Running hot and cold: Behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila

Genes and Development

Volumn 24, Issue 21, 2010, Pages 2365-2382

  Garrity, Paul A ^a   Goodman, Miriam B ^b   Samuel, Aravinthan D ^c   Sengupta, Piali ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

C. Elegans; cGMP; Drosophila; Thermosensory; Thermotaxis; TRP

Indexed keywords

NEUROTRANSMITTER;

BEHAVIORAL RESEARCH; BODY TEMPERATURE SENSATION; CAENORHABDITIS ELEGANS; DROSOPHILA; ETHOLOGY; GENETIC ANALYSIS; HEAT SENSITIVITY; LARVA; NERVE CELL NETWORK; NOMENCLATURE; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; REVIEW; SENSORY NERVE CELL; TEMPERATURE SENSITIVITY; THERMORECEPTOR; THERMOSENSORY NERVE CELL; THERMOTAXIS;

ANIMALS; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; COLD TEMPERATURE; DROSOPHILA MELANOGASTER; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HOT TEMPERATURE; SENSORY RECEPTOR CELLS; THERMOSENSING;

ANIMALIA; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; NEMATODA;

EID: 78049433579     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1953710     Document Type: Review

References (144)

1. Ailion M, Thomas JH. 2000. Dauer formation induced by high temperatures in Caenorhabditis elegans. Genetics 156: 1047-1067.
2. Ainsley JA, Kim MJ, Wegman LJ, Pettus JM, Johnson WA. 2008. Sensory mechanisms controlling the timing of larval developmental and behavioral transitions require the Drosophila DEG/ENaC subunit, Pickpocket1. Dev Biol 322: 46-55.
3. Anderson JL, Albergotti L, Proulx S, Peden C, Huey RB, Phillips PC. 2007. Thermal preference of Caenorhabditis elegans: A null model and empirical tests. J Exp Biol 210: 3107-3116.
4. Antebi A, Yeh WH, Tait D, Hedgecock EM, Riddle DL. 2000. daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 14: 1512-1527.
5. Bargmann CI. 2006. Chemosensation in C. elegans. In Worm Book (ed. The C. elegans Research Community). WormBook. doi: 10.1895/wormbook.1.123.1. http://www.wormbook.org.
6. Bennett AF. 1990. Thermal dependence of locomotor capacity. Am J Physiol 259: R253-R258.
7. Biron D, Shibuya M, Gabel C, Wasserman SM, Clark DA, Brown A, Sengupta P, Samuel AD. 2006. A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans. Nat Neurosci 9: 1499-1505.
8. Biron D, Wasserman SM, Thomas JH, Samuel AD, Sengupta P. 2008. An olfactory neuron responds stochastically to temperature and modulates C. elegans thermotactic behavior. Proc Natl Acad Sci 105: 11002-11007.
9. Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H, Rubin G, Pak WL. 1988. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54: 723-733.
10. Branson K, Robie AA, Bender J, Perona P, Dickinson MH. 2009. High-throughput ethomics in large groups of Drosophila. Nat Methods 6: 451-457.
11. Bullock TH, Diecke FP. 1956. Properties of an infra-red receptor. J Physiol 134: 47-87.
12. Butcher RA, Fujita M, Schroeder FC, Clardy J. 2007. Small molecule signaling of dauer formation in C. elegans. Nat Chem Biol 3: 420-422.
13. Butcher RA, Ragains JR, Kim E, Clardy J. 2008. A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components. Proc Natl Acad Sci 105: 14288-14292.
14. Butcher RA, Ragains JR, Clardy J. 2009. An indole-containing dauer pheromone component with unusual dauer inhibitory activity at higher concentrations. Org Lett 11: 3100-3103.
15. Card G, Dickinson MH. 2008. Visually mediated motor planning in the escape response of Drosophila. Curr Biol 18: 1300-1307.
16. Chalasani SH, Chronis N, Tsunozaki M, Gray JM, Ramot D, Goodman MB, Bargmann CI. 2007. Dissecting a neural circuit for food-seeking behavior in Caenorhabditis elegans. Nature 450: 63-70. (Pubitemid 350070575)
17. Chalasani SH, Kato S, Albrecht DR, Nakagawa T, Abbott LF, Bargmann CI. 2010. Neuropeptide feedback modifies odorevoked dynamics in Caenorhabditis elegans olfactory neurons. Nat Neurosci 13: 615-621.
