1932

Abstract

Temperature is a universal cue and regulates many essential processes ranging from enzymatic reactions to species migration. Due to the profound impact of temperature on physiology and behavior, animals and humans have evolved sophisticated mechanisms to detect temperature changes. Studies from animal models, such as mouse, , and , have revealed many exciting principles of thermosensation. For example, conserved molecular thermosensors, including thermosensitive channels and receptors, act as the initial detectors of temperature changes across taxa. Additionally, thermosensory neurons and circuits in different species appear to adopt similar logic to transduce and process temperature information. Here, we present the current understanding of thermosensation at the molecular and cellular levels. We also discuss the fundamental coding strategies of thermosensation at the circuit level. A thorough understanding of thermosensation not only provides key insights into sensory biology but also builds a foundation for developing better treatments for various sensory disorders.

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2021-02-10
2024-04-21
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Literature Cited

  1. 1. 
    Frazer JG. 1930. Myths of the Origin of Fire—An Essay London: Macmillan & Co.
  2. 2. 
    Hall JE. 2016. Guyton and Hall Textbook of Medical Physiology Philadelphia: Elsevier
  3. 3. 
    Kandel ER. 2013. Principles of Neural Science New York/London: McGraw-Hill Med.
  4. 4. 
    Gowers WR. 1888. A Manual of Diseases of the Nervous System Philadelphia: Blakiston
  5. 5. 
    Brown-Séquard E. 1858. Dr. E. Brown-Séquard on the physiology and pathology of the nervous system. J. Psychol. Med. Ment. Pathol. 11:i–xvi
    [Google Scholar]
  6. 6. 
    Adrian EDA. 1928. The Basis of Sensation, the Action of the Sense Organs New York: W.W. Norton
  7. 7. 
    Iggo A. 1959. Cutaneous heat and cold receptors with slowly conducting (C) afferent fibres. Q. J. Exp. Physiol. Cogn. Med. Sci. 44:362–70
    [Google Scholar]
  8. 8. 
    Darian-Smith I, Johnson KO, Dykes R 1973. “Cold” fiber population innervating palmar and digital skin of the monkey: responses to cooling pulses. J. Neurophysiol. 36:325–46
    [Google Scholar]
  9. 9. 
    Hensel H, Boman KK. 1960. Afferent impulses in cutaneous sensory nerves in human subjects. J. Neurophysiol. 23:564–78
    [Google Scholar]
  10. 10. 
    Brown AG, Iggo A. 1967. A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit. J. Physiol. 193:707–33
    [Google Scholar]
  11. 11. 
    Dhaka A, Viswanath V, Patapoutian A 2006. Trp ion channels and temperature sensation. Annu. Rev. Neurosci. 29:135–61
    [Google Scholar]
  12. 12. 
    Vriens J, Nilius B, Voets T 2014. Peripheral thermosensation in mammals. Nat. Rev. Neurosci. 15:573–89
    [Google Scholar]
  13. 13. 
    Morrison SF, Nakamura K. 2019. Central mechanisms for thermoregulation. Annu. Rev. Physiol. 81:285–308
    [Google Scholar]
  14. 14. 
    Garrity PA, Goodman MB, Samuel AD, Sengupta P 2010. Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila. . Genes Dev 24:2365–82
    [Google Scholar]
  15. 15. 
    Xiao R, Zhang B, Dong Y, Gong J, Xu T et al. 2013. A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152:806–17
    [Google Scholar]
  16. 16. 
    Zhang B, Xiao R, Ronan EA, He Y, Hsu A-L et al. 2015. Environmental temperature differentially modulates C. elegans longevity through a thermosensitive TRP channel. Cell Rep 11:1414–24
    [Google Scholar]
  17. 17. 
    Xiao R, Liu J, Xu XZS 2015. Thermosensation and longevity. J. Comp. Physiol. A 201:857–67
    [Google Scholar]
  18. 18. 
    Conti B. 2008. Considerations on temperature, longevity and aging. Cell. Mol. Life Sci. 65:1626–30
    [Google Scholar]
  19. 19. 
