A multilevel multimodal circuit enhances action selection in Drosophila

Nature

Volumn 520, Issue 7549, 2015, Pages 633-639

  Ohyama, Tomoko ^a   Schneider Mizell, Casey M ^a   Fetter, Richard D ^a   Aleman, Javier Valdes ^a   Franconville, Romain ^a   Rivera Alba, Marta ^a   Mensh, Brett D ^a   Branson, Kristin M ^a   Simpson, Julie H ^a   Truman, James W ^a   Cardona, Albert ^a   Zlatic, Marta ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAGRAM; ENVIRONMENTAL CUE; ESCAPE BEHAVIOR; FLY; LARVA; LOCOMOTION; NEUROLOGY; SENSORY SYSTEM;

ARTICLE; DROSOPHILA; ELECTRON MICROSCOPY; INTERNEURON; LOCOMOTION; MOTOR NERVE; NERVE CELL NETWORK; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ASSOCIATION; CENTRAL NERVOUS SYSTEM; CYTOLOGY; DROSOPHILA MELANOGASTER; FEMALE; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MOTONEURON; NERVE TRACT; PHYSIOLOGY; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SYNAPSE;

HEXAPODA;

ANIMALS; CENTRAL NERVOUS SYSTEM; CUES; DROSOPHILA MELANOGASTER; FEMALE; INTERNEURONS; LARVA; LOCOMOTION; MOTOR NEURONS; NEURAL PATHWAYS; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84928798062     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14297     Document Type: Article

References (78)

