Cutaneous Mechanisms of Tactile Perception: Morphological and Chemical Organization of the Innervation to the Skin

The Senses: A Comprehensive Reference

Volumn 6, Issue , 2008, Pages 1-31

  Rice, F L ^a   Albrecht, P J ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Cutaneous innervation; Dorsal root ganglia; Epidermis; Glabrous skin; Sensory endings; Sensory integration; Vascular innervation; Vibrissae; Whiskers

Indexed keywords

EID: 84882494433     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012370880-9.00340-6     Document Type: Chapter

References (139)

1. Albrecht P.J., Hines S., Eisenberg E., Pud D., Finlay D.R., Connolly M.K., Paré M., Davar G., Rice F.L. Pathologic alterations of cutaneous innervation and vasculature in affected limbs from patients with complex regional pain syndrome. Pain 2006, 120:244-266.
2. Andres K.H. On the fine structure of Merkel's tactile apparatus in the sinus hair. Naturwissenschaften 1966, 53:706.
3. Andres K.H. On the microstructure of receptors on sinus hair. Z. Zellforsch. Mikrosk. Anat. 1966, 75:339-365.
4. Arvidsson J., Rice F.L. Central projections of primary sensory neurons innervating different parts of the vibrissae follicles and intervibrissal skin on the mystacial pad of the rat. J. Comp. Neurol. 1991, 309:1-16.
5. Bensmaia S.J., Leung Y.Y., Hsiao S.S., Johnson K.O. Vibratory adaptation of cutaneous mechanoreceptive afferents. J. Neurophysiol. 2005, 94:3023-3036.
6. Bessou P., Perl E.R. Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J. Neurophysiol. 1969, 32:1025-1043.
7. Bessou P., Burgess P.R., Perl E.R., Taylor C.B. Dynamic properties of mechanoreceptors with unmyelinated (C) fibers. J. Neurophysiol. 1971, 34:116-131.
8. Biemesderfer D., Munger B.L., Binck J., Dubner R. The pilo-Ruffini complex: a non-sinus hair and associated slowly-adapting mechanoreceptor in primate facial skin. Brain Res. 1978, 142:197-222.
9. Bolanowski S.J. Intensity and frequency characteristics of Pacinian corpuscles. III. Effects of tetrodotoxin on transduction process. J. Neurophysiol. 1984, 51:831-839.
10. Bolanowski S.J., Pawson L. Organization of Meissner corpuscles in the glabrous skin of monkey and cat. Somatosens. Mot. Res. 2003, 20:223-231.
11. Bolanowski S.J., Zwislocki J.J. Intensity and frequency characteristics of Pacinian corpuscles. I. Action potentials. J. Neurophysiol. 1984, 51:793-811.
12. Bolanowski S.J., Zwislocki J.J. Intensity and frequency characteristics of Pacinian corpuscles. II. Receptor potentials. J. Neurophysiol. 1984, 51:812-830.
13. Brown A.G., Iggo A. A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit. J. Physiol. 1967, 193:707-733.
14. Burgess P.R., Perl E.R. Myelinated afferent fibres responding specifically to noxious stimulation of the skin. J. Physiol. 1967, 190:541-562.
15. Cahusac P.M., Senok S.S. Metabotropic glutamate receptor antagonists selectively enhance responses of slowly adapting type I mechanoreceptors. Synapse 2006, 59:235-242.
16. Cahusac P.M., Senok S.S., Hitchcock I.S., Genever P.G., Baumann K.I. Are unconventional NMDA receptors involved in slowly adapting type I mechanoreceptor responses?. Neuroscience 2005, 133:763-773.
17. Caterina M.J. Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R64-R76.
18. Cauna N. Nature and functions of the papillary ridges of the digital skin. Anat. Rec. 1954, 119:449-468.
19. Cauna N. Nerve supply and nerve endings in Meissner's corpuscles. Am. J. Anat. 1956, 29:315-350.
20. Cauna N., Ross L.L. The fine structure of Meissner's touch corpuscles of human fingers. J. Biophys. Biochem. Cytol. 1960, 8:467-482.
21. Chambers M.R., Andres K.H., von Duering M., Iggo A. The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. Q. J. Exp. Physiol. Cogn. Med. Sci. 1972, 57:417-445.
22. Chung M.K., Lee H., Mizuno A., Suzuki M., Caterina M.J. TRPV3 and TRPV4 mediate warmth-evoked currents in primary mouse keratinocytes. J. Biol. Chem. 2004, 279:21569-21575.
23. 2 receptor subunit in mediating multiple sensory effects of ATP. J. Physiol. 2005, 567:621-639.