18. Chatzigeorgiou M, Yoo S, Watson JD, Lee WH, Spencer WC, Kindt KS, Hwang SW, Miller DM III, Treinin M, Driscoll M, et al. 2010. Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat Neurosci 13: 861-868.
19. Chi CA, Clark DA, Lee S, Biron D, Luo L, Gabel CV, Brown J, Sengupta P, Samuel AD. 2007. Temperature and food mediate long-term thermotactic behavioral plasticity by association- independent mechanisms in C. elegans. J Exp Biol 210: 4043-4052. (Pubitemid 350275044)
20. Chung SH, Clark DA, Gabel CV, Mazur E, Samuel AD. 2006. The role of the AFD neuron in C. elegans thermotaxis analyzed using femtosecond laser ablation. BMC Neurosci 7: 30. doi: 10.1186/1471-2202-7-30.
21. Clark DA, Biron D, Sengupta P, Samuel ADT. 2006. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in C. elegans. J Neurosci 26: 7444-7451. (Pubitemid 44315213)
22. Clark DA, Gabel CV, Gabel H, Samuel AD. 2007a. Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. J Neurosci 27: 6083-6090.
23. Clark DA, Gabel CV, Lee TM, Samuel AD. 2007b. Short-term adaptation and temporal processing in the cryophilic response of Caenorhabditis elegans. J Neurophysiol 97: 1903-1910.
24. Coburn C, Bargmann CI. 1996. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17: 695-706. (Pubitemid 26365348)
25. Colosimo ME, Brown A, Mukhopadhyay S, Gabel C, Lanjuin AE, Samuel AD, Sengupta P. 2004. Identification of thermosensory and olfactory neuron-specific genes via expression profiling of single neuron types. Curr Biol 14: 2245-2251.
26. Conti B, Sanchez-Alavez M, Winsky-Sommerer R, Morale MC, Lucero J, Brownell S, Fabre V, Huitron-Resendiz S, Henriksen S, Zorrilla EP, et al. 2006. Transgenic mice with a reduced core body temperature have an increased life span. Science 314: 825-828.
27. Damann N, Voets T, Nilius B. 2008. TRPs in our senses. Curr Biol 18: R880-R889. doi: 10.1016/j.cub.2008.07.063.
28. Deal J. 1941. The temperature preferendum of certain insects. J Anim Ecol 10: 323-356.
29. Dhaka A, Viswanath V, Patapoutian A. 2006. TRP ion channels and temperature sensation. Annu Rev Neurosci 29: 135-161. (Pubitemid 44476842)
30. Dillon ME, Wang G, Garrity PA, Huey RB. 2009. Review: Thermal preference in Drosophila. J Therm Biol 34: 109-119.
31. Duistermars BJ, Chow DM, Frye MA. 2009. Flies require bilateral sensory input to track odor gradients in flight. Curr Biol 19: 1301-1307.
32. Dusenbery DB, Barr J. 1980. Thermal limits and chemotaxis in mutants of the nematode Caenorhabditis elegans defective in thermotaxis. J Comp Physiol 137: 353-356.
33. Dusenbery DB, Sheridan RE, Russell RL. 1975. Chemotaxis-defective mutants of the nematode Caenorhabditis elegans. Genetics 80: 297-309.
34. Etchberger JF, Lorch A, Sleumer MC, Zapf R, Jones SJ, Marra MA, Holt RA, Moerman DG, Hobert O. 2007. The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. Genes Dev 21: 1653-1674. (Pubitemid 47026369)
35. Fry SN, Sayaman R, Dickinson MH. 2005. The aerodynamics of hovering flight in Drosophila. J Exp Biol 208: 2303-2318.
36. Fry SN, Rohrseitz N, Straw AD, Dickinson MH. 2008. TrackFly: Virtual reality for a behavioral system analysis in free-flying fruit flies. J Neurosci Methods 171: 110-117.
37. Fry SN, Rohrseitz N, Straw AD, Dickinson MH. 2009. Visual control of flight speed in Drosophila melanogaster. J Exp Biol 212: 1120-1130.
38. Fu Y, Yau KW. 2007. Phototransduction in mouse rods and cones. Pflugers Arch 454: 805-819.
39. Galbadage T, Hartman PS. 2008. Repeated temperature fluctuation extends the life span of Caenorhabditis elegans in a daf-16-dependent fashion. Mech Ageing Dev 129: 507-514.
40. Gerisch B, Antebi A. 2004. Hormonal signals produced by DAF-9/ cytochrome P450 regulate C. elegans dauer diapause in response to environmental cues. Development 131: 1765-1776. (Pubitemid 38559844)
