A stochastic neuronal model predicts random search behaviors at multiple spatial scales in C. elegans

eLife

Volumn 5, Issue JANUARY2016, 2016, Pages

  Roberts, William M ^a   Augustine, Steven B ^b   Lawton, Kristy J ^c   Lindsay, Theodore H ^d   Thiele, Tod R ^e   Izquierdo, Eduardo J ^f   Faumont, Serge ^a   Lindsay, Rebecca A ^g   Britton, Matthew Cale ^h   Pokala, Navin ⁱ   Bargmann, Cornelia I ^j   Lockery, Shawn R ^a  

^a UNIVERSITY OF OREGON   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c REED COLLEGE   (United States)

^d California Institute of Technology   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

^f INDIANA UNIVERSITY   (United States)

^g CHILDREN S HOSPITAL LOS ANGELES   (United States)

^h UNIVERSITY OF MINNESOTA   (United States)

ⁱ NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

^j ROCKEFELLER UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIOR; CAENORHABDITIS ELEGANS; CONCEPTUAL FRAMEWORK; CONNECTOME; CONTROLLED STUDY; GENETIC MODEL; LOCOMOTION; MODEL; NERVE CELL; POPULATION MODEL; STATISTICAL MODEL; STOCHASTIC MODEL; WILD TYPE;

EID: 84961285205     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12572.001     Document Type: Article

References (109)

