Mapping the Neural Substrates of Behavior

Cell

Volumn 170, Issue 2, 2017, Pages 393-406.e28

  Robie, Alice A ^a   Hirokawa, Jonathan ^a,b   Edwards, Austin W ^a   Umayam, Lowell A ^a   Lee, Allen ^a   Phillips, Mary L ^a,d   Card, Gwyneth M ^a   Korff, Wyatt ^a   Rubin, Gerald M ^a   Simpson, Julie H ^a,c   Reiser, Michael B ^a   Branson, Kristin ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

behavior; computer vision; Drosophila; machine learning; neural activation; neural anatomy; neural substrates; neuroscience; whole brain mapping

Indexed keywords

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CONTROL; BRAIN MAPPING; COMPUTER VISION; CONTROLLED STUDY; COURTSHIP; DROSOPHILA MELANOGASTER; FEMALE; IMAGE PROCESSING; LOCOMOTION; MACHINE LEARNING; MALE; MOTOR CONTROL; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; SLEEP; SOCIAL BEHAVIOR; ANIMAL; ANIMAL BEHAVIOR; PHYSIOLOGY; PROCEDURES; SOFTWARE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN MAPPING; DROSOPHILA MELANOGASTER; FEMALE; LOCOMOTION; MALE; SOFTWARE;

EID: 85023610188     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.06.032     Document Type: Article

References (54)

