Neurotrapping: Cellular screens to identify the neural substrates of behavior in Drosophila

Frontiers in Molecular Neuroscience

Volumn 2, Issue NOV, 2011, Pages

  White, Benjamin H ^a   Peabody, Nathan C ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Circuits; Excitability; Genetic; Neural networks; Synaptic

Indexed keywords

INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; RHODOPSIN;

BEHAVIOR; CELL SCREENING; DROSOPHILA; GENE EXPRESSION; GENE TARGETING; MUTAGENESIS; NERVE CELL; NERVE CELL EXCITABILITY; NEUROTRAPPING; NONHUMAN; REVIEW; STIMULATION; SYNAPTIC TRANSMISSION; TRANSGENE;

EID: 77957974177     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.02.020.2009     Document Type: Review

References (63)

1. Adamantidis, A. R., Zhang, F., Aravanis, A. M., Deisseroth, K., and De Lecea, L. (2007). Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450, 420-429.
2. Baines, R. A., Uhler, J. P., Thompson, A., Sweeney, S. T., and Bate, M. (2001). Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523-1531.
3. Brand, A. H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
4. Broughton, S. J., Kitamoto, T., and Greenspan, R. J. (2004). Excitatory and inhibitory switches for courtship in the brain of Drosophila melanogaster. Curr. Biol. 14, R290-R547.
5. Deisseroth, K., Feng, G., Majewska, A. K., Miesenbock, G., Ting, A., and Schnitzer, M. J. (2006). Nextgeneration optical technologies for illuminating genetically targeted brain circuits. J. Neurosci. 26, 10380-10386.
6. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K., and Dickson, B. J. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
7. Ferveur, J. F., Stortkuhl, K. F., Stocker, R. F., and Greenspan, R. J. (1995). Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267, 902-905.
8. Gao, S., Takemura, S. Y., Ting, C. Y., Huang, S., Lu, Z., Luan, H., Rister, J., Thum, A. S., Yang, M., Hong, S. T., Wang, J. W., Odenwald, W. F., White, B. H., Meinertzhagen, I. A., and Lee, C. H. (2008). The neural substrate of spectral preference in Drosophila. Neuron 60, 328-342.
9. Gordon, M. D., and Scott, K. (2009). Motor control in a Drosophila taste circuit. Neuron 61, 373-384.
10. Hamada, F. N., Rosenzweig, M., Kang, K., Pulver, S. R., Ghezzi, A., Jegla, T. J., and Garrity, P. A. (2008). An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, U217-U255.
11. Han, X., Qian, X., Stern, P., Chuong, A., and Boyden, E. S. (2009). Informational lesions: optical perturbation of spike timing and neural synchrony via microbial opsin gene fusions. Front. Mol. Neurosci. 2. doi: 10.3389/neuro.02.012.2009.
12. Hodge, J. (2009). Ion channels to inactivate neurons in Drosophila. Front. Mol. Neurosci. 2. doi: 10.3389/neuro.02.013.2009.
13. Hodge, J. J., Choi, J. C., O'Kane C. J., and Griffith, L. C. (2005). Shaw potassium channel genes in Drosophila. J. Neurobiol. 63, 235-254.
14. Holford, M., Auer, S., Laqua, M., and Ibañez-Tallon, I. (2009). Manipulating neuronal circuits with endogenous and recombinant cell-surface tethered modulators. Front. Mol. Neurosci. 2. doi: 10.3389/neuro.02.021.2009.
15. Holmes, T. C., Sheeba, V., Mizrak, D., Rubovszky, B., and Dahdal, D. (2007). Circuit-breaking and behavioral analysis by molecular genetic manipulation of neural activity in Drosophila. In Invertebrate Neurobiology, G. North, and R. J. Greenspan, eds (Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press), pp. 19-52.
16. Horn, C., and Handler, A. M. (2005). Site-specific genomic targeting in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 102, 12483-12488.
17. Hughes, C. L., and Thomas, J. B. (2007). A sensory feedback circuit coordinates muscle activity in Drosophila. Mol. Cell. Neurosci. 35, 383-396.
18. Joiner, W. J., Crocker, A., White, B. H., and Sehgal, A. (2006). Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441, 757-760.
19. Kasuya, J., Ishimoto, H., and Kitamoto, T. (2009). Neuronal mechanisms of learning and memory revealed by spatial and temporal suppression of neurotransmission using shibirets1, a temperature-sensitive dynamin mutant gene in Drosophila melanogaster. Front. Mol. Neurosci. 2. doi: 10.3389/neuro.02.011.2009.
20. Katsov, A. Y., and Clandinin, T. R. (2008). Motion processing streams in Drosophila are behaviorally specialized. Neuron 59, 322-335.
21. Keller, A., Sweeney, S. T., Zars, T., O'Kane, C. J., and Heisenberg, M. (2002). Targeted expression of tetanus neurotoxin interferes with behavioral responses to sensory input in Drosophila. J. Neurobiol. 50, 221-233.