1. Stein, E. B. & Meredith, M. A. The Merging of the Senses (MIT press, 1993).
2. Fetsch, C. R., DeAngelis, G. C.& Angelaki, D. E. Bridging the gap between theories of sensory cue integration and the physiology of multisensory neurons. Nature Rev. Neurosci. 14, 429-442 (2013).
3. van Atteveldt, N., Murray, M. M., Thut, G. & Schroeder, C. E. Multisensory integration: flexible use of general operations. Neuron 81, 1240-1253 (2014).
4. Stein, B. E., Meredith, M. A., Huneycutt, W. S. & McDade, L. Behavioral indices of multisensory integration: orientation to visual cues is affected by auditory stimuli. J. Cogn. Neurosci. 1, 12-24 (1989).
5. McMeniman, C. J., Corfas, R. A., Matthews, B. J., Ritchie, S. A. & Vosshall, L. B. Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156, 1060-1071 (2014).
6. Stein, B. E. & Stanford, T. R. Multisensory integration: current issues from the perspective of the single neuron. Nature Rev. Neurosci. 9, 255-266 (2008).
7. Cybenko, G. Approximation by superpositions of a sigmoidal function. Math. Control Signals Syst. 2, 303-314 (1989).
8. Duda, R. O. E. H. P. Stork, D. G. Pattern Classification (John Wiley and Sons, 2001).
9. Hastie, T., Friedman, J. & Tibshirani, R. The Elements of Statistical Learning Vol. 2 (Springer, 2009).
10. Rigotti, M. et al. The importance of mixed selectivity in complex cognitive tasks. Nature 497, 585-590 (2013).
11. Fetsch, C. R., Pouget, A., DeAngelis, G. C. & Angelaki, D. E. Neural correlates of reliability-based cue weighting during multisensory integration. Nature Neurosci. 15, 146-154 (2012).
12. Meredith, M. A. & Stein, B. E. Interactions among converging sensory inputs in the superior colliculus. Science 221, 389-391 (1983).
13. Meredith, M. A. & Stein, B. E. Descending efferents from the superior colliculus relay integrated multisensory information. Science 227, 657-659 (1985).
14. Olcese, U., Iurilli, G. & Medini, P. Cellular and synaptic architecture ofmultisensory integration in the mouse neocortex. Neuron 79, 579-593 (2013).
15. Homberg, U., Christensen, T. A. & Hildebrand, J. G. Structure and function of the deutocerebrum in insects. Annu. Rev. Entomol. 34, 477-501 (1989).
16. Milde, J. J. & Strausfeld, N. J. Cluster organization and response characteristics of the giant fiber pathway of the blowfly Calliphora erythrocephala. J. Comp. Neurol. 294, 59-75 (1990).
17. Mu, L., Bacon, J. P., Ito, K. & Strausfeld, N. J. Responses of Drosophila giant descending neurons to visual and mechanical stimuli. J. Exp. Biol. 217, 2121-2129 (2014).
18. Basura, G. J., Koehler, S. D. & Shore, S. E. Multi-sensory integration in brainstem and auditory cortex. Brain Res. 1485, 95-107 (2012).
19. Jain, R. & Shore, S. External inferior colliculus integrates trigeminal and acoustic information: unit responses to trigeminal nucleus and acoustic stimulation in the guinea pig. Neurosci. Lett. 395, 71-75 (2006).
20. Lakatos, P., Chen, C. M., O'Connell, M. N., Mills, A. & Schroeder, C. E. Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53, 279-292 (2007).
21. Shore, S. E.Multisensory integration in thedorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation. Eur. J. Neurosci. 21, 3334-3348 (2005).
22. Cardona, A. et al. An integrated micro-and macroarchitectural analysis of the Drosophila brain by computer-assisted serial section electron microscopy. PLoS Biol. 8, e1000502 (2010).
23. Saalfeld, S., Fetter, R., Cardona, A. & Tomancak, P. Elastic volume reconstruction fromseries of ultra-thin microscopy sections. Nature Methods 9, 717-720 (2012).
24. Pfeiffer, B. D. et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl Acad. Sci. USA 105, 9715-9720 (2008).
25. Pfeiffer, B. D. et al. Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735-755 (2010).
26. Li, H. H. et al. A GAL4 driver resource for developmental and behavioral studies on the larval CNS of Drosophila. Cell Rep. 8, 897-908 (2014).
27. Hwang, R. Y. et al. Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 17, 2105-2116 (2007).
28. Ohyama, T. et al. High-throughput analysis of stimulus-evoked behaviors in Drosophila larva revealsmultiplemodality-specific escape strategies. PLoSONE 8, e71706 (2013).
29. Tsubouchi, A., Caldwell, J. C. & Tracey, W. D. Dendritic filopodia, Ripped Pocket, NOMPC, and NMDARs contribute to the sense of touch in Drosophila larvae. Curr. Biol. 22, 2124-2134 (2012).
30. Yan, Z. et al. Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493, 221-225 (2013).
31. Zhang, W., Yan, Z., Jan, L. Y. & Jan, Y. N. Sound response mediated by the TRP channelsNOMPC, NANCHUNG, andINACTIVE inchordotonal organs of Drosophila larvae. Proc. Natl Acad. Sci. USA 110, 13612-13617 (2013).
32. Robertson, J. L., Tsubouchi, A. & Tracey, W. D. Larval defense against attack from parasitoid wasps requires nociceptive neurons. PLoS ONE 8, e78704 (2013).
33. Tracey, W. D. Jr, Wilson, R. I., Laurent, G. & Benzer, S. painless, a Drosophila gene essential for nociception. Cell 113, 261-273 (2003).
34. Vogelstein, J. T. et al. Discovery of brainwide neural-behavioralmaps viamultiscale unsupervised structure learning. Science 344, 386-392 (2014).
35. Xiang, Y. et al. Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468, 921-926 (2010).
36. Zhong, L. et al. Thermosensory and nonthermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat-sensor domains of a thermoTRP Channel. Cell Rep. 1, 43-55 (2012).