    Clapham DE, Miller C. 2011. A thermodynamic framework for understanding temperature sensing by transient receptor potential (TRP) channels. PNAS 108:19492–97
    [Google Scholar]
  20. 20. 
    Hille B. 2001. Ion Channels of Excitable Membranes Sunderland, MA: Sinauer
  21. 21. 
    Montell C, Rubin GM. 1989. Molecular characterization of the Drosophila TRP locus: a putative integral membrane protein required for phototransduction. Neuron 2:1313–23
    [Google Scholar]
  22. 22. 
    Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D 1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–24
    [Google Scholar]
  23. 23. 
    Venkatachalam K, Montell C. 2007. TRP channels. Annu. Rev. Biochem. 76:387–417
    [Google Scholar]
  24. 24. 
    Yarnitsky D, Sprecher E, Zaslansky R, Hemli JA 1995. Heat pain thresholds: normative data and repeatability. Pain 60:329–32
    [Google Scholar]
  25. 25. 
    Defrin R, Ohry A, Blumen N, Urca G 2002. Sensory determinants of thermal pain. Brain 125:501–10
    [Google Scholar]
  26. 26. 
    Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H et al. 1998. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21:531–43
    [Google Scholar]
  27. 27. 
    Julius D. 2013. TRP channels and pain. Annu. Rev. Cell Dev. Biol. 29:355–84
    [Google Scholar]
  28. 28. 
    Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J et al. 2000. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306–13
    [Google Scholar]
  29. 29. 
    Mishra SK, Hoon MA. 2010. Ablation of TrpV1 neurons reveals their selective role in thermal pain sensation. Mol. Cell. Neurosci. 43:157–63
    [Google Scholar]
  30. 30. 
    Mishra SK, Tisel SM, Orestes P, Bhangoo SK, Hoon MA 2011. TRPV1-lineage neurons are required for thermal sensation. EMBO J 30:582–93
    [Google Scholar]
  31. 31. 
    Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J et al. 2003. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–29
    [Google Scholar]
  32. 32. 
    Vriens J, Owsianik G, Hofmann T, Philipp SE, Stab J et al. 2011. TRPM3 is a nociceptor channel involved in the detection of noxious heat. Neuron 70:482–94
    [Google Scholar]
  33. 33. 
    Tan C-H, McNaughton PA. 2016. The TRPM2 ion channel is required for sensitivity to warmth. Nature 536:460–63
    [Google Scholar]
  34. 34. 
    Cho H, Yang YD, Lee J, Lee B, Kim T et al. 2012. The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat. Neurosci. 15:1015–21
    [Google Scholar]
  35. 35. 
    Vandewauw I, De Clercq K, Mulier M, Held K, Pinto S et al. 2018. A TRP channel trio mediates acute noxious heat sensing. Nature 555:662–66
    [Google Scholar]
  36. 36. 
    Tracey WD Jr., Wilson RI, Laurent G, Benzer S. 2003. painless, a Drosophila gene essential for nociception. Cell 113:261–73
    [Google Scholar]
  37. 37. 
    Sokabe T, Tsujiuchi S, Kadowaki T, Tominaga M 2008. Drosophila Painless is a Ca2+-requiring channel activated by noxious heat. J. Neurosci. 28:9929–38
    [Google Scholar]
  38. 38. 
    Xiao R, Xu XZ. 2009. Function and regulation of TRP family channels in C. elegans. . Pflügers Arch 458:851–60
    [Google Scholar]
  39. 39. 
    Chatzigeorgiou M, Schafer WR. 2011. Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans. . Neuron 70:299–309
    [Google Scholar]
  40. 40. 
    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
    [Google Scholar]
  41. 41. 
    Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ et al. 2002. A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046–49
    [Google Scholar]
  42. 42. 
    Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA et al. 2002. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418:181–86
    [Google Scholar]
  43. 43. 
    Smith GD, Gunthorpe MJ, Kelsell RE, Hayes PD, Reilly P et al. 2002. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418:186–90
    [Google Scholar]
  44. 44. 
    Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M 2002. Heat-evoked activation of the ion channel, TRPV4. J. Neurosci. 22:6408–14
    [Google Scholar]
  45. 45. 
    Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B 2002. Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J. Biol. Chem. 277:47044–51
    [Google Scholar]
  46. 46. 
    Huang SM, Li X, Yu Y, Wang J, Caterina MJ 2011. TRPV3 and TRPV4 ion channels are not major contributors to mouse heat sensation. Mol. Pain 7:37
    [Google Scholar]
  47. 47. 
    Yarmolinsky DA, Peng Y, Pogorzala LA, Rutlin M, Hoon MA, Zuker CS 2016. Coding and plasticity in the mammalian thermosensory system. Neuron 92:1079–92
    [Google Scholar]
  48. 48. 
    Togashi K, Hara Y, Tominaga T, Higashi T, Konishi Y et al. 2006. TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J 25:1804–15
    [Google Scholar]
  49. 49. 
    Song K, Wang H, Kamm GB, Pohle J, de Castro Reis F et al. 2016. The TRPM2 channel is a hypothalamic heat sensor that limits fever and can drive hypothermia. Science 353:1393–98
    [Google Scholar]
  50. 50. 
    Vilar B, Tan CH, McNaughton PA 2020. Heat detection by the TRPM2 ion channel. Nature 584:7820E5–12
    [Google Scholar]
  51. 51. 
    Mulier M, Vandewauw I, Vriens J, Voets T 2020. Reply to: Heat detection by the TRPM2 ion channel. Nature 584:7820E13–15
    [Google Scholar]
  52. 52. 
    Liu X, Wang H, Jiang Y, Zheng Q, Petrus M et al. 2019. STIM1 thermosensitivity defines the optimal preference temperature for warm sensation in mice. Cell Res 29:95–109
    [Google Scholar]
  53. 53. 
    Wang TA, Teo CF, Åkerblom M, Chen C, Tynan-La Fontaine M et al. 2019. Thermoregulation via temperature-dependent PGD2 production in mouse preoptic area. Neuron 103:309–22.e7
    [Google Scholar]
  54. 54. 
    Rosenzweig M, Brennan KM, Tayler TD, Phelps PO, Patapoutian A, Garrity PA 2005. The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19:419–24
    [Google Scholar]
  55. 55. 
    Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM et al. 2003. Opposite thermosensor in fruitfly and mouse. Nature 423:822–23
    [Google Scholar]
  56. 56. 
    Ni L, Bronk P, Chang EC, Lowell AM, Flam JO et al. 2013. A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila. . Nature 500:580–84
    [Google Scholar]
  57. 57. 
    Mishra A, Salari A, Berigan BR, Miguel KC, Amirshenava M et al. 2018. The Drosophila Gr28bD product is a non-specific cation channel that can be used as a novel thermogenetic tool. Sci. Rep. 8:901
    [Google Scholar]
  58. 58. 
    Shen WL, Kwon Y, Adegbola AA, Luo J, Chess A, Montell C 2011. Function of rhodopsin in temperature discrimination in Drosophila. . Science 331:1333–36
    [Google Scholar]
  59. 59. 
    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. 11:871–73
    [Google Scholar]
  60. 60. 
    Sokabe T, Chen HC, Luo J, Montell C 2016. A switch in thermal preference in Drosophila larvae depends on multiple rhodopsins. Cell Rep 17:336–44
    [Google Scholar]
  61. 61. 
    Goodman MB, Sengupta P. 2018. The extraordinary AFD thermosensor of C. elegans. . Pflügers Arch 470:839–49
    [Google Scholar]
  62. 62. 
    Takeishi A, Yu YV, Hapiak VM, Bell HW, O'Leary T, Sengupta P 2016. Receptor-type guanylyl cyclases confer thermosensory responses in C. elegans. . Neuron 90:235–44
    [Google Scholar]
  63. 63. 
    Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA et al. 2002. A TRP channel that senses cold stimuli and menthol. Cell 108:705–15
    [Google Scholar]
  64. 64. 