22. Kim, J. C., Cook, M. N., Carey, M. R., Shen, C., Regehr, W. G., and Dymecki, S. M. (2009). Linking genetically defined neurons to behavior through a broadly applicable silencing allele. Neuron 63, 305-315.
23. Kitamoto, T. (2001). Conditional modification of behavior in drosophila by targeted expression of a temperaturesensitive shibire allele in defined neurons. J. Neurobiol. 47, 81-92.
24. Kitamoto, T. (2002a). Conditional disruption of synaptic transmission induces male-male courtship behavior in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 99, 13232-13237.
25. Kitamoto, T. (2002b). Targeted expression of temperature-sensitive dynamin to study neural mechanisms of complex behavior in Drosophila. J. Neurogenet. 16, 205-228.
26. Lee, T. M., and Luo, L. Q. (2001). Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254.
27. Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., Chen, L., Chen, L., Chen, T. M., Chin, M. C., Chong, J., Crook, B. E., Czaplinska, A., Dang, C. N., Datta, S., Dee, N. R., Desaki, A. L., Desta, T., Diep, E., Dolbeare, T. A., Donelan, M. J., Dong, H. W., Dougherty, J. G., Duncan, B. J., Ebbert, A. J., Eichele, G., Estin, L. K., Faber, C., Facer, B. A., Fields, R., Fischer, S. R., Fliss, T. P., Frensley, C., Gates, S. N., Glattfelder, K. J., Halverson, K. R., Hart, M. R., Hohmann, J. G., Howell, M. P., Jeung, D. P., Johnson, R. A., Karr, P. T., Kawal, R., Kidney, J. M., Knapik, R. H., Kuan, C. L., Lake, J. H., Laramee, A. R., Larsen, K. D., Lau, C., Lemon, T. A., Liang, A. J., Liu, Y., Luong, L. T., Michaels, J., Morgan, J. J., Morgan, R. J., Mortrud, M. T., Mosqueda, N. F., Ng, L. L., Ng, R., Orta, G. J., Overly, C. C., Pak, T. H., Parry, S. E., Pathak, S. D., Pearson, O. C., Puchalski, R. B., Riley, Z. L., Rockett, H. R., Rowland, S. A., Royall, J. J., Ruiz, M. J., Sarno, N. R., Schaffnit, K., Shapovalova, N. V., Sivisay, T., Slaughterbeck, C. R., Smith, S. C., Smith, K. A., Smith, B. I., Sodt, A. J., Stewart, N. N., Stumpf, K. R., Sunkin, S. M., Sutram, M., Tam, A., Teemer, C. D., Thaller, C., Thompson, C. L., Varnam, L. R., Visel, A., Whitlock, R. M., Wohnoutka, P. E., Wolkey, C. K., Wong, V. Y., Wood, M., Yaylaoglu, M. B., Young, R. C., Youngstrom, B. L., Yuan, X. F., Zhang, B., Zwingman, T. A., and Jones, A. R. (2007). Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176.
28. Lima, S. Q., and Miesenbock, G. (2005). Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141-152.
29. Luan, H., Lemon, W. C., Peabody, N. C., Pohl, J. B., Zelensky, P. K., Wang, D., Nitabach, M. N., Holmes, T. C., and White, B. H. (2006a). Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila. J. Neurosci. 26, 573-584.
30. Luan, H., Peabody, N. C., Vinson, C. R., and White, B. H. (2006b). Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52, 425-436.
31. Luan, H., and White, B. H. (2007). Combinatorial methods for refined neuronal gene targeting. Curr. Opin. Neurobiol. 17, 572-580.
32. Luo, L., Callaway, E. M., and Svoboda, K. (2008). Genetic dissection of neural circuits. Neuron 57, 634-660.
33. Martin, J. R., Keller, A., and Sweeney, S. T. (2002). Targeted expression of tetanus toxin: a new tool to study the neurobiology of behavior. Adv. Genet. 47, 1-47.
34. McGuire, S. E., Roman, G., and Davis, R. L. (2004). Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet. 20, 384-391.
35. Mochida, S., Poulain, B., Eisel, U., Binz, T., Kurazono, H., Niemann, H., and Tauc, L. (1990). Exogenous mRNA encoding tetanus or botulinum neurotoxins expressed in Aplysia neurons. Proc. Natl. Acad. Sci. U.S.A. 87, 7844-7848.
36. Ng, L., Bernard, A., Lau, C., Overly, C. C., Dong, H. W., Kuan, C., Pathak, S., Sunkin, S. M., Dang, C., Bohland, J. W., Bokil, H., Mitra, P. P., Puelles, L., Hohmann, J., Anderson, D. J., Lein, E. S., Jones, A. R., and Hawrylycz, M. (2009). An anatomic gene expression atlas of the adult mouse brain. Nat. Neurosci. 12, 356-362.
37. Nitabach, M. N., Blau, J., and Holmes, T. C. (2002). Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109, 485-495.
38. Nitabach, M. N., Wu, Y., Sheeba, V., Lemon, W. C., Strumbos, J., Zelensky, P. K., White, B. H., and Holmes, T. C. (2006). Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J. Neurosci. 26, 479-489.
39. Osterwalder, T., Yoon, K. S., White, B. H., and Keshishian, H. (2001). A conditional tissue-specific transgene expression system using inducible GAL4. Proc. Natl. Acad. Sci. U.S.A. 98, 12596-12601.