1. Ahrens, M.B., Orger, M.B., Robson, D.N., Li, J.M., Keller, P.J., Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 10 (2013), 413–420.
2. Aso, Y., Hattori, D., Yu, Y., Johnston, R.M., Iyer, N.A., Ngo, T.T., Dionne, H., Abbott, L.F., Axel, R., Tanimoto, H., Rubin, G.M., The neuronal architecture of the mushroom body provides a logic for associative learning. eLife, 3, 2014, e04577.
3. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate - a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57 (1995), 289–300.
4. Benjamini, Y., Yekutieli, D., The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29 (2001), 1165–1188.
5. Berman, G.J., Choi, D.M., Bialek, W., Shaevitz, J.W., Mapping the stereotyped behaviour of freely moving fruit flies. J. R. Soc. Interface, 11, 2014, 20140672.
6. Branson, K., Robie, A.A., Bender, J., Perona, P., Dickinson, M.H., High-throughput ethomics in large groups of Drosophila. Nat. Methods 6 (2009), 451–457.
7. Cavanaugh, D.J., Geratowski, J.D., Wooltorton, J.R., Spaethling, J.M., Hector, C.E., Zheng, X., Johnson, E.C., Eberwine, J.H., Sehgal, A., Identification of a circadian output circuit for rest:activity rhythms in Drosophila. Cell 157 (2014), 689–701.
8. Chiang, A.S., Lin, C.Y., Chuang, C.C., Chang, H.M., Hsieh, C.H., Yeh, C.W., Shih, C.T., Wu, J.J., Wang, G.T., Chen, Y.C., et al. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 21 (2011), 1–11.
9. Costa, M., Manton, J.D., Ostrovsky, A.D., Prohaska, S., Jefferis, G.S., NBLAST: rapid, sensitive comparison of neuronal structure and construction of neuron family databases. Neuron 91 (2016), 293–311.
10. Dasgupta, S., Long, P.M., Performance guarantees for hierarchical clustering. J. Comput. Syst. Sci. 70 (2005), 555–569.
11. Dus, M., Lai, J.S., Gunapala, K.M., Min, S., Tayler, T.D., Hergarden, A.C., Geraud, E., Joseph, C.M., Suh, G.S., Nutrient sensor in the brain directs the action of the brain-gut axis in Drosophila. Neuron 87 (2015), 139–151.
12. Foltenyi, K., Greenspan, R.J., Newport, J.W., Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat. Neurosci. 10 (2007), 1160–1167.
13. Fosque, B.F., Sun, Y., Dana, H., Yang, C.T., Ohyama, T., Tadross, M.R., Patel, R., Zlatic, M., Kim, D.S., Ahrens, M.B., et al. Neural circuits. Labeling of active neural circuits in vivo with designed calcium integrators. Science 347 (2015), 755–760.
14. Groppe, D.M., Urbach, T.P., Kutas, M., Mass univariate analysis of event-related brain potentials/fields I: a critical tutorial review. Psychophysiology 48 (2011), 1711–1725.
15. Hale, M.E., Katz, H.R., Peek, M.Y., Fremont, R.T., Neural circuits that drive startle behavior, with a focus on the Mauthner cells and spiral fiber neurons of fishes. J. Neurogenet. 30 (2016), 89–100.
16. Hampel, S., Franconville, R., Simpson, J.H., Seeds, A.M., A neural command circuit for grooming movement control. eLife, 4, 2015, e08758.
17. Hanesch, U., Fischbach, K.-F., Heisenberg, M., Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 257 (1989), 343–366.
18. Hoopfer, E.D., Jung, Y., Inagaki, H.K., Rubin, G.M., Anderson, D.J., P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. eLife, 4, 2015, e11346.
19. Hsu, C.T., Bhandawat, V., Organization of descending neurons in Drosophila melanogaster. Sci. Rep., 6, 2016, 20259.
20. Ito, K., Shinomiya, K., Ito, M., Armstrong, J.D., Boyan, G., Hartenstein, V., Harzsch, S., Heisenberg, M., Homberg, U., Jenett, A., et al., Insect Brain Name Working Group. A systematic nomenclature for the insect brain. Neuron 81 (2014), 755–765.
21. Jenett, A., Rubin, G.M., Ngo, T.T., Shepherd, D., Murphy, C., Dionne, H., Pfeiffer, B.D., Cavallaro, A., Hall, D., Jeter, J., et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep. 2 (2012), 991–1001.
22. Kabra, M., Robie, A.A., Rivera-Alba, M., Branson, S., Branson, K., JAABA: interactive machine learning for automatic annotation of animal behavior. Nat. Methods 10 (2013), 64–67.
23. Kato, S., Kaplan, H.S., Schrödel, T., Skora, S., Lindsay, T.H., Yemini, E., Lockery, S., Zimmer, M., Global brain dynamics embed the motor command sequence of Caenorhabditis elegans. Cell 163 (2015), 656–669.
24. Luan, H., Peabody, N.C., Vinson, C.R., White, B.H., Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52 (2006), 425–436.
25. Mann, K., Gordon, M.D., Scott, K., A pair of interneurons influences the choice between feeding and locomotion in Drosophila. Neuron 79 (2013), 754–765.
26. Martín-Peña, A., Acebes, A., Rodríguez, J.R., Chevalier, V., Casas-Tinto, S., Triphan, T., Strauss, R., Ferrús, A., Cell types and coincident synapses in the ellipsoid body of Drosophila. Eur. J. Neurosci. 39 (2014), 1586–1601.
27. Nern, A., Pfeiffer, B.D., Rubin, G.M., Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proc. Natl. Acad. Sci. USA 112 (2015), E2967–E2976.