    McKemy DD, Neuhausser WM, Julius D 2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58
    [Google Scholar]
  65. 65. 
    Brauchi S, Orio P, Latorre R 2004. Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. PNAS 101:15494–99
    [Google Scholar]
  66. 66. 
    Dhaka A, Earley TJ, Watson J, Patapoutian A 2008. Visualizing cold spots: TRPM8-expressing sensory neurons and their projections. J. Neurosci. 28:566–75
    [Google Scholar]
  67. 67. 
    Takashima Y, Ma L, McKemy DD 2010. The development of peripheral cold neural circuits based on TRPM8 expression. Neuroscience 169:828–42
    [Google Scholar]
  68. 68. 
    Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI et al. 2007. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204–8
    [Google Scholar]
  69. 69. 
    Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A 2007. TRPM8 is required for cold sensation in mice. Neuron 54:371–78
    [Google Scholar]
  70. 70. 
    Knowlton WM, Palkar R, Lippoldt EK, McCoy DD, Baluch F et al. 2013. A sensory-labeled line for cold: TRPM8-expressing sensory neurons define the cellular basis for cold, cold pain, and cooling-mediated analgesia. J. Neurosci. 33:2837–48
    [Google Scholar]
  71. 71. 
    Pogorzala LA, Mishra SK, Hoon MA 2013. The cellular code for mammalian thermosensation. J. Neurosci. 33:5533–41
    [Google Scholar]
  72. 72. 
    Zimmermann K, Lennerz JK, Hein A, Link AS, Kaczmarek JS et al. 2011. Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. PNAS 108:18114–19
    [Google Scholar]
  73. 73. 
    Chao Y-C, Chen C-C, Lin Y-C, Breer H, Fleischer J, Yang R-B 2015. Receptor guanylyl cyclase-G is a novel thermosensory protein activated by cool temperatures. EMBO J 34:294–306
    [Google Scholar]
  74. 74. 
    Sayeed O, Benzer S. 1996. Behavioral genetics of thermosensation and hygrosensation in Drosophila. . PNAS 93:6079–84
    [Google Scholar]
  75. 75. 
    Gallio M, Ofstad TA, Macpherson LJ, Wang JW, Zuker CS 2011. The coding of temperature in the Drosophila brain. Cell 144:614–24
    [Google Scholar]
  76. 76. 
    Budelli G, Ni L, Berciu C, van Giesen L, Knecht ZA et al. 2019. Ionotropic receptors specify the morphogenesis of phasic sensors controlling rapid thermal preference in Drosophila. . Neuron 101:738–47.e3
    [Google Scholar]
  77. 77. 
    Ni L, Klein M, Svec KV, Budelli G, Chang EC et al. 2016. The ionotropic receptors IR21a and IR25a mediate cool sensing in Drosophila. . eLife 5:e13254
    [Google Scholar]
  78. 78. 
    Enjin A, Zaharieva EE, Frank DD, Mansourian S, Suh GS et al. 2016. Humidity sensing in Drosophila. Curr. Biol 26:1352–58
    [Google Scholar]
  79. 79. 
    Knecht ZA, Silbering AF, Ni L, Klein M, Budelli G et al. 2016. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. . eLife 5:e17879
    [Google Scholar]
  80. 80. 
    Chatzigeorgiou M, Yoo S, Watson JD, Lee WH, Spencer WC et al. 2010. Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat. Neurosci. 13:861–68
    [Google Scholar]
  81. 81. 
    Kindt KS, Viswanath V, Macpherson L, Quast K, Hu H et al. 2007. Caenorhabditis elegans TRPA-1 functions in mechanosensation. Nat. Neurosci. 10:568–77
    [Google Scholar]
  82. 82. 
    Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang D-S et al. 2006. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277–89
    [Google Scholar]
  83. 83. 
    Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ et al. 2006. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269–82
    [Google Scholar]
  84. 84. 