37. Schrader, S.&Merritt, D. J.Central projections of Drosophila sensory neurons in the transition from embryo to larva. J. Comp. Neurol. 425, 34-44 (2000).
38. Zlatic, M., Li, F., Strigini, M., Grueber, W. & Bate, M. Positional cues in the Drosophila nerve cord: semaphorins pattern the dorso-ventral axis. PLoS Biol. 7, e1000135 (2009).
39. Grueber, W. B. et al. Projections of Drosophilamultidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development 134, 55-64 (2007).
40. Klapoetke, N. C. et al. Independent optical excitation of distinct neural populations. Nature Methods 11, 338-346 (2014).
41. Ernst, M. O.&Bulthoff, H. H.Merging the senses into a robust percept. Trends Cogn. Sci. 8, 162-169 (2004).
42. Kenshalo, D. R., Iwata, K., Sholas, M. & Thomas, D. A. Response properties and organization of nociceptive neurons in area 1 of monkey primary somatosensory cortex. J. Neurophysiol. 84, 719-729 (2000).
43. Mendell, L. M. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp. Neurol. 16, 316-332 (1966).
44. Ohshiro, T., Angelaki, D. E. & DeAngelis, G. C. A normalization model of multisensory integration. Nature Neurosci. 14, 775-782 (2011).
45. Bargmann, C. I. & Marder, E. From the connectome to brain function. Nature Methods 10, 483-490 (2013).
46. White, J. G., Southgate, E., Thomson, J. N.&Brenner, S. Thestructure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1-340 (1986).
47. Bock, D. D. et al. Network anatomyand in vivo physiology of visual cortical neurons. Nature 471, 177-182 (2011).
48. Briggman, K. L., Helmstaedter, M. & Denk, W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183-188 (2011).
49. Kim, J. S. et al. Space-time wiring specificity supports direction selectivity in the retina. Nature 509, 331-336 (2014).
50. Takemura, S. Y. et al. A visual motion detection circuit suggested by Drosophila connectomics. Nature 500, 175-181 (2013).
51. Jenett, A. et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep. 2, 991-1001 (2012).
52. Hamada, F. N. et al. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217-220 (2008).
53. Kang, K. et al. Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481, 76-80 (2012).
54. Pfeiffer, B. D., Truman, J. W. & Rubin, G. M. Using translational enhancers to increase transgene expression in Drosophila. Proc. Natl Acad. Sci. USA 109, 6626-6631 (2012).
55. Chen, T.-W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
56. Tian, L. et al.Imaging neural activity inworms, flies and mice withimprovedGCaMP calcium indicators. Nature Methods 6, 875-881 (2009).
57. Ainsley, J. A. et al. Enhanced locomotion caused by loss of the Drosophila DEG/ENaC protein Pick-pocket1. Curr. Biol. 13, 1557-1563 (2003).
58. Baines, R. A., Uhler, J. P., Thompson, A., Sweeney, S. T. & Bate, M. Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523-1531 (2001).
59. Lima, S. Q. & Miesenbck, G. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141-152 (2005).
60. von Philipsborn, A. C. et al. Neuronal control of Drosophila courtship song. Neuron 69, 509-522 (2011).
61. Calleja, M., Moreno, E., Pelaz, S. & Morata, G. Visualization of gene expression in living adult Drosophila. Science 274, 252-255 (1996).
62. Luan, H., Peabody, N. C., Vinson, C. R.&White, B. H. Refined spatialmanipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52, 425-436 (2006).
63. Struhl, G. & Basler, K. Organizing activity of wingless protein in Drosophila. Cell 72, 527-540 (1993).
64. Swierczek, N. A., Giles, A. C., Rankin, C. H. & Kerr, R. A. High-throughput behavioral analysis in C. elegans. Nature Methods 8, 592-598 (2011).
65. Kabra, M., Robie, A. A., Rivera-Alba, M., Branson, S.&Branson, K. JAABA: interactive machine learning for automatic annotation of animal behavior. Nature Methods 10, 64-67 (2013).
66. Schneider, C. A. et al. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675 (2012).
67. Verstreken, P., Ohyama, T. & Bellen, H. J. in Exocytosis and Endocytosis 349-369 (Springer, 2008).
68. Glasbey, C. A. An analysis of histogram-based thresholding algorithms. CVGIP. Graph. Models Image Proc. 55, 532-537 (1993).
69. Sato, T. A modified method for lead staining of thin sections. J. Electron Microsc. (Tokyo) 17, 158-159 (1968).
70. Suloway, C. et al. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151, 41-60 (2005).
71. Saalfeld, S., Cardona, A., Hartenstein, V. & Tomancak, P. CATMAID: collaborative annotation toolkit for massive amounts of image data. Bioinformatics 25, 1984-1986 (2009).
72. Prokop, A. & Meinertzhagen, I. A. Development and structure of synaptic contacts in Drosophila. Semin. Cell Dev. Biol. 17, 20-30 (2006).
73. Landgraf, M., Snchez Soriano, N., Technau, G. M., Urban, J. & Prokop, A. Charting the Drosophila neuropile: a strategy for the standardised characterization of genetically amenable neurites. Dev. Biol. 260, 207-225 (2003).
74. Grueber, W. B., Jan, L. & Jan, Y. Tiling of the Drosophila epidermis bymultidendritic sensory neurons. Development 129, 2867-2878 (2002).
75. Bastian, M. et al. Gephi: an open source software for exploring and manipulating networks (International AAAI Conference on Weblogs and Social Media, 2009).
76. Bate, M., Goodman, C.&Spitzer, N.Embryonic development of identified neurons: Segment-specific differences in the H cell homologues. J. Neurosci. 1, 103-106 (1981).
77. Jefferis, G. S. et al. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128, 1187-1203 (2007).
78. Dayan, P. & Abbott, L. F. Theoretical Neuroscience (MIT Press, 2001).