40. Parisky, K. M., Agosto, J., Pulver, S. R., Shang, Y., Kuklin, E., Hodge, J. J., Kang, K., Liu, X., Garrity, P. A., Rosbash, M., and Griffith, L. C. (2008). PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60, 672-682.
41. Peabody, N. C., Pohl, J. B., Diao, F., Vreede, A. P., Sandstrom, D. J., Wang, H., Zelensky, P. K., and White, B. H. (2009). Characterization of the decision network for wing expansion in Drosophila using targeted expression of the TRPM8 channel. J. Neurosci. 29, 3343-3353.
42. Pfeiffer, B. D., Jenett, A., Hammonds, A. S., Ngo, T. T. B., Misra, S., Murphy, C., Scully, A., Carlson, J. W., Wan, K. H., Laverty, T. R., Mungall, C., Svirskas, R., Kadonaga, J. T., Doe, C. Q., Eisen, M. B., Celniker, S. E., and Rubin, G. M. (2008). Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 105, 9715-9720.
43. Pitman, J. L., McGill, J. J., Keegan, K. P., and Allada, R. (2006). A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441, 753-756.
44. Rodan, A. R., Kiger, J. A., Jr., and Heberlein, U. (2002). Functional dissection of neuroanatomical loci regulating ethanol sensitivity in Drosophila. J. Neurosci. 22, 9490-9501.
45. Roman, G., Endo, K., Zong, L., and Davis, R. L. (2001). P[Switch], a system for spatial and temporal control of gene expression in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 98, 12602-12607.
46. Schroll, C., Riemensperger, T., Bucher, D., Ehmer, J., Voller, T., Erbguth, K., Gerber, B., Hendel, T., Nagel, G., Buchner, E., and Fiala, A. (2006). Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16, 1741-1747.
47. Sepp, K. J., and Auld, V. J. (1999). Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151, 1093-1101.
48. Simpson, J. H. (2009). Mapping and manipulating neural circuits in the fly brain. Adv. Genet. 65, 79-143.
49. Sohal, V. S., Zhang, F., Yizhar, O., and Deisseroth, K. (2009). Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698-702.
50. Song, W., Onishi, M., Jan, L. Y., and Jan, Y. N. (2007). Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae. Proc. Natl. Acad. Sci. U.S.A. 104, 5199-5204.
51. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L., and Dickson, B. J. (2005). Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807.
52. Suh, G. S. B., Wong, A. M., Hergarden, A. C., Wang, J. W., Simon, A. F., Benzer, S., Axel, R., and Anderson, D. J. (2004). A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854-859.
53. Suster, M. L., Martin, J. R., Sung, C., and Robinow, S. (2003). Targeted expression of tetanus toxin reveals sets of neurons involved in larval locomotion in Drosophila. J. Neurobiol. 55, 233-246.
54. Sweeney, S. T., Broadie, K., Keane, J., Niemann, H., and Okane, C. J. (1995). Targeted expression of tetanus toxin light-chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341-351.
55. Tan, W., Janczewski, W. A., Yang, P., Shao, X. M., Callaway, E. M., and Feldman, J. L. (2008). Silencing preBotzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nat. Neurosci. 11, 538-540.
56. Thum, A. S., Knapek, S., Rister, J., Dierichs-Schmitt, E., Heisenberg, M., and Tanimoto, H. (2006). Differential potencies of effector genes in adult Drosophila. J. Comp. Neurol. 498, 194-203.
57. Tsai, H. C., Zhang, F., Adamantidis, A., Stuber, G. D., Bonci, A., de Lecea, L., and Deisseroth, K. (2009). Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084.
58. White, B., Osterwalder, T., and Keshishian, H. (2001a). Molecular genetic approaches to the targeted suppression of neuronal activity. Curr. Biol. 11, R1041-R1053.
59. White, B. H., Osterwalder, T. P., Yoon, K. S., Joiner, W. J., Whim, M. D., Kaczmarek, L. K., and Keshishian, H. (2001b). Targeted attenuation of electrical activity in Drosophila using a genetically modified Kmmchannel. Neuron 31, 699-711.
60. Wu, Y., Cao, G., Pavlicek, B., Luo, X., and Nitabach, M. N. (2008). Phase coupling of a circadian neuropeptide with rest/activity rhythms detected using a membrane-tethered spider toxin. PLoS Biol. 6, e273. doi: 10.1371/journal. pbio.0060273.
61. Wyart, C., Bene, F. D., Warp, E., Scott, E. K., Trauner, D., Baier, H., and Isacoff, E. Y. (2009). Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 461, 407-410.
62. Yu, C. R., Power, J., Barnea, G., O'Donnell, S., Brown, H. E., Osborne, J., Axel, R., and Gogos, J. A. (2004). Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42, 553-566.
63. Zhu, Y., Nern, A., Zipursky, S. L., and Frye, M. A. (2009). Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly. Curr. Biol. 19, 613-619.