1. Abbott LF. 2008. Theoretical neuroscience rising. Neuron 60:489-495. doi: 10.1016/j.neuron.2008.10.019
2. Bargmann CI, Avery L. 1995. Laser killing of cells in Caenorhabditis elegans. Methods in Cell Biology 48:225-250. doi: 10.1016/S0091-679X(08)61390-4
3. Ben Arous J, Laffont S, Chatenay D. 2009. Molecular and sensory basis of a food related two-state behavior in C. elegans. PloS One 4:e7584. doi: 10.1371/journal.pone.0007584
4. Bendesky A, Tsunozaki M, Rockman MV, Kruglyak L, Bargmann CI. 2011. Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 472:313-318. doi: 10.1038/nature09821
5. Berg HC, Brown DA. 1972. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239: 500-504. doi: 10.1038/239500a0
6. Bertrand S, Bertrand A, Guevara-Carrasco R, Gerlotto F. 2007. Scale-invariant movements of fishermen: the same foraging strategy as natural predators. Ecological Applications: A Publication of the Ecological Society of America 17:331-337. doi: 10.1890/06-0303
7. Bhattacharya R, Touroutine D, Barbagallo B, Climer J, Lambert CM, Clark CM, Alkema MJ, Francis MM. 2014. A conserved dopamine-cholecystokinin signaling pathway shapes context-dependent Caenorhabditis elegans behavior. PLoS Genetics 10:e1004584. doi: 10.1371/journal.pgen.1004584
8. Block SM, Segall JE, Berg HC. 1982. Impulse responses in bacterial chemotaxis. Cell 31:215-226. doi: 10.1016/0092-8674(82)90421-4
9. Boon JP, Yip S. 1980. Molecular Hydrodynamics. Courier Dover Publications. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
10. Brockie PJ, Mellem JE, Hills T, Madsen DM, Maricq AV. 2001. The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion. Neuron 31: 617-630. doi: 10.1016/S0896-6273(01)00394-4
11. Brown CT, Liebovitch LS, Glendon R. 2007. Lvy flights in dobe ju/'hoansi foraging patternss. Human Ecology 35:129-138. doi: 10.1007/s10745-006-9083-4
12. Bohm H, Schildberger K. 1992. Brain neurones involved in the control of walking in the cricket gryllus bimaculatus. Journal of Experimental Biology 166:113-130.
13. Calhoun AJ, Chalasani SH, Sharpee TO. 2014. Maximally informative foraging by Caenorhabditis elegans. eLife 3. doi: 10.7554/eLife.04220
14. Calhoun AJ, Tong A, Pokala N, Fitzpatrick JA, Sharpee TO, Chalasani SH. 2015. Neural Mechanisms for Evaluating Environmental Variability in Caenorhabditis elegans. Neuron 86:428-441. doi: 10.1016/j.neuron.2015.03.026
15. Chalasani SH, Chronis N, Tsunozaki M, Gray JM, Ramot D, Goodman MB, Bargmann CI. 2007. Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450:63-70. doi: 10.1038/nature06292
16. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S. 1985. The neural circuit for touch sensitivity in Caenorhabditis elegans. The Journal of Neuroscience 5:956-964.
17. Colquhoun D, Hawkes AG. 1995. a q-matrix cookbook. how to write only one program to calculate the single-channel and macroscopic predictions for any kinetic mechanims. Single-Channel Recording:589-633. doi: 10.1007/978-1-4419-1229-9_20
18. Croll NA. 1975. Components and patterns in the behaviour of the nematode caenorhabditis elegans. Journal of Zoology 176:159-176. doi: 10.1111/j.1469-7998.1975.tb03191.x
19. Cronin CJ, Mendel JE, Mukhtar S, Kim YM, Stirbl RC, Bruck J, Sternberg PW. 2005. An automated system for measuring parameters of nematode sinusoidal movement. BMC Genetics 6:5. doi: 10.1186/1471-2156-6-5
20. Deliagina TG, Zelenin PV, Fagerstedt P, Grillner S, Orlovsky GN. 2000. Activity of reticulospinal neurons during locomotion in the freely behaving lamprey. Journal of Neurophysiology 83:853-863.
21. Dembrow NC, Jing J, Proekt A, Romero A, Vilim FS, Cropper EC, Weiss KR. 2003. A newly identified buccal interneuron initiates and modulates feeding motor programs in aplysia. Journal of Neurophysiology 90:2190-2204. doi: 10.1152/jn.00173.2003
22. Fang-Yen C, Alkema MJ, Samuel ADT. 2015. Illuminating neural circuits and behaviour in caenorhabditis elegans with optogenetics. Philosophical Transactions of the Royal Society B: Biological Sciences 370: 20140212. doi: 10.1098/rstb.2014.0212
23. Faumont S, Lindsay TH, Lockery SR. 2012. Neuronal microcircuits for decision making in C. elegans. Current Opinion in Neurobiology 22:580-591. doi: 10.1016/j.conb.2012.05.005
