Labeled lines meet and talk: Population coding of somatic sensations

Journal of Clinical Investigation

Volumn 120, Issue 11, 2010, Pages 3773-3778

  Ma, Qiufu ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CAPSAICIN; PURINERGIC P2X RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2Y RECEPTOR; PURINERGIC P2Y2 RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; URIDINE TRIPHOSPHATE; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 3;

CELL COMMUNICATION; CELL STIMULATION; COLD SENSATION; HEAT SENSATION; HUMAN; HYPOTHESIS; MYELINATED NERVE; NOCICEPTION; NONHUMAN; NONMYELINATED NERVE; PAIN; POPULATION CODING HYPOTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PRURITUS; REVIEW; SENSORY NERVE CELL;

ANIMALS; HUMANS; MODELS, THEORETICAL; NEURAL PATHWAYS; PAIN; PRURITUS; SENSATION; SENSORY THRESHOLDS; SKIN; TEMPERATURE; TOUCH;

EID: 78049422591     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI43426     Document Type: Review

References (106)

1. Melzack R, Wall PD. Pain mechanisms: a new theory. Science. 1965;150(699):971-979.
2. Craig AD. Pain mechanisms: labeled lines versus convergence in central processing. Annu Rev Neurosci. 2003;26:1-30.
3. Perl ER. Getting a line on pain: is it mediated by dedicated pathways? Nat Neurosci. 1998;1(3):177-178.
4. Green BG. Temperature perception and nociception. J Neurobiol. 2004;61(1):13-29.
5. Perl ER. Ideas about pain, a historical view. Nat Rev Neurosci. 2007;8(1):71-80.
6. Norrsell U, Finger S, Lajonchere C. Cutaneous sensory spots and the "law of specific nerve energies": history and development of ideas. Brain Res Bull. 1999;48(5):457-465.
7. Torebjörk HE, Schady W, Ochoa J. Sensory correlates of somatic afferent fibre activation. Hum Neurobiol. 1984;3(1):15-20.
8. Handwerker HO, Kobal G. Psychophysiology of experimentally induced pain. Physiol Rev. 1993;73(3):639-671.
9. Belmonte C, Brock JA, Viana F. Converting cold into pain. Exp Brain Res. 2009;196(1):13-30.
10. Campero M, Bostock H. Unmyelinated afferents in human skin and their responsiveness to low temperature. Neurosci Lett. 2010;470(3):188-192.
11. Schmelz M. Itch and pain. Neurosci Biobehav Rev. 2010;34(2):171-176.
12. Woolf CJ, Ma Q. Nociceptors-noxious stimulus detectors. Neuron. 2007;55(3):353-364.
13. Foulkes T, Wood JN. Pain genes. PLoS Genetics. 2008;4(7):e1000086.
14. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell. 2009;139(2):267-284.
15. Wall PD. The gate control theory of pain mechanisms. A re-examination and re-statement. Brain. 1978;101(1):1-18.
16. Wood GJ, Akiyama T, Carstens E, Oaklander AL, Yosipovitch G. An insatiable itch. J Pain. 2009;10(8):792-797.
17. Handwerker HO. Microneurography of pruritus. Neurosci Lett. 2010;470(3):193-196.
18. Campero M, Baumann TK, Bostock H, Ochoa JL. Human cutaneous C fibres activated by cooling, heating and menthol. J Physiol. 2009;587(pt 23):5633-5652.
19. Alrutz S. On the temperature senses: II. The sensation of 'hot'. Mind. 1898;7:140-144.
20. Mackenzie RA, Burke D, Skuse NF, Lethlean AK. Fibre function and perception during cutaneous nerve block. J Neurol Neurosurg Psychiatry. 1975;38(9):865-873.
21. Fruhstorfer H. Thermal sensibility changes during ischemic nerve block. Pain. 1984;20(4):355-361.
22. Wahren LK, Torebjörk E, Jörum E. Central suppression of cold-induced C fibre pain by myelinated fibre input. Pain. 1989;38(3):313-319.
23. Yarnitsky D, Ochoa JL. Release of cold-induced burning pain by block of cold-specific afferent input. Brain. 1990;113(pt 4):893-902.
24. Craig AD, Bushnell MC. The thermal grill illusion: unmasking the burn of cold pain. Science. 1994;265(5169):252-255.
25. Craig AD, Reiman EM, Evans A, Bushnell MC. Functional imaging of an illusion of pain. Nature. 1996;384(6606):258-260.
26. Price DD, Hu JW, Dubner R, Gracely RH. Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses. Pain. 1977;3(1):57-68.
27. Meyer RA, Campbell JN. Evidence for two distinct classes of unmyelinated nociceptive afferents in monkey. Brain Res. 1981;224(1):149-152.