41. Gerisch B, Weitzel C, Kober-Eisermann C, Rottiers V, Antebi A. 2001. A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev Cell 1: 841-851.
42. Golden JW, Riddle DL. 1982. A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 218: 578-580.
43. Golden JW, Riddle DL. 1984a. A pheromone-induced developmental switch in Caenorhabditis elegans: Temperaturesensitive mutants reveal a wild-type temperature-dependent process. Proc Natl Acad Sci 81: 819-823.
44. Golden JW, Riddle DL. 1984b. The Caenorhabditis elegans dauer larva: Developmental effects of pheromone, food, and temperature. Dev Biol 102: 368-378.
45. 2+ signaling via the neuronal calcium sensor-1 regulates associative learning and memory in C. elegans. Neuron 30: 241-248.
46. Goodman MB, Schwarz EM. 2003. Transducing touch in Caenorhabditis elegans. Annu Rev Physiol 65: 429-452.
47. Gray JM, Hill JJ, Bargmann CI. 2005. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci 102: 3184-3191.
48. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA. 2008. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454: 217-220.
49. 2+ channel in Drosophila photoreceptors. Neuron 8: 643-651.
50. Hart A, Sims S, Kaplan J. 1995. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378: 82-85.
51. Harvey SC, Viney ME. 2007. Thermal variation reveals natural variation between isolates of Caenorhabditis elegans. J Exp Zoolog B Mol Dev Evol 308: 409-416.
52. Hastings JW, Sweeney BM. 1957. On the mechanism of temperature independence in a biological clock. Proc Natl Acad Sci 43: 804-811.
53. Hedgecock EM, Russell RL. 1975. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci 72: 4061-4065.
54. Heinrich B. 1993. The hot-blooded insects: Strategies and mechanisms of thermoregulation. Harvard University Press, Cambridge, MA.
55. Hensel H. 1973. Neural processes in thermoregulation. Physiol Rev 53: 948-1017.
56. Hobert O, Mori I, Yamashita Y, Honda H, Ohshima Y, Liu Y, Ruvkun G. 1997. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19: 345-357.
57. Hoffmann AA. 2010. Physiological climatic limits in Drosophila: Patterns and implications. J Exp Biol 213: 870-880.
58. Hong ST, Bang S, Paik D, Kang J, Hwang S, Jeon K, Chun B, Hyun S, Lee Y, Kim J. 2006. Histamine and its receptors modulate temperature-preference behaviors in Drosophila. J Neurosci 26: 7245-7256.
59. Hong ST, Bang S, Hyun S, Kang J, Jeong K, PaikD, Chung J, Kim J. 2008. cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila. Nature 454: 771-775.
60. Hosono R, Mitsui Y, Sato Y, Aizawa S, Miwa J. 1982. Life span of the wild and mutant nematode Caenorhabditis elegans. Effects of sex, sterilization, and temperature. Exp Gerontol 17: 163-172.
61. Huey RB, Hertz PE, Sinervo B. 2003. Behavioral drive versus behavioral inertia in evolution: A null model approach. Am Nat 161: 357-366.
62. Iino Y, Yoshida K. 2009. Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans. J Neurosci 29: 5370-5380.
63. Inada H, Ito H, Satterlee J, Sengupta P, Matsumoto K, Mori I. 2006. Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans. Genetics 172: 2239-2252.
64. Ito H, Inada H, Mori I. 2006. Quantitative analysis of thermotaxis in the nematode Caenorhabditis elegans. J Neurosci Methods 154: 45-52.
65. Jeong PY, Jung M, Yim YH, Kim H, Park M, Hong E, Lee W, Kim YH, Kim K, Paik YK. 2005. Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 433: 541-545. (Pubitemid 40204313)
66. Jia K, Albert PS, Riddle DL. 2002. DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longevity. Development 129: 221-231. (Pubitemid 34863790)
67. Jurado P, Kodama E, Tanizawa Y, Mori I. 2010. Distinct thermal migration behaviors in response to different thermal gradients in Caenorhabditis elegans. Genes Brain Behav 9: 120-127.