24. Faumont S, Rondeau G, Thiele TR, Lawton KJ, McCormick KE, Sottile M, Griesbeck O, Heckscher ES, Roberts WM, Doe CQ, Lockery SR. 2011. An image-free opto-mechanical system for creating virtual environments and imaging neuronal activity in freely moving Caenorhabditis elegans. PloS One 6:e24666. doi: 10.1371/journal.pone.0024666
25. Flavell SW, Pokala N, Macosko EZ, Albrecht DR, Larsch J, Bargmann CI. 2013. Serotonin and the neuropeptide PDF initiate and extend opposing behavioral states in C. elegans. Cell 154:1023-1035. doi: 10.1016/j.cell.2013.08.001
26. Fry AL, Laboy JT, Norman KR. 2014. VAV-1 acts in a single interneuron to inhibit motor circuit activity in Caenorhabditis elegans. Nature Communications 5:5579. doi: 10.1038/ncomms6579
27. Frezal L, Felix MA. 2015. C. elegans outside the Petri dish. eLife 4. doi: 10.7554/eLife.05849
28. Fujiwara M, Sengupta P, McIntire SL. 2002. Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36:1091-1102. doi: 10.1016/ S0896-6273(02)01093-0
29. Gao S, Xie L, Kawano T, Po MD, Guan S, Zhen M, Pirri JK, Alkema MJ. 2015. The NCA sodium leak channel is required for persistent motor circuit activity that sustains locomotion. Nature Communications 6:6323. doi: 10.1038/ncomms7323
30. Gloria-Soria A, Azevedo RB. 2008. npr-1 Regulates foraging and dispersal strategies in Caenorhabditis elegans. Current Biology 18:1694-1699. doi: 10.1016/j.cub.2008.09.043
31. Gordus A, Pokala N, Levy S, Flavell SW, Bargmann CI. 2015. Feedback from network states generates variability in a probabilistic olfactory circuit. Cell 161:215-227. doi: 10.1016/j.cell.2015.02.018
32. Gray J, Lissmann HW. 1964. The locomotion of nematodes. The Journal of Experimental Biology 41:135-154.
33. GRAY J. 1946. The mechanism of locomotion in snakes. The Journal of Experimental Biology 23:101-120.
34. Gray J. 1953. Undulatory propulsion. Quarterly Journal of Microscopical Science 3:551-578.
35. Gray JM, Hill JJ, Bargmann CI. 2005. A circuit for navigation in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 102:3184-3191. doi: 10.1073/pnas.0409009101
36. Hart AC, Sims S, Kaplan JM. 1995. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378:82-85. doi: 10.1038/378082a0
37. Harvey SC. 2009. Non-dauer larval dispersal in caenorhabditis elegans. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 312B:224-230. doi: 10.1002/jez.b.21287
38. Hedwig B. 2000. Control of cricket stridulation by a command neuron: efficacy depends on the behavioral state. Journal of Neurophysiology 83:712-722.
39. Hills T, Brockie PJ, Maricq AV. 2004. Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. The Journal of Neuroscience 24:1217-1225. doi: 10.1523/JNEUROSCI.1569-03.2004
40. Hopfield JJ. 1982. Neural networks and physical systems with emergent collective computational abilities. Proceedings of the National Academy of Sciences of the United States of America 79:2554-2558. doi: 10.1073/pnas.79.8.2554
41. Humphries NE, Queiroz N, Dyer JR, Pade NG, Musyl MK, Schaefer KM, Fuller DW, Brunnschweiler JM, Doyle TK, Houghton JD, Hays GC, Jones CS, Noble LR, Wearmouth VJ, Southall EJ, Sims DW. 2010. Environmental context explains Levy and Brownian movement patterns of marine predators. Nature 465:1066-1069. doi: 10.1038/nature09116
42. Humphries NE, Sims DW. 2014. Optimal foraging strategies: Levy walks balance searching and patch exploitation under a very broad range of conditions. Journal of Theoretical Biology 358:179-193. doi: 10.1016/j.jtbi.2014.05.032
43. Humphries NE, Weimerskirch H, Queiroz N, Southall EJ, Sims DW. 2012. Foraging success of biological Levy flights recorded in situ. Proceedings of the National Academy of Sciences of the United States of America 109: 7169-7174. doi: 10.1073/pnas.1121201109
44. lino Y, Yoshida K. 2009. Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans. The Journal of Neuroscience 29:5370-5380. doi: 10.1523/JNEUROSCI.3633-08.2009
45. Jander R. 1975. Ecological aspects of spatial orientation. Annual Review of Ecology and Systematics 6:171-188. doi: 10.1146/annurev.es.06.110175.001131
46. Kato S, Kaplan HS, Schrtodel T, Skora S, Lindsay TH, Yemini E, Lockery S, Zimmer M. 2015. Global brain dynamics embed the motor command sequence of Caenorhabditis elegans. Cell 163:656-669. doi: 10.1016/j.cell.2015.09.034