28. Defrin R, Benstein-Sheraizin A, Bezalel A, Mantzur O, Arendt-Nielsen L. The spatial characteristics of the painful thermal grill illusion. Pain. 2008;138(3):577-586.
29. Jenkins WL, Karr AC. Paradoxical warmth: a sufficient condition for its arousal. Am J Psychol. 1957;70(4):640-641.
30. Hämäläinen H, Vartiainen M, Karvanen L, Järvilehto T. Paradoxical heat sensations during moderate cooling of the skin. Brain Res. 1982;251(1):77-81.
31. Zhou HY, Zhang HM, Chen SR, Pan H. Increased nociceptive input rapidly modulates spinal GABA-ergic transmission through endogenously released glutamate. J Neurophysiol. 2007;97(1):871-882.
32. Dodt E, Zotterman Y. The discharge of specific cold fibres at high temperatures; the paradoxical cold. Acta Physiol Scand. 1952;26(4):358-365.
33. McKemy DD, Neuhausser WM, Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature. 2002;416(6876):52-58.
34. Peier AM, et al. A TRP channel that senses cold stimuli and menthol. Cell. 2002;108(5):705-715.
35. Alloui A, et al. TREK-1, a K+ channel involved in polymodal pain perception. EMBO J. 2006;25(11):2368-2376.
36. Madrid R, de la Peña E, Donovan-Rodriguez T, Belmonte C, Viana F. Variable threshold of trigeminal cold-thermosensitive neurons is determined by a balance between TRPM8 and Kv1 potassium channels. J Neurosci. 2009;29(10):3120-3131.
37. Noël J, et al. The mechano-activated K+ channels TRAAK and TREK-1 control both warm and cold perception. EMBO J. 2009;28(9):1308-1318.
38. Colburn RW, et al. Attenuated cold sensitivity in TRPM8 null mice. Neuron. 2007;54(3):379-386.
39. Bautista DM, et al. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature. 2007;448(7150):204-208.
40. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A. TRPM8 is required for cold sensation in mice.[see comment]. Neuron. 2007;54(3):371-378.
41. Knowlton WM, Bifolck-Fisher A, Bautista DM, McKemy DD. TRPM8, but not TRPA1, is required for neural and behavioral responses to acute noxious cold temperatures and cold-mimetics in vivo. Pain. 2010;150(2):340-350.
42. Takashima Y, Daniels RL, Knowlton W, Teng J, Liman ER, McKemy DD. Diversity in the neural circuitry of cold sensing revealed by genetic axonal labeling of transient receptor potential melastatin 8 neurons. J NeuroSci. 2007;27(51):14147-14157.
43. Story GM, et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell. 2003;112(6):819-829.
44. Bautista DM, et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell. 2006;124(6):1269-1282.
45. Kwan KY, et al. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron. 2006;50(2):277-289.
46. Karashima Y, et al. TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci U S A. 2009;106(4):1273-1278.
47. Dunham JP, Leith JL, Lumb BM, Donaldson LF. Transient receptor potential channel A1 and noxious cold responses in rat cutaneous nociceptors. NeuroScience. 2010;165(4):1412-1419.
48. Jordt SE, et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature. 2004;427(6971):260-265.
49. Fajardo O, Meseguer V, Belmonte C, Viana F. TRPA1 channels mediate cold temperature sensing in mammalian vagal sensory neurons: pharmacological and genetic evidence. J Neurosci. 2008;28(31):7863-7875.
50. Kwan KY, Corey DP. Burning cold: involvement of TRPA1 in noxious cold sensation. J Gen Physiol. 2009;133(3):251-256.
51. Munns C, AlQatari M, Koltzenburg M. Many cold sensitive peripheral neurons of the mouse do not express TRPM8 or TRPA1. Cell Calcium. 2007;41(1):41.
52. Namer B, Seifert F, Handwerker HO, Maihöfner C. TRPA1 and TRPM8 activation in humans: effects of cinnamaldehyde and menthol. Neuroreport. 2005;16(9):955-959.
53. Lawson JJ, McIlwrath SL, Woodbury CJ, Davis BM, Koerber HR. TRPV1 unlike TRPV2 is restricted to a subset of mechanically insensitive cutaneous nociceptors responding to heat. J Pain. 2008;9(4):298-308.
54. Dhaka A, Earley TJ, Watson J, Patapoutian A. Visualizing cold spots: TRPM8-expressing sensory neurons and their projections. J Neurosci. 2008;28(3):566-575.