24. Cohen R.H., Perl E.R. Chemical factors in the sensitization of cutaneous nociceptors. Prog. Brain Res. 1988, 74:201-206.
25. Cole J., Bushnell M.C., McGlone F., Elam M., Lamarre Y., Vallbo A., Olausson H. Unmyelinated tactile afferents underpin detection of low-force monofilaments. Muscle Nerve 2006, 34:105-107.
26. Connor C.E., Johnson K.O. Neural coding of tactile texture: comparison of spatial and temporal mechanisms for roughness perception. J. Neurosci. 1992, 12:3414-3426.
27. Connor C.E., Hsiao S.S., Phillips J.R., Johnson K.O. Tactile roughness: neural codes that account for psychophysical magnitude estimates. J. Neurosci. 1990, 10:3823-3836.
28. Craig A.D. Interoception: the sense of the physiological condition of the body. Curr. Opin. Neurobiol. 2003, 13:500-505.
29. Craig A.D. A new view of pain as a homeostatic emotion. Trends Neurosci. 2003, 26:303-307.
30. Dehnhardt G., Mauck B., Hanke W., Bleckmann H. Hydrodynamic trail-following in harbor seals (Phoca vitulina). Science 2001, 293:102-104.
31. Dhaka A., Viswanath V., Patapoutian A. TRP ion channels and temperature sensation. Annu. Rev. Neurosci. 2006, 29:135-161.
32. Djourhi L., Bleazard K., Lawson S.N. Association of somatic action potential shape with sensory receptive properties in guinea pig dorsal root ganglion neurons. J. Physiol. (Lond). 1998, 513:857-872.
33. Drummond H.A., Abboud F.M., Welsh M.J. Localization of beta and gamma subunits of ENaC in sensory nerve endings in the rat foot pad. Brain Res. 2000, 894:1-12.
34. Ebara S., Kumamoto K., Matsuura T., Mazurkiewicz J.E., Rice F.L. Similarities and differences in the innervation of mystacial vibrissal follicle-sinus complexes in the rat and cat: a confocal microscopic study. J. Comp. Neurol. 2002, 449:103-119.
35. Freeman B., Rowe M. The effect of sympathetic nerve stimulation on responses of cutaneous Pacinian corpuscles in the cat. Neurosci. Lett. 1981, 22:145-150.
36. + channels and stomatin are expressed in rat trigeminal mechanosensory neurons. Cell Tissue Res. 2000, 299:327-334.
37. Friedman R.M., Khalsa P.S., Greenquist K.W., LaMotte R.H. Neural coding of the location and direction of a moving object by a spatially distributed population of mechanoreceptors. J. Neurosci. 2002, 22:9556-9566.
38. Fundin B.T., Arvidsson J., Aldskogius H., Johansson O., Rice S.N., Rice F.L. A comprehensive immunofluorescence and lectin binding analysis of intervibrissal fur innervation in the mystacial pad of the rat. J. Comp. Neurol. 1997, 385:185-206.
39. Fundin B.T., Pfaller K., Rice F.L. Different distributions of the sensory and autonomic innervation among the microvasculature of the rat mystacial pad. J. Comp. Neurol. 1997, 389:545-568.
40. Funfschilling U., Ng Y.G., Zang K., Miyazaki J., Reichardt L.F., Rice F.L. TrkC kinase expression in distinct subsets of cutaneous trigeminal innervation and nonneuronal cells. J. Comp. Neurol. 2004, 480:392-414.
41. Garcia-Anoveros J., Samad T.A., Zuvela-Jelaska L., Woolf C.J., Corey D.P. Transport and localization of the DEG/ENaC ion channel BNaC1alpha to peripheral mechanosensory terminals of dorsal root ganglia neurons. J. Neurosci. 2001, 21:2678-2686.
42. Gardner E., Martin J. Coding of Sensory Information. Principles of Neuroscience 2000, 411-429. McGraw-Hill. 4th edn. E. Kandel, J. Schwartz, T. Jessell (Eds.).
43. Gardner E., Martin J., Jessell T. The Bodily Senses. Principles of Neuroscience 2000, 430-450. McGraw-Hill. 4th edn. E. Kandel, J. Schwartz, T. Jessell (Eds.).
44. Gibson J.M., Welker W.I. Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 2. Adaptation and coding of stimulus parameters. Somatosens. Res. 1983, 1:95-117.
45. Gibson J.M., Welker W.I. Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 1. Receptive field properties and threshold distributions. Somatosens. Res. 1983, 1:51-67.
46. Gillespie P.G., Walker R.G. Molecular basis of mechanosensory transduction. Nature 2001, 413:194-202.