    Moparthi L, Kichko TI, Eberhardt M, Hogestatt ED, Kjellbom P et al. 2016. Human TRPA1 is a heat sensor displaying intrinsic U-shaped thermosensitivity. Sci. Rep. 6:28763
    [Google Scholar]
  85. 85. 
    del Camino D, Murphy S, Heiry M, Barrett LB, Earley TJ et al. 2010. TRPA1 contributes to cold hypersensitivity. J. Neurosci. 30:15165–74
    [Google Scholar]
  86. 86. 
    Gong J, Liu J, Ronan EA, He F, Cai W et al. 2019. A cold-sensing receptor encoded by a glutamate receptor gene. Cell 178:1375–86.e11
    [Google Scholar]
  87. 87. 
    Rodriguez-Moreno A, Lerma J. 1998. Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 20:1211–18
    [Google Scholar]
  88. 88. 
    Kang D, Choe C, Kim D 2005. Thermosensitivity of the two-pore domain K+ channels TREK-2 and TRAAK. J. Physiol. 564:103–16
    [Google Scholar]
  89. 89. 
    Noel J, Zimmermann K, Busserolles J, Deval E, Alloui A et al. 2009. The mechano-activated K+ channels TRAAK and TREK-1 control both warm and cold perception. EMBO J 28:1308–18
    [Google Scholar]
  90. 90. 
    Zimmermann K, Leffler A, Babes A, Cendan CM, Carr RW et al. 2007. Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 447:855–58
    [Google Scholar]
  91. 91. 
    Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B 2004. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748–54
    [Google Scholar]
  92. 92. 
    Matta JA, Ahern GP. 2007. Voltage is a partial activator of rat thermosensitive TRP channels. J. Physiol. 585:469–82
    [Google Scholar]
  93. 93. 
    Makhatadze GI, Privalov PL. 1990. Heat capacity of proteins. I. Partial molar heat capacity of individual amino acid residues in aqueous solution: hydration effect. J. Mol. Biol. 213:375–84
    [Google Scholar]
  94. 94. 
    Chowdhury S, Jarecki BW, Chanda B 2014. A molecular framework for temperature-dependent gating of ion channels. Cell 158:1148–58
    [Google Scholar]
  95. 95. 
    Yao J, Liu B, Qin F 2011. Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. PNAS 108:11109–14
    [Google Scholar]
  96. 96. 
    Cui Y, Yang F, Cao X, Yarov-Yarovoy V, Wang K, Zheng J 2012. Selective disruption of high sensitivity heat activation but not capsaicin activation of TRPV1 channels by pore turret mutations. J. Gen. Physiol. 139:273–83
    [Google Scholar]
  97. 97. 
    Grandl J, Kim SE, Uzzell V, Bursulaya B, Petrus M et al. 2010. Temperature-induced opening of TRPV1 ion channel is stabilized by the pore domain. Nat. Neurosci. 13:708–14
    [Google Scholar]
  98. 98. 
    Grandl J, Hu H, Bandell M, Bursulaya B, Schmidt M et al. 2008. Pore region of TRPV3 ion channel is specifically required for heat activation. Nat. Neurosci. 11:1007–13
    [Google Scholar]
  99. 99. 
    Pertusa M, Rivera B, Gonzalez A, Ugarte G, Madrid R 2018. Critical role of the pore domain in the cold response of TRPM8 channels identified by ortholog functional comparison. J. Biol. Chem. 293:12454–71
    [Google Scholar]
  100. 100. 
    Brauchi S, Orta G, Mascayano C, Salazar M, Raddatz N et al. 2007. Dissection of the components for PIP2 activation and thermosensation in TRP channels. PNAS 104:10246–51
    [Google Scholar]
  101. 101. 
    Brauchi S, Orta G, Salazar M, Rosenmann E, Latorre R 2006. A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J. Neurosci. 26:4835–40
    [Google Scholar]
  102. 102. 
    Arrigoni C, Rohaim A, Shaya D, Findeisen F, Stein RA et al. 2016. Unfolding of a temperature-sensitive domain controls voltage-gated channel activation. Cell 164:922–36
    [Google Scholar]
  103. 103. 
    Paulsen CE, Armache JP, Gao Y, Cheng Y, Julius D 2015. Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature 520:511–17
    [Google Scholar]
  104. 104. 