47. Kawano T, Po MD, Gao S, Leung G, Ryu WS, Zhen M. 2011. An imbalancing act: gap junctions reduce the backward motor circuit activity to bias C. elegans for forward locomotion. Neuron 72:572-586. doi: 10.1016/j. neuron.2011.09.005
48. Kocabas A, Shen CH, Guo ZV, Ramanathan S. 2012. Controlling interneuron activity in Caenorhabditis elegans to evoke chemotactic behaviour. Nature 490:273-277. doi: 10.1038/nature11431
49. Kunert J, Shlizerman E, Kutz JN. 2014. Low-dimensional functionality of complex network dynamics: neurosensory integration in the Caenorhabditis Elegans connectome. Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics 89. doi: 10.1103/PhysRevE.89.052805
50. Li W, Feng Z, Sternberg PW, Xu XZ. 2006. A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440:684-687. doi: 10.1038/nature04538
51. Lindsay TH, Thiele TR, Lockery SR. 2011. Optogenetic analysis of synaptic transmission in the central nervous system of the nematode Caenorhabditis elegans. Nature Communications 2:306. doi: 10.1038/ncomms1304
52. Lipton J, Kleemann G, Ghosh R, Lints R, Emmons SW. 2004. Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. The Journal of Neuroscience 24:7427-7434. doi: 10.1523/JNEUROSCI.1746-04.2004
53. Liu P, Chen B, Wang ZW. 2014. SLO-2 potassium channel is an important regulator of neurotransmitter release in Caenorhabditis elegans. Nature Communications 5:5155. doi: 10.1038/ncomms6155
54. Liu S, Schulze E, Baumeister R. 2012. Temperature- and touch-sensitive neurons couple CNG and TRPV channel activities to control heat avoidance in Caenorhabditis elegans. PloS One 7:e32360. doi: 10.1371/journal.pone.0032360
55. Lo CC, Chou T, Penzel T, Scammell TE, Strecker RE, Stanley HE, Ivanov PCh. 2004. Common scale-invariant patterns of sleep-wake transitions across mammalian species. Proceedings of the National Academy of Sciences of the United States of America 101:17545-17548. doi: 10.1073/pnas.0408242101
56. Lockery SR, Goodman MB. 1998. Tight-seal whole-cell patch clamping of Caenorhabditis elegans neurons. Methods in Enzymology 293:201-217. doi: 10.1016/S0076-6879(98)93016-6
57. Lockery SR. 2011. The computational worm: spatial orientation and its neuronal basis in C. elegans. Current Opinion in Neurobiology 21:782-790. doi: 10.1016/j.conb.2011.06.009
58. Luo L, Wen Q, Ren J, Hendricks M, Gershow M, Qin Y, Greenwood J, Soucy ER, Klein M, Smith-Parker HK, Calvo AC, Colon-Ramos DA, Samuel AD, Zhang Y. 2014. Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit. Neuron 82:1115-1128. doi: 10.1016/j.neuron.2014.05.010
59. Mantegna RN, Stanley HE. 1994. Stochastic process with ultraslow convergence to a Gaussian: The truncated Levy flight. Physical Review Letters 73:2946-2949. doi: 10.1103/PhysRevLett.73.2946
60. Mellem JE, Brockie PJ, Madsen DM, Maricq AV. 2008. Action potentials contribute to neuronal signaling in C. elegans. Nature Neuroscience 11:865-867. doi: 10.1038/nn.2131
61. Mello C, Fire A. 1995. DNA transformation. Methods in Cell Biology 48:451-182. doi: 10.1016/S0091-679X(08)61399-0
62. Mohammadi A, Byrne Rodgers J, Kotera I, Ryu WS. 2013. Behavioral response of Caenorhabditis elegans to localized thermal stimuli. BMC Neuroscience 14:66. doi: 10.1186/1471-2202-14-66
63. Nguyen JP, Shipley FB, Linder AN, Plummer GS, Liu M, Setru SU, Shaevitz JW, Leifer AM. 2015. Whole-brain calcium imaging with cellular resolution in freelybehaving caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America:201507110. doi: 10.1073/pnas.1507110112
64. Peliti M, Chuang JS, Shaham S. 2013. Directional locomotion of C. elegans in the absence of external stimuli. PloS One 8:e78535. doi: 10.1371/journal.pone.0078535
65. Pereira L, Kratsios P, Serrano-Saiz E, Sheftel H, Mayo AE, Hall DH, White JG, LeBoeuf B, Garcia LR, Alon U, Hobert O. 2015. A cellular and regulatory map of the cholinergic nervous system of C. elegans. eLife 4. doi: 10.7554/eLife.12432
66. Pierce-Shimomura JT, Morse TM, Lockery SR. 1999. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. The Journal of Neuroscience 19:9557-9569.
67. Piggott BJ, Liu J, Feng Z, Wescott SA, Xu XZ. 2011. The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans. Cell 147:922-933. doi: 10.1016/j.cell.2011.08.053