28. Nilsen, S.P., Chan, Y.B., Huber, R., Kravitz, E.A., Gender-selective patterns of aggressive behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 101 (2004), 12342–12347.
29. Otsuna, H., Ito, K., Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J. Comp. Neurol. 497 (2006), 928–958.
30. Owald, D., Lin, S., Waddell, S., Light, heat, action: neural control of fruit fly behaviour. Philos. Trans. R. Soc. Lond. B Biol. Sci., 370, 2015, 20140211.
31. Panser, K., Tirian, L., Schulze, F., Villalba, S., Jefferis, G.S., Bühler, K., Straw, A.D., Automatic segmentation of Drosophila neural compartments using GAL4 expression data reveals novel visual pathways. Curr. Biol. 26 (2016), 1943–1954.
32. Penfield, W., The supplementary motor area in the cerebral cortex of man. Arch Psychiatr Nervenkr Z Gesamte Neurol Psychiatr 185 (1950), 670–674.
33. Peng, H., Chung, P., Long, F., Qu, L., Jenett, A., Seeds, A.M., Myers, E.W., Simpson, J.H., BrainAligner: 3D registration atlases of Drosophila brains. Nat. Methods 8 (2011), 493–500.
34. Pfeiffer, B.D., Jenett, A., Hammonds, A.S., Ngo, T.T., Misra, S., Murphy, C., Scully, A., Carlson, J.W., Wan, K.H., Laverty, T.R., et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. USA 105 (2008), 9715–9720.
35. Pfeiffer, B.D., Ngo, T.T., Hibbard, K.L., Murphy, C., Jenett, A., Truman, J.W., Rubin, G.M., Refinement of tools for targeted gene expression in Drosophila. Genetics 186 (2010), 735–755.
36. Pfeiffer, K., Kinoshita, M., Homberg, U., Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J. Neurophysiol. 94 (2005), 3903–3915.
37. Randlett, O., Wee, C.L., Naumann, E.A., Nnaemeka, O., Schoppik, D., Fitzgerald, J.E., Portugues, R., Lacoste, A.M., Riegler, C., Engert, F., Schier, A.F., Whole-brain activity mapping onto a zebrafish brain atlas. Nat. Methods 12 (2015), 1039–1046.
38. Renn, S.C., Armstrong, J.D., Yang, M., Wang, Z., An, X., Kaiser, K., Taghert, P.H., Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. J. Neurobiol. 41 (1999), 189–207.
39. Schoofs, A., Hückesfeld, S., Schlegel, P., Miroschnikow, A., Peters, M., Zeymer, M., Spieß, R., Chiang, A.S., Pankratz, M.J., Selection of motor programs for suppressing food intake and inducing locomotion in the Drosophila brain. PLoS Biol., 12, 2014, e1001893.
40. Schwarz, R.F., Branicky, R., Grundy, L.J., Schafer, W.R., Brown, A.E., Changes in postural syntax characterize sensory modulation and natural variation of C. elegans locomotion. PLoS Comput. Biol., 11, 2015, e1004322.
41. Seelig, J.D., Jayaraman, V., Feature detection and orientation tuning in the Drosophila central complex. Nature 503 (2013), 262–266.
42. Simon, J.C., Dickinson, M.H., A new chamber for studying the behavior of Drosophila. PLoS ONE, 5, 2010, e8793.
43. Sivanantharajah, L., Zhang, B., Current techniques for high-resolution mapping of behavioral circuits in Drosophila. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 201 (2015), 895–909.
44. Strauss, R., Heisenberg, M., A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci. 13 (1993), 1852–1861.
45. Träger, U., Wagner, R., Bausenwein, B., Homberg, U., A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J. Comp. Neurol. 506 (2008), 288–300.
46. Triphan, T., Nern, A., Roberts, S.F., Korff, W., Naiman, D.Q., Strauss, R., A screen for constituents of motor control and decision making in Drosophila reveals visual distance-estimation neurons. Sci. Rep., 6, 2016, 27000.
47. Vogelstein, J.T., Park, Y., Ohyama, T., Kerr, R.A., Truman, J.W., Priebe, C.E., Zlatic, M., Discovery of brainwide neural-behavioral maps via multiscale unsupervised structure learning. Science 344 (2014), 386–392.
48. von Philipsborn, A.C., Liu, T., Yu, J.Y., Masser, C., Bidaye, S.S., Dickson, B.J., Neuronal control of Drosophila courtship song. Neuron 69 (2011), 509–522.
49. Walker, R.G., Willingham, A.T., Zuker, C.S., A Drosophila mechanosensory transduction channel. Science 287 (2000), 2229–2234.
50. Wolff, T., Iyer, N.A., Rubin, G.M., Neuroarchitecture and neuroanatomy of the Drosophila central complex: A GAL4-based dissection of protocerebral bridge neurons and circuits. J. Comp. Neurol. 523 (2015), 997–1037.
51. Wu, M., Nern, A., Williamson, W.R., Morimoto, M.M., Reiser, M.B., Card, G.M., Rubin, G.M., Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs. eLife, 5, 2016, e21022.
52. Yamamoto, D., Koganezawa, M., Genes and circuits of courtship behaviour in Drosophila males. Nat. Rev. Neurosci. 14 (2013), 681–692.
53. Young, J.M., Armstrong, J.D., Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J. Comp. Neurol. 518 (2010), 1500–1524.
54. Yu, J.Y., Kanai, M.I., Demir, E., Jefferis, G.S., Dickson, B.J., Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr. Biol. 20 (2010), 1602–1614.