    Tsuruda PR, Julius D, Minor DL Jr 2006. Coiled coils direct assembly of a cold-activated TRP channel. Neuron 51:201–12
    [Google Scholar]
  105. 105. 
    Kang K, Panzano VC, Chang EC, Ni L, Dainis AM et al. 2011. Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. . Nature 481:76–80
    [Google Scholar]
  106. 106. 
    Numazaki M, Tominaga T, Toyooka H, Tominaga M 2002. Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cε and identification of two target serine residues. J. Biol. Chem. 277:13375–78
    [Google Scholar]
  107. 107. 
    Cao E, Cordero-Morales JF, Liu B, Qin F, Julius D 2013. TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids. Neuron 77:667–79
    [Google Scholar]
  108. 108. 
    Luo J, Shen WL, Montell C 2017. TRPA1 mediates sensation of the rate of temperature change in Drosophila larvae. Nat. Neurosci. 20:34–41
    [Google Scholar]
  109. 109. 
    Bessou P, Perl ER. 1969. Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J. Neurophysiol. 32:1025–43
    [Google Scholar]
  110. 110. 
    Kenton B, Coger R, Crue B, Pinsky J, Friedman Y, Carmon A 1980. Peripheral fiber correlates to noxious thermal stimulation in humans. Neurosci. Lett. 17:301–6
    [Google Scholar]
  111. 111. 
    Konietzny F. 1984. Peripheral neural correlates of temperature sensations in man. Hum. Neurobiol. 3:21–32
    [Google Scholar]
  112. 112. 
    Kenshalo DR, Duclaux R. 1977. Response characteristics of cutaneous cold receptors in the monkey. J. Neurophysiol. 40:319–32
    [Google Scholar]
  113. 113. 
    Darian-Smith I, Johnson KO, LaMotte C, Shigenaga Y, Kenins P, Champness P 1979. Warm fibers innervating palmar and digital skin of the monkey: responses to thermal stimuli. J. Neurophysiol. 42:1297–315
    [Google Scholar]
  114. 114. 
    Simone DA, Kajander KC. 1997. Responses of cutaneous A-fiber nociceptors to noxious cold. J. Neurophysiol. 77:2049–60
    [Google Scholar]
  115. 115. 
    Campero M, Serra J, Ochoa JL 1996. C-polymodal nociceptors activated by noxious low temperature in human skin. J. Physiol. 497:Part 2565–72
    [Google Scholar]
  116. 116. 
    Price DD, Hu JW, Dubner R, Gracely RH 1977. Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses. Pain 3:57–68
    [Google Scholar]
  117. 117. 
    Wang F, Belanger E, Cote SL, Desrosiers P, Prescott SA et al. 2018. Sensory afferents use different coding strategies for heat and cold. Cell Rep 23:2001–13
    [Google Scholar]
  118. 118. 
    Zhang ET, Han ZS, Craig AD 1996. Morphological classes of spinothalamic lamina I neurons in the cat. J. Comp. Neurol. 367:537–49
    [Google Scholar]
  119. 119. 
    Han ZS, Zhang ET, Craig AD 1998. Nociceptive and thermoreceptive lamina I neurons are anatomically distinct. Nat. Neurosci. 1:218–25
    [Google Scholar]
  120. 120. 
    Todd AJ. 2010. Neuronal circuitry for pain processing in the dorsal horn. Nat. Rev. Neurosci. 11:823–36
    [Google Scholar]
  121. 121. 
    Zheng J, Lu Y, Perl ER 2010. Inhibitory neurones of the spinal substantia gelatinosa mediate interaction of signals from primary afferents. J. Physiol. 588:2065–75
    [Google Scholar]
  122. 122. 
    McCoy ES, Taylor-Blake B, Street SE, Pribisko AL, Zheng J, Zylka MJ 2013. Peptidergic CGRPα primary sensory neurons encode heat and itch and tonically suppress sensitivity to cold. Neuron 78:1138–51
    [Google Scholar]
  123. 123. 