55. Viana F, de la Peña E, Belmonte C. Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat Neurosci. 2002;5(3):254-260.
56. Hjerling-Leffler J, Alqatari M, Ernfors P, Koltzenburg M. Emergence of functional sensory subtypes as defined by transient receptor potential channel expression. J Neurosci. 2007;27(10):2435-2443.
57. Kiasalari Z, Salehi I, Zhong Y, McMahon SB, Michael-Titus AT, Michael GJ. Identification of perineal sensory neurons activated by innocuous heat. J Comp Neurol. 2010;518(2):137-162.
58. Dhaka A, Viswanath V, Patapoutian A. Trp ion channels and temperature sensation. Annu Rev NeuroSci. 2006;29:135-161.
59. Lumpkin EA, Caterina MJ. Mechanisms of sensory transduction in the skin. Nature. 2007;445(7130):858-865.
60. Dussor G, Koerber HR, Oaklander AL, Rice FL, Molliver DC. Nucleotide signaling and cutaneous mechanisms of pain transduction. Brain Res Rev. 2009;60(1):24-35.
61. Mandadi S, et al. TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP. Pflugers Arch. 2009;458(6):1093-1102.
62. Malin SA, Davis BM, Koerber HR, Reynolds IJ, Albers KM, Molliver DC. Thermal nociception and TRPV1 function are attenuated in mice lacking the nucleotide receptor P2Y2. Pain. 2008;138(3):484-496.
63. Handwerker HO. What is a polymodal nociceptor? J Pain. 2008;9(4):309-310.
64. Dong X, Han S, Zylka MJ, Simon MI, Anderson DJ. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell. 2001;106(5):619-632.
65. Zylka MJ, Rice FL, Anderson DJ. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron. 2005;45(1):17-25.
66. Rau KK, et al. Mrgprd enhances excitability in specific populations of cutaneous murine polymodal nociceptors. J Neurosci. 2009;29(26):8612-8619.
67. Ikoma A, Steinhoff M, Ständer S, Yosipovitch G, Schmelz M. The neurobiology of itch. Nat Rev Neurosci. 2006;7(7):535-547.
68. von Frey M. Zur physiologie der juckempfindug. Arc Néerl Phyiol. 1922;7:142-145.
69. Schmelz M, Schmidt R, Bickel A, Handwerker HO, Torebjörk HE. Specific C-receptors for itch in human skin. J Neurosci. 1997;17(20):8003-8008.
70. Liu Y, et al. Mechanisms of compartmentalized expression of Mrg class G-protein-coupled sensory receptors. J Neurosci. 2008;28(1):125-132.
71. Liu Q, et al. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell. 2009;139(7):1353-1365.
72. Sun YG, Chen ZF. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature. 2007;448(7154):700-703.
73. Sun YG, Zhao ZQ, Meng XL, Yin J, Liu XY, Chen ZF. Cellular basis of itch sensation. Science. 2009;325(5947):1531-1534.
74. Green BG, Shaffer GS. The sensory response to capsaicin during repeated topical exposures: differential effects on sensations of itching and pungency. Pain. 1993;53(3):323-334.
75. Schmelz M, Schmidt R, Weidner C, Hilliges M, Torebjork HE, Handwerker HO. Chemical response pattern of different classes of C-nociceptors to pruritogens and algogens. J Neurophysiol. 2003;89(5):2441-2448.
76. Shim WS, et al. TRPV1 mediates histamine-induced itching via the activation of phospholipase A2 and 12-lipoxygenase. J Neurosci. 2007;27(9):2331-2337.
77. Costa R, et al. Evidence for the role of neurogenic inflammation components in trypsin-elicited scratching behaviour in mice. Br J Pharmacol. 2008;154(5):1094-1103.
78. Shim WS, Oh U. Histamine-induced itch and its relationship with pain. Mol Pain. 2008;4:29.
79. Shimada SG, LaMotte RH. Behavioral differentiation between itch and pain in mouse. Pain. 2008;139(3):681-687.
80. Imamachi N, et al. TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms. Proc Natl Acad Sci U S A. 2009;106(27):11330-11335.
81. Johanek LM, et al. A role for polymodal C-fiber afferents in nonhistaminergic itch. J Neurosci. 2008;28(30):7659-7669.
82. Namer B, Carr R, Johanek LM, Schmelz M, Handwerker HO, Ringkamp M. Separate peripheral pathways for pruritus in man. J Neurophysiol. 2008;100(4):2062-2069.
