activity in Drosophila. Molecular and Cellular Neuroscience 35: 383-396.
16. Song W, Onishi M, Jan LY, Jan YN, (2007) Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae. Proc Natl Acad Sci USA 104: 5199-5204.
17. Cheng LE, Song W, Looger LL, Jan LY, Jan YN, (2010) The role of the TRP channel NompC in Drosophila larval and adult locomotion. Neuron 67: 373-380.
18. Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, et al. (2010) Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468: 921-926.
19. Kim SE, Coste B, Chadha A, Cook B, Patapoutian A, (2012) The role of Drosophila Piezo in mechanical nociception. Nature 483: 209-212.
20. Zhong L, Hwang RY, Tracey WD, (2010) Pickpocket is a DEG/ENaC protein required for mechanical nociception in Drosophila larvae. Curr Biol 20: 429-434.
21. Walker RG, Willingham AT, Zuker CS, (2000) A Drosophila mechanosensory transduction channel. Science 287: 2229-2234.
22. Zlatic M, Landgraf M, Bate M, (2003) Genetic specification of axonal arbors: atonal regulates robo3 to position terminal branches in the Drosophila nervous system. Neuron 37: 41-51.
23. Pfeiffer BD, Ngo TT, Hibbard KL, Murphy C, Jenett A, et al. (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186: 735-755.
24. Oswald M, Rymarczyk B, Chatters A, Sweeney ST, (2011) A novel thermosensitive escape behavior in Drosophila larvae. Fly (Austin) 5: 304-306.
25. Gershow M, Berck M, Mathew D, Luo L, Kane EA, et al. (2012) Controlling airborne cues to study small animal navigation. Nat Methods 9: 290-296.
26. Gomez-Marin A, Stephens GJ, Louis M, (2011) Active sampling and decision making in Drosophila chemotaxis. Nat Commun 2: 441.
27. Kabra M, Robie AA, Rivera-Alba M, Branson S, Branson K, (2013) JAABA: interactive machine learning for automatic annotation of animal behavior. Nat Methods 10: 64-67.
28. Brand AH, Manoukian AS, Perrimon N, (1994) Ectopic expression in Drosophila. Methods Cell Biol 44: 635-654.
29. Kitamoto T, (2001) Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47: 81-92.
30. Schroll C, Riemensperger T, Bucher D, Ehmer J, Voller T, et al. (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16: 1741-1747.
31. Kwon Y, Shen WL, Shim HS, Montell C, (2010) Fine thermotactic discrimination between the optimal and slightly cooler temperatures via a TRPV channel in chordotonal neurons. J Neurosci 30: 10465-10471.
32. Zipursky SL, Venkatesh TR, Teplow DB, Benzer S, (1984) Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36: 15-26.
33. Babcock M, Macleod GT, Leither J, Pallanck L, (2004) Genetic analysis of soluble N-ethylmaleimide-sensitive factor attachment protein function in Drosophila reveals positive and negative secretory roles. J Neurosci 24: 3964-3973.
34. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682.
35. Swierczek NA, Giles AC, Rankin CH, Kerr RA, (2011) High-throughput behavioral analysis in C. elegans. Nat Methods 8: 592-598.
36. Robie AA, Straw AD, Dickinson MH, (2010) Object preference by walking fruit flies, Drosophila melanogaster, is mediated by vision and graviperception. J Exp Biol 213: 2494-2506.
37. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (2007) The Art of Scientific Computing. New York: Cambridge University Press.
38. Cohen EH, Singh M, Maloney LT (2008) Perceptual segmentation and the perceived orientation of dot clusters: The role of robust statistics. Journal of Vision 8.
39. Berrigan D, Pepin DJ, (1995) How Maggots Move- Allometry and Kinematics of Crawling in Larval Diptera. Journal of Insect Physiology 41: 329-337.
40. Ainsley JA, Pettus JM, Bosenko D, Gerstein CE, Zinkevich N, et al. (2003) Enhanced locomotion caused by loss of the Drosophila DEG/ENaC protein Pickpocket1. Curr Biol 13: 1557-1563.
41. Hughes CL, Thomas JB, (2007) A sensory feedback circuit coordinates muscle activity in Drosophila. Mol Cell Neurosci 35: 383-396.
42. Yorozu S, Wong A, Fischer BJ, Dankert H, Kernan MJ, et al. (2009) Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 458: 201-U204.
43. Yorozu S, Wong A, Fischer BJ, Dankert H, Kernan MJ, et al. (2009) Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 458: 201-205.
44. Mazzoni EO, Desplan C, Blau J, (2005) Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 45: 293-300.
45. Yuan Q, Xiang Y, Yan Z, Han C, Jan LY, et al. (2011) Light-induced structural and functional plasticity in Drosophila larval visual system. Science 333: 1458-1462.
46. Busto M, Iyengar B, Campos AR, (1999) Genetic dissection of behavior: modulation of locomotion by light in the Drosophila melanogaster larva requires genetically distinct visual system functions. J Neurosci 19: 3337-3344.
47. Honjo K, Hwang RY, Tracey WD Jr, (2012) Optogenetic manipulation of neural circuits and behavior in Drosophila larvae. Nat Protoc 7: 1470-1478.
48. Gomez-Marin A, Partoune N, Stephens GJ, Louis M, Brembs B, (2012) Automated tracking of animal posture and movement during exploration and sensory orientation behaviors. PLoS One 7: e41642.
49. Gomez-Marin A, Louis M, (2012) Active sensation during orientation behavior in the Drosophila larva: more sense than luck. Curr Opin Neurobiol 22: 208-215.
50. Luo L, Gershow M, Rosenzweig M, Kang K, Fang-Yen C, et al. (2010) Navigational decision making in Drosophila thermotaxis. J Neurosci 30: 4261-4272.
51. Kwon Y, Shen WL, Shim HS, Montell C, (2010) Fine thermotactic discrimination between the optimal and slightly cooler temperatures via a TRPV channel in chordotonal neurons. J Neurosci 30: 10465-10471.
52. Inada K, Kohsaka H, Takasu E, Matsunaga T, Nose A, (2011) Optical dissection of neural circuits responsible for Drosophila larval locomotion with halorhodopsin. PLoS One 6: e29019.
53. Fushiki A, Kohsaka H, Nose A, (2013) Role of sensory experience in functional development of Drosophila motor circuits. PLoS One 8: e62199.
54. Grueber WB, Jan LY, Jan YN, (2002) Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129: 2867-2878.