68. Kang K, Pulver SR, Panzano VC, Chang EC, Griffith LC, Theobald DL, Garrity PA. 2010. Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464: 597-600.
69. Katsov AY, Clandinin TR. 2008. Motion processing streams in Drosophila are behaviorally specialized. Neuron 59: 322-335.
70. Kimura KD, Miyawaki A, Matsumoto K, Mori I. 2004. The C. elegans thermosensory neuron AFD responds to warming. Curr Biol 14: 1291-1295. (Pubitemid 38991818)
71. Klass MR. 1977. Aging in the nematode Caenorhabditis elegans: Major biological and environmental factors influencing life span. Mech Ageing Dev 6: 413-429.
72. Kodama E, Kuhara A, Mohri-Shiomi A, Kimura KD, Okumura M, Tomioka M, Iino Y, Mori I. 2006. Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. Genes Dev 20: 2955-2960.
73. Komatsu H, Mori I, Ohshima Y. 1996. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17: 707-718.
74. Komatsu H, Jin YH, L'Etoile N, Mori I, Bargmann CI, Akaike N, Ohshima Y. 1999. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res 821: 160-168.
75. Krochmal AR, Bakken GS. 2003. Thermoregulation is the pits: Use of thermal radiation for retreat site selection by rattlesnakes. J Exp Biol 206: 2539-2545.
76. Krstevska B, Hoffmann AA. 1994. The effects of acclimation and rearing conditions on the response of tropical and temperate populations of Drosophila melanogaster and D. simulans to a temperature gradient (Diptera: Drosophilidae). J Insect Behav 7: 279-288. (Pubitemid 2098176)
77. Kuhara A, Mori I. 2006. Molecular physiology of the neural circuit for calcineurin-dependent associative learning in Caenorhabditis elegans. J Neurosci 26: 9355-9364.
78. Kuhara A, Inada H, Katsura I, Mori I. 2002. Negative regulation and gain control of sensory neurons by the C. elegans calcineurin TAX-6. Neuron 33: 751-763.
79. Kuhara A, Okumura M, Kimata T, Tanizawa Y, Takano R, Kimura KD, Inada H, Matsumoto K, Mori I. 2008. Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science 320: 803-807.
80. Kwon Y, Shim HS, Wang X, Montell C. 2008. Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nat Neurosci 11: 871-873.
81. 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.
82. Lee SJ, Kenyon C. 2009. Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans. Curr Biol 19: 715-722.
83. Lee RY, Sawin ER, Chalfie M, Horvitz HR, Avery L. 1999. EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans. J Neurosci 19: 159-167.
84. Lee Y, Lee Y, Lee J, Bang S, Hyun S, Kang J, Hong ST, Bae E, Kaang BK, Kim J. 2005. Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nat Genet 37: 305-310.
85. Leon LR. 2005. The use of gene knockout mice in thermoregulation studies. J Therm Biol 30: 273-288.
86. Li C, Nelson LS, Kim K, Nathoo A, Hart AC. 1999. Neuropeptide gene families in the nematode Caenorhabditis elegans. Ann N Y Acad Sci 897: 239-252.
87. Liu L, Yermolaieva O, Johnson WA, Abboud FM, Welsh MJ. 2003. Identification and function of thermosensory neurons in Drosophila larvae. Nat Neurosci 6: 267-273.
88. Liu J, Ward A, Gao J, Dong Y, Nishio N, Inada H, Kang L, Yu Y, Ma D, Xu T, et al. 2010. C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nat Neurosci 13: 715-722.
89. Louis M, Huber T, Benton R, Sakmar TP, Vosshall LB. 2008. Bilateral olfactory sensory input enhances chemotaxis behavior. Nat Neurosci 11: 187-199.
90. Luo L, Clark DA, Biron D, Mahadevan L, Samuel AD. 2006. Sensorimotor control during isothermal tracking in Caenorhabditis elegans. J Exp Biol 209: 4652-4662.
91. Luo L, Gabel CV, Ha HI, Zhang Y, Samuel AD. 2008. Olfactory behavior of swimming C. elegans analyzed by measuring motile responses to temporal variations of odorants. J Neurophysiol 99: 2617-2625.
92. Luo L, Gershow M, Rosenzweig M, Kang K, Fang-Yen C, Garrity PA, Samuel AD. 2010. Navigational decision making in Drosophila thermotaxis. J Neurosci 30: 4261-4272.