68. Pokala N, Liu Q, Gordus A, Bargmann CI. 2014. Inducible and titratable silencing of Caenorhabditis elegans neurons in vivo with histamine-gated chloride channels. Proceedings of the National Academy of Sciences of the United States of America 111:2770-2775. doi: 10.1073/pnas.1400615111
69. Pradel E, Zhang Y, Pujol N, Matsuyama T, Bargmann CI, Ewbank JJ. 2007. Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 104:2295-2300. doi: 10.1073/pnas.0610281104
70. Prevedel R, Yoon YG, Hoffmann M, Pak N, Wetzstein G, Kato S, Schrodel T, Raskar R, Zimmer M, Boyden ES, Vaziri A. 2014. Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy. Nature Methods 11:727-730. doi: 10.1038/nmeth.2964
71. Pujol N, Link EM, Liu LX, Kurz CL, Alloing G, Tan MW, Ray KP, Solari R, Johnson CD, Ewbank JJ. 2001. A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Current Biology 11: 809-821. doi: 10.1016/S0960-9822(01)00241-X
72. Qi YB, Garren EJ, Shu X, Tsien RY, Jin Y. 2012. Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singlet oxygen generating protein miniSOG. Proceedings ofthe National Academy of Sciences of the United States of America 109:7499-7504. doi: 10.1073/pnas.1204096109
73. Qi YB, Po MD, Mac P, Kawano T, Jorgensen EM, Zhen M, Jin Y. 2013. Hyperactivation of B-type motor neurons results in aberrant synchrony of the Caenorhabditis elegans motor circuit. The Journal of Neuroscience 33: 5319-5325. doi: 10.1523/JNEUROSCI.4017-12.2013
74. Rabiner L, Juang B. 1986. An introduction to hidden markov models. IEEE ASSP Magazine 3:4-16. doi: 10.1109/MASSP.1986.1165342
75. Rabiner LR. 1989. A tutorial on hidden markov models and selected applications in speech recognition. Proceedings of the IEEE 77:257-286. doi: 10.1109/5.18626
76. Rakowski F, Srinivasan J, Sternberg PW, Karbowski J. 2013. Synaptic polarity of the interneuron circuit controlling C. elegans locomotion. Frontiers in Computational Neuroscience 7. doi: 10.3389/fncom.2013.00128
77. Reddy KC, Andersen EC, Kruglyak L, Kim DH. 2009. A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 323:382-384. doi: 10.1126/science.1166527
78. Ryu WS, Samuel AD. 2002. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined Thermal stimuli. The Journal of Neuroscience 22:5727-5733.
79. Salvador LCM, Bartumeus F, Levin SA, Ryu WS. 2014. Mechanistic analysis of the search behaviour of caenorhabditis elegans. Journal of the Royal Society Interface 11:20131092. doi: 10.1098/rsif.2013.1092
80. Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE. 2010. Sleep state switching. Neuron 68:1023-1042. doi: 10.1016/j.neuron.2010.11.032
81. Satterlie RA, Norekian TP. 2001. Mechanisms of locomotory speed change: the pteropod solution. American Zoologist 41:1001-1008. doi: 10.1093/icb/41.4.1001
82. Schmitt C, Schultheis C, Pokala N, Husson SJ, Liewald JF, Bargmann CI, Gottschalk A. 2012. Specific expression of channelrhodopsin-2 in single neurons of Caenorhabditis elegans. PloS One 7:e43164. doi: 10.1371/journal.pone.0043164
83. Schrodel T, Prevedel R, Aumayr K, Zimmer M, Vaziri A. 2013. Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light. Nature Methods 10:1013-1020. doi: 10.1038/nmeth.2637
84. Shingai R. 2000. Durations and frequencies of free locomotion in wild type and GABAergic mutants of Caenorhabditis elegans. Neuroscience Research 38:71-84. doi: 10.1016/S0168-0102(00)00148-6
85. Shtonda BB, Avery L. 2006. Dietary choice behavior in Caenorhabditis elegans. The Journal of Experimental Biology 209:89-102. doi: 10.1242/jeb.01955
86. Sims DW, Humphries NE, Bradford RW, Bruce BD. 2012. Levy flight and Brownian search patterns of a free-ranging predator reflect different prey field characteristics. The Journal of Animal Ecology 81:432-442. doi: 10. 1111/j.1365-2656.2011.01914.x
87. Sirota MG, Di Prisco GV, Dubuc R. 2000. Stimulation of the mesencephalic locomotor region elicits controlled swimming in semi-intact lampreys. The European Journal of Neuroscience 12:4081-4092. doi: 10.1046/j.1460-9568.2000.00301.x
88. Stephens GJ, Bueno de Mesquita M, Ryu WS, Bialek W. 2011. Emergence of long timescales and stereotyped behaviors in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 108:7286-7289. doi: 10.1073/pnas.1007868108