83. Sikand P, Shimada SG, Green BG, LaMotte RH. Similar itch and nociceptive sensations evoked by punctate cutaneous application of capsaicin, histamine and cowhage. Pain. 2009;144(1-2):66-75.
84. LaMotte RH, Shimada SG, Green BG, Zelterman D. Pruritic and nociceptive sensations and dysesthesias from a spicule of cowhage. J Neurophysiol. 2009;101(3):1430-1443.
85. Andrew D, Craig AD. Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch. Nat Neurosci. 2001;4(1):72-77.
86. Akiyama T, Merrill AW, Carstens MI, Carstens E. Activation of superficial dorsal horn neurons in the mouse by a PAR-2 agonist and 5-HT: potential role in itch. J Neurosci. 2009;29(20):6691-6699.
87. McMahon SB, Koltzenburg M. Itching for an explanation. Trends Neurosci. 1992;15(12):497-501.
88. Lewis T, Grant RT, Marvin HM. Vascular rections of skin to injury. Part X. The intervention of a chemical stimulus illustrated especially by the flare. Heart. 1929;14:139-160.
89. Ward L, Wright E, McMahon SB. A comparison of the effects of noxious and innocuous counterstimuli on experimentally induced itch and pain. Pain. 1996;64(1):129-138.
90. Atanassoff PG, Brull SJ, Zhang J, Greenquist K, Silverman DG, Lamotte RH. Enhancement of experimental pruritus and mechanically evoked dysesthesiae with local anesthesia. Somatosens Mot Res. 1999;16(4):291-298. (Pubitemid 30006504)
91. Davidson S, Zhang X, Khasabov SG, Simone DA, Giesler GJJ. Relief of itch by scratching: state-dependent inhibition of primate spinothalamic tract neurons. Nat Neurosci. 2009;12(5):544-546.
92. Graham DT, Goodell H, Wolff HG. Neural mechanisms involved in itch, itchy skin, and tickle sensations. J Clin Invest. 1951;30(1):37-49.
93. Liu Q, Vrontou S, Rice FL, Zylka MJ, Dong X, Anderson DJ. Molecular genetic visualization of a rare subset of unmyelinated sensory neurons that may detect gentle touch. Nat Neurosci. 2007;10(8):946-948.
94. Southall MD, Li T, Gharibova LS, Pei Y, Nicol GD, Travers JB. Activation of epidermal vanilloid receptor-1 induces release of proinflammatory mediators in human keratinocytes. J Pharmacol Exp Ther. 2003;304(1):217-222.
95. Shimada SG, Shimada KA, Collins JG. Scratching behavior in mice induced by the proteinase-activated receptor-2 agonist, SLIGRL-NH2. Eur J Pharmacol. 2006;530(3):281-283.
96. Davidson S, Zhang X, Yoon CH, Khasabov SG, Simone DA, Giesler GJJ. The itch-producing agents histamine and cowhage activate separate populations of primate spinothalamic tract neurons. J Neurosci. 2007;27(37):10007-10014.
97. Johanek LM, et al. Psychophysical and physiological evidence for parallel afferent pathways mediating the sensation of itch. J Neurosci. 2007;27(28):7490-7497.
98. Tsujii K, Andoh T, Lee JB, Kuraishi Y. Activation of proteinase-activated receptors induces itch-associated response through histamine-dependent and - independent pathways in mice. J Pharmacol Sci. 2008;108(3):385-388.
99. Dai Y, et al. Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci. 2004;24(18):4293-4299.
100. Amadesi S, et al. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci. 2004;24(18):4300-4312.
101. Linley JE, Rose K, Patil M, Robertson B, Akopian AN, Gamper N. Inhibition of M current in sensory neurons by exogenous proteases: a signaling pathway mediating inflammatory nociception. J Neurosci. 2008;28(44):11240-11249.
102. Paszcuk AF, et al. Mechanisms underlying the nociceptive and inflammatory responses induced by trypsin in the mouse paw. Eur J Pharmacol. 2008;581(1-2):204-215.
103. Tuckett RP. Itch evoked by electrical stimulation of the skin. J Invest Dermatol. 1982;79(6):368-373.
104. Van Hees J, Gybels J. C nociceptor activity in human nerve during painful and non painful skin stimulation. J Neurol Neurosurg Psychiatry. 1981;44(7):600-607.
105. Zou X, Lin Q, Willis WD. The effects of sympathectomy on capsaicin-evoked fos expression of spinal dorsal horn GABAergic neurons. Brain Res. 2002;958(2):322-329.
106. Ross SE, et al. Loss of inhibitory interneurons in the dorsal spinal cord and elevated itch in Bhlhb5 mutant mice. Neuron. 2010;65(6):886-898.