93. Mak HY, Ruvkun G. 2004. Intercellular signaling of reproductive development by the C. elegans DAF-9 cytochrome P450. Development 131: 1777-1786.
94. Maricq AV, Peckol E, Bargmann CI. 1995. Mechanosensory signalling in C.elegans mediated by the GLR-1 glutamate receptor. Nature 378: 78-81.
95. McKay RR, Chen DM, Miller K, Kim S, Stark WS, Shortridge RD. 1995. Phospholipase C rescues visual defect in norpA mutant of Drosophila melanogaster. J Biol Chem 270: 13271-13276.
96. Mohri A, Kodama E, Kimura KD, Koike M, Mizuno T, Mori I. 2005. Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics 169: 1437-1450.
97. Mori I. 1999. Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu Rev Genet 33: 399-422.
98. Mori I, Ohshima Y. 1995. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376: 344-348.
99. Motola DL, Cummins CL, Rottiers V, Sharma KK, Li T, Li Y, Suino-Powell K, Xu HE, Auchus RJ, Antebi A, et al. 2006. Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124: 1209-1223.
100. Murakami H, Bessinger K, Hellmann J, Murakami S. 2005. Aging-dependent and -independent modulation of associative learning behavior by insulin/insulin-like growth factor-1 signal in Caenorhabditis elegans. J Neurosci 25: 10894-10904.
101. Nakazato K, Mochizuki A. 2009. Steepness of thermal gradient is essential to obtain a unified view of thermotaxis in C. elegans. J Theor Biol 260: 56-65.
102. Nathoo AN, Moeller RA, Westlund BA, Hart AC. 2001. Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. Proc Natl Acad Sci 98: 14000-14005.
103. Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS. 1996. The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell 85: 651-659.
104. Noroozi M, Azmi BZ, Wahab ZA, Moksin MM, Mamat MH. 2009. Thermal diffusivity determination of liquid through thermal diffusion length measurement. Solid State Sci Technol 17: 44-49.
105. Okochi Y, Kimura KD, Ohta A, Mori I. 2005. Diverse regulation of sensory signaling by C. elegans nPKC-ε/η TTX-4. EMBO J 24: 2127-2137.
106. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG. 1986. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117: 456-487.
107. Pierce-Shimomura JT, Morse TM, Lockery SR. 1999. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci 19: 9557-9569.
108. Pittendrigh CS. 1954. On temperature independence in the clock system controlling emergence time in Drosophila. Proc Natl Acad Sci 40: 1018-1029.
109. Prahlad V, Cornelius T, Morimoto RI. 2008. Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320: 811-814.
110. Pungaliya C, Srinivasan J, Fox BW, Malik RU, Ludewig AH, Sternberg PW, Schroeder FC. 2009. A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditis elegans. Proc Natl Acad Sci 106: 7708-7713.
111. Ramot D, MacInnis BL, Goodman MB. 2008a. Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat Neurosci 11: 908-915.
112. Ramot D, MacInnis BL, Lee HC, Goodman MB. 2008b. Thermotaxis is a robust mechanism for thermoregulation in Caenorhabditis elegans nematodes. J Neurosci 28: 12546-12557.
113. Rosenzweig M, Brennan KM, Tayler TD, Phelps PO, Patapoutian A, Garrity PA. 2005. The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19: 419-424.
114. Rosenzweig M, Kang K, Garrity PA. 2008. Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proc Natl Acad Sci 105: 14668-14673.
115. Ryu WS, Samuel AD. 2002. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined thermal stimuli. J Neurosci 22: 5727-5733.
116. Sarin S, Prabhu S, O'Meara MM, Pe'er I, Hobert O. 2008. Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nat Methods 5: 865-867.
117. Satterlee JS, Sasakura H, Kuhara A, Berkeley M, Mori I, Sengupta P. 2001. Specification of thermosensory neuron fate in C. elegans requires ttx-1, a homolog of otd/Otx. Neuron 31: 943-956.