89. Stephens GJ, Johnson-Kerner B, Bialek W, Ryu WS. 2008. Dimensionality and dynamics in the behavior of C. elegans. PLoS Computational Biology 4:e1000028. doi: 10.1371/journal.pcbi.1000028
90. Stephens GJ, Johnson-Kerner B, Bialek W, Ryu WS. 2010. From modes to movement in the behavior of Caenorhabditis elegans. PloS One 5:e13914. doi: 10.1371/journal.pone.0013914
91. Stiller W. 1989. Arrhenius Equation and Non-Equilibrium Kinetics: 100 Years Arrhenius Equation. BSB BG Teubner.
92. Stirman JN, Brauner M, Gottschalk A, Lu H. 2010. High-throughput study of synaptic transmission at the neuromuscular junction enabled by optogenetics and microfluidics. Journal ofNeuroscience Methods 191:9093. doi: 10.1016/j.jneumeth.2010.05.019
93. Styer KL, Singh V, Macosko E, Steele SE, Bargmann CI, Aballay A. 2008. Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science 322:460-464. doi: 10.1126/science.1163673
94. Suzuki H, Thiele TR, Faumont S, Ezcurra M, Lockery SR, Schafer WR. 2008. Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 454:114-117. doi: 10.1038/nature06927
95. Thiele TR, Faumont S, Lockery SR. 2009. The neural network for chemotaxis to tastants in Caenorhabditis elegans is specialized for temporal differentiation. The Journal of Neuroscience 29:11904-11911. doi: 10.1523/JNEUROSCI.0594-09.2009
96. Tobin DM, Madsen DM, Kahn-Kirby A, Peckol EL, Moulder G, Barstead R, Maricq AV, Bargmann CI. 2002. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35:307-318. doi: 10.1016/S0896-6273(02)00757-2
97. Tsalik EL, Hobert O. 2003. Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. Journal of Neurobiology 56:178-197. doi: 10.1002/neu.10245
98. Varshney LR, Chen BL, Paniagua E, Hall DH, Chklovskii DB. 2011. Structural properties of the Caenorhabditis elegans neuronal network. PLoS Computational Biology 7:e1001066. doi: 10.1371/journal.pcbi.1001066
99. Venkatachalam V, Ji N, Wang X, Clark C, Mitchell JK, Klein M, Tabone CJ, Florman J, Ji H, Greenwood J, Chisholm AD, Srinivasan J, Alkema M, Zhen M, Samuel AD. 2016. Pan-neuronal imaging in roaming Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 113. doi: 10.1073/pnas.1507109113
100. Viswanathan GM. 2011. The physics of foraging: an introduction to random searches and biological encounters. Cambridge University Press.
101. Viterbi A. 1967. Error bounds for convolutional codes and an asymptotically optimum decoding algorithm. IEEE Transactions on Information Theory 13:260-269. doi: 10.1109/TIT.1967.1054010
102. Wakabayashi T, Kitagawa I, Shingai R. 2004. Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. Neuroscience Research 50:103-111. doi: 10.1016/j.neures.2004.06.005
103. Weeks JC, Kristan WB. 1978. Initiation maintenance and modulation of swimming in the medicinal leech by the activity of a single neurone. The Journal of Experimental Biology 77:71-88.
104. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode caenorhabditis elegans. Philosophical Transactions of the Royal Society B: Biological Sciences 314: 1-340. doi: 10.1098/rstb.1986.0056
105. Wicks SR, Roehrig CJ, Rankin CH. 1996. A dynamic network simulation of the nematode tap withdrawal circuit: predictions concerning synaptic function using behavioral criteria. The Journal of Neuroscience 16:4017-4031.
106. Wittenburg N, Baumeister R. 1999. Thermal avoidance in Caenorhabditis elegans: an approach to the study of nociception. Proceedings of the National Academy of Sciences of the United States of America 96:10477-10482. doi: 10.1073/pnas.96.18.10477
107. Xie L, Gao S, Alcaire SM, Aoyagi K, Wang Y, Griffin JK, Stagljar I, Nagamatsu S, Zhen M. 2013. NLF-1 delivers a sodium leak channel to regulate neuronal excitability and modulate rhythmic locomotion. Neuron 77:1069-1082. doi: 10.1016/j.neuron.2013.01.018
108. Zhao B, Khare P, Feldman L, Dent JA. 2003. Reversal frequency in Caenorhabditis elegans represents an integrated response to the state of the animal and its environment. The Journal of Neuroscience 23:5319-5328.
109. Zheng Y, Brockie PJ, Mellem JE, Madsen DM, Maricq AV. 1999. Neuronal control of locomotion in C. elegans is modified by a dominant mutation in the GLR-1 ionotropic glutamate receptor. Neuron 24:347-361. doi: 10.1016/S0896-6273(00)80849-1