    Ran C, Hoon MA, Chen X 2016. The coding of cutaneous temperature in the spinal cord. Nat. Neurosci. 19:1201–9
    [Google Scholar]
  124. 124. 
    Craig AD, Chen K, Bandy D, Reiman EM 2000. Thermosensory activation of insular cortex. Nat. Neurosci. 3:184–90
    [Google Scholar]
  125. 125. 
    Gauriau C, Bernard J-F. 2004. A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: the forebrain. J. Comp. Neurol. 468:24–56
    [Google Scholar]
  126. 126. 
    Craig AD, Bushnell MC, Zhang ET, Blomqvist A 1994. A thalamic nucleus specific for pain and temperature sensation. Nature 372:770–73
    [Google Scholar]
  127. 127. 
    Bokiniec P, Zampieri N, Lewin GR, Poulet JF 2018. The neural circuits of thermal perception. Curr. Opin. Neurobiol. 52:98–106
    [Google Scholar]
  128. 128. 
    Klein M, Afonso B, Vonner AJ, Hernandez-Nunez L, Berck M et al. 2015. Sensory determinants of behavioral dynamics in Drosophila thermotaxis. PNAS 112:E220–29
    [Google Scholar]
  129. 129. 
    Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A et al. 2008. An internal thermal sensor controlling temperature preference in Drosophila. . Nature 454:217–20
    [Google Scholar]
  130. 130. 
    Barbagallo B, Garrity PA. 2015. Temperature sensation in Drosophila. Curr. Opin. Neurobiol 34:8–13
    [Google Scholar]
  131. 131. 
    Liu WW, Mazor O, Wilson RI 2015. Thermosensory processing in the Drosophila brain. Nature 519:353–57
    [Google Scholar]
  132. 132. 
    Frank DD, Jouandet GC, Kearney PJ, Macpherson LJ, Gallio M 2015. Temperature representation in the Drosophila brain. Nature 519:358–61
    [Google Scholar]
  133. 133. 
    Hedgecock EM, Russell RL. 1975. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. . PNAS 72:4061–65
    [Google Scholar]
  134. 134. 
    Mori I, Ohshima Y. 1995. Neural regulation of thermotaxis in Caenorhabditis elegans. . Nature 376:344–48
    [Google Scholar]
  135. 135. 
    Luo L, Cook N, Venkatachalam V, Martinez-Velazquez LA, Zhang X et al. 2014. Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. PNAS 111:2776–81
    [Google Scholar]
  136. 136. 
    Cook SJ, Jarrell TA, Brittin CA, Wang Y, Bloniarz AE et al. 2019. Whole-animal connectomes of both Caenorhabditis elegans sexes. Nature 571:63–71
    [Google Scholar]
  137. 137. 
    White JG, Southgate E, Thomson JN, Brenner S 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. B 314:1–340
    [Google Scholar]
  138. 138. 
    Ohnishi N, Kuhara A, Nakamura F, Okochi Y, Mori I 2011. Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans. . EMBO J 30:1376–88
    [Google Scholar]
  139. 139. 
    Li C, Kim K. 2008. Neuropeptides. WormBook 2008:1–36
    [Google Scholar]
  140. 140. 
    Narayan A, Laurent G, Sternberg PW 2011. Transfer characteristics of a thermosensory synapse in Caenorhabditis elegans. . PNAS 108:9667–72
    [Google Scholar]
  141. 141. 
    Ikeda M, Nakano S, Giles AC, Xu L, Costa WS et al. 2020. Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans. . PNAS 117:6178–88
    [Google Scholar]
  142. 142. 
    Kimura KD, Miyawaki A, Matsumoto K, Mori I 2004. The C. elegans thermosensory neuron AFD responds to warming. Curr. Biol. 14:1291–95
    [Google Scholar]
  143. 143. 
    Clark DA, Biron D, Sengupta P, Samuel AD 2006. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. J. Neurosci 26:7444–51
    [Google Scholar]
  144. 144. 
    Kobayashi K, Nakano S, Amano M, Tsuboi D, Nishioka T et al. 2016. Single-cell memory regulates a neural circuit for sensory behavior. Cell Rep 14:11–21
    [Google Scholar]
  145. 145. 