118. Sayeed O, Benzer S. 1996. Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc Natl Acad Sci 93: 6079-6084.
119. Sehadova H, Glaser FT, Gentile C, Simoni A, Giesecke A, Albert JT, Stanewsky R. 2009. Temperature entrainment of Drosophila's circadian clock involves the gene nocte and signaling from peripheral sensory tissues to the brain. Neuron 64: 251-266.
120. Shaw RF, Bercaw BL. 1962. Temperature and life-span in poikilothermous animals. Nature 196: 454-457.
121. Shen Y, Sarin S, Liu Y, Hobert O, Pe'er I. 2008. Comparing platforms for C. elegans mutant identification using highthroughput whole-genome sequencing. PLoS ONE 3: e4012. doi: 10.1371/journal.pone.0004012.
122. Siddiqui WH, Barlow CA. 1972. Population growth of Drosophila melanogaster (Diptera: Drosophilidae) at constant and alternating temperatures. Ann Entomol Soc Am 65: 993-1001.
123. Simon E, Pierau FK, Taylor DC. 1986. Central and peripheral thermal control of effectors in homeothermic temperature regulation. Physiol Rev 66: 235-300.
124. 2+-requiring channel activated by noxious heat. J Neurosci 28: 9929-9938.
125. Stephens GJ, Johnson-Kerner B, Bialek W, Ryu WS. 2008. Dimensionality and dynamics in the behavior of C. elegans. PLoS Comput Biol 4: e1000028. doi: 10.1371/journal.pcbi. 1000028.
126. Stevenson RD. 1985. The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am Nat 126: 362-386.
127. Sun Y, Liu L, Ben-Shahar Y, Jacobs JS, Eberl DF, Welsh MJ. 2009. TRPA channels distinguish gravity sensing from hearing in Johnston's organ. Proc Natl Acad Sci 106: 13606-13611.
128. Thomsen E, Thomsen M. 1937. Uber das thermopraferendum der larven einiger fliegenarten. Z Vgl Physiol 24: 343-380.
129. Tissenbaum HA, Hawdon J, Perregaux M, Hotez P, Guarente L, Ruvkun G. 2000. A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. Proc Natl Acad Sci 97: 460-465.
130. Tominaga M, Caterina MJ. 2004. Thermosensation and pain. J Neurobiol 61: 3-12.
131. Tracey WD Jr, Wilson RI, Laurent G, Benzer S. 2003. painless, a Drosophila gene essential for nociception. Cell 113: 261-273.
132. Tsalik EL, Hobert O. 2003. Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. J Neurobiol 56: 178-197.
133. Vermeulen CJ, Bijlsma R. 2004. Changes in mortality patterns and temperature dependence of lifespan in Drosophila melanogaster caused by inbreeding. Heredity 92: 275-281.
134. Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang SW, Patapoutian A, Jegla T. 2003. Opposite thermosensor in fruitfly and mouse. Nature 423: 822-823.
135. Wakabayashi T, Kitagawa I, Shingai R. 2004. Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. Neurosci Res 50: 103-111.
136. Ward A, Liu J, Feng Z, Xu XZ. 2008. Light-sensitive neurons and channels mediate phototaxis in C. elegans. Nat Neurosci 11: 916-922.
137. Wenick AS, Hobert O. 2004. Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. Dev Cell 6: 757-770.
138. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B 314: 1-340.
139. Xu SY, Cang CL, Liu XF, Peng YQ, Ye YZ, Zhao ZQ, Guo AK. 2006. Thermal nociception in adult Drosophila: Behavioral characterization and the role of the painless gene. Genes Brain Behav 5: 602-613.
140. Xu J, Sornborger AT, Lee JK, Shen P. 2008. Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response. Nat Neurosci 11: 676-682.
141. Yamada Y, Ohshima Y. 2003. Distribution and movement of Caenorhabditis elegans on a thermal gradient. J Exp Biol 206: 2581-2593.
142. Yau KW, Hardie RC. 2009. Phototransduction motifs and variations. Cell 139: 246-264.
143. Zariwala HA, Miller AC, Faumont S, Lockery SR. 2003. Step response analysis of thermotaxis in Caenorhabditis elegans. J Neurosci 23: 4369-4377.
144. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, Watzke N, Wood PG, Bamberg E, Nagel G, Gottschalk A, et al. 2007. Multimodal fast optical interrogation of neural circuitry. Nature 446: 633-639.