    Hawk JD, Calvo AC, Liu P, Almoril-Porras A, Aljobeh A et al. 2018. Integration of plasticity mechanisms within a single sensory neuron of C. elegans actuates a memory. Neuron 97:356–67.e4
    [Google Scholar]
  146. 146. 
    Chi CA, Clark DA, Lee S, Biron D, Luo L et al. 2007. Temperature and food mediate long-term thermotactic behavioral plasticity by association-independent mechanisms in C. elegans. J. Exp. Biol 210:4043–52
    [Google Scholar]
  147. 147. 
    Ramot D, MacInnis BL, Goodman MB 2008. Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat. Neurosci 11:908–15
    [Google Scholar]
  148. 148. 
    Zhang B, Gong J, Zhang W, Xiao R, Liu J, Xu XZS 2018. Brain-gut communications via distinct neuroendocrine signals bidirectionally regulate longevity in C. elegans. . Genes Dev 32:258–70
    [Google Scholar]
  149. 149. 
    Li W, Kang L, Piggott BJ, Feng Z, Xu XZ 2011. The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat. Commun 2:315
    [Google Scholar]
  150. 150. 
    Husson SJ, Costa WS, Wabnig S, Stirman JN, Watson JD et al. 2012. Optogenetic analysis of a nociceptor neuron and network reveals ion channels acting downstream of primary sensors. Curr. Biol. 22:743–52
    [Google Scholar]
  151. 151. 
    Davis KD, Pope GE. 2002. Noxious cold evokes multiple sensations with distinct time courses. Pain 98:179–85
    [Google Scholar]
  152. 152. 
    Knowlton WM, Palkar R, Lippoldt EK, McCoy DD, Baluch F et al. 2013. A sensory-labeled line for cold: TRPM8-expressing sensory neurons define the cellular basis for cold, cold pain, and cooling-mediated analgesia. J. Neurosci. 33:2837–48
    [Google Scholar]
  153. 153. 
    Ma Q. 2010. Labeled lines meet and talk: population coding of somatic sensations. J. Clin. Investig. 120:3773–78
    [Google Scholar]
  154. 154. 
    Uchida N, Poo C, Haddad R 2014. Coding and transformations in the olfactory system. Annu. Rev. Neurosci. 37:363–85
    [Google Scholar]
  155. 155. 
    Craig AD, Bushnell MC. 1994. The thermal grill illusion: unmasking the burn of cold pain. Science 265:252–55
    [Google Scholar]
  156. 156. 
    Paricio-Montesinos R, Schwaller F, Udhayachandran A, Rau F, Walcher J et al. 2020. The sensory coding of warm perception. Neuron 106:830–41.e3
    [Google Scholar]
  157. 157. 
    Elliot SL, Blanford S, Thomas MB 2002. Host-pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proc. Biol. Sci. 269:1599–607
    [Google Scholar]
  158. 158. 
    Corfas RA, Vosshall LB. 2015. The cation channel TRPA1 tunes mosquito thermotaxis to host temperatures. eLife 4:e11750
    [Google Scholar]
  159. 159. 
    Greppi C, Laursen WJ, Budelli G, Chang EC, Daniels AM et al. 2020. Mosquito heat seeking is driven by an ancestral cooling receptor. Science 367:681–84
    [Google Scholar]
  160. 160. 
    Liu B, Hui K, Qin F 2003. Thermodynamics of heat activation of single capsaicin ion channels VR1. Biophys. J. 85:2988–3006
    [Google Scholar]
  161. 161. 
    Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY et al. 2009. TRPA1 acts as a cold sensor in vitro and in vivo. PNAS 106:1273–78
    [Google Scholar]
  162. 162. 
    Park U, Vastani N, Guan Y, Raja SN, Koltzenburg M, Caterina MJ 2011. TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception. J. Neurosci. 31:11425–36
    [Google Scholar]
  163. 163. 
    Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N et al. 2005. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:1022–25
    [Google Scholar]
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