47. Gokin A.P., Fareed M.U., Pan H.L., Hans G., Strichartz G.R., Davar G. Local injection of endothelin-1 produces pain-like behavior and excitation of nociceptors in rats. J. Neurosci. 2001, 21:5358-5366.
48. Gottschaldt K.M., Iggo A., Young D.W. Electrophysiology of the afferent innervation of sinus hairs, including vibrissae, of the cat. J. Physiol. 1972, 222:60P-61P.
49. Gottschaldt K.M., Iggo A., Young D.W. Functional characteristics of mechanoreceptors in sinus hair follicles of the cat. J. Physiol. 1973, 235:287-315.
50. Guclu B., Schepis E.A., Yelke S., Yucesoy C.A., Bolanowski S.J. Ovoid geometry of the Pacinian corpuscle is not the determining factor for mechanical excitation. Somatosens. Mot. Res. 2006, 23:119-126.
51. 3 purinoceptor and IB4 binding sites. Eur. J. Neurosci. 1999, 11:946-958.
52. Hardie R.C. TRP channels and lipids: from Drosophila to mammalian physiology. J. Physiol. 2007, 578:9-24.
53. Hilliges M., Astback J., Wang L., Arvidson K., Johansson O. Protein gene product 9.5-immunoreactive nerves and cells in human oral mucosa. Anat. Rec. 1996, 245:621-632.
54. Ibrahim M.M., Porreca F., Lai J., Albrecht P.J., Rice F.L., Khodorova A., Davar G., Makriyannis A., Vanderah T.W., Mata H.P., Malan T.P. CB2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:3093-3098.
55. Ichikawa H., Sugimoto T. Calcium-binding protein-immunoreactive innervation of the rat vibrissa. Brain Res. 2003, 970:226-231.
56. Iggo A. Cutaneous mechanoreceptors with afferent C fibres. J. Physiol. 1960, 152:337-353.
57. Iggo A. Temperature discrimination in the skin. Nature 1964, 204:481-483.
58. Iggo A. Cutaneous receptors and their sensory functions. J. Hand Surg. [Br.] 1984, 9:7-10.
59. Iggo A., Andres K.H. Morphology of cutaneous receptors. Annu. Rev. Neurosci. 1982, 5:1-31.
60. Iggo A., Muir A.R. The structure and function of a slowly adapting touch corpuscle in hairy skin. J. Physiol. 1969, 200:763-796.
61. Ju G., Hokfelt T., Brodin E., Fahrenkrug J., Fischer J.A., Frey P., Elde R.P., Brown J.C. Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res. 1987, 247:417-431.
62. Kennedy W.R., Wendelschafer-Crabb G. The innervation of human epidermis. J. Neurol. Sci. 1993, 115:184-190.
63. Khalsa P.S., Friedman R.M., Srinivasan M.A., Lamotte R.H. Encoding of shape and orientation of objects indented into the monkey fingerpad by populations of slowly and rapidly adapting mechanoreceptors. J. Neurophysiol. 1998, 79:3238-3251.
64. Khodorova A., Navarro B., Jouaville L.S., Murphy J.E., Rice F.L., Mazurkiewicz J.E., Long-Woodward D., Stoffel M., Strichartz G.R., Yukhananov R., Davar G. Endothelin-B receptor activation triggers an endogenous analgesic cascade at sites of peripheral injury. Nat. Med. 2003, 9:1055-1061.
65. Kleinfeld D., Ahissar E., Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 2006, 16:435-444.
66. Koerber H.R., Mandell L.M. Functional Heterogeneity of Dorsal root ganglion Cells. Sensory Neurons: Diverity, Development and Plasticity 1992, Oxford University Press, pp. 77-96.
67. Koerber H.R., Woodbury C.J. Comprehensive phenotyping of sensory neurons using an exvivo somatosensory system. Physiol. Behav. 2002, 77:589-594.
68. 2 receptor activation. Biochem. J. 2004, 380:329-338.
69. Koltzenburg M., Stucky C.L., Lewin G.R. Receptive properties of mouse sensory neurons innervating hairy skin. J. Neurophysiol. 1997, 78:1841-1850.
70. Kruger L. Morphological features of thin sensory afferent fibers: a new interpretation of 'nociceptor' function. Prog. Brain Res. 1988, 74:253-257.
71. Kruger L. The functional morphology of thin sensory axons: some principles and problems. Prog. Brain Res. 1996, 113:255-272.
72. Kruger L., Perl E.R., Sedivec M.J. Fine structure of myelinated mechanical nociceptor endings in cat hairy skin. J. Comp. Neurol. 1981, 198:137-154.
73. Kruger L., Silverman J.D., Mantyh P.W., Sternini C., Brecha N.C. Peripheral patterns of calcitonin-gene-related peptide general somatic sensory innervation: cutaneous and deep terminations. J. Comp. Neurol. 1989, 280:291-302.
74. Kumazawa T., Perl E.R. Primate cutaneous sensory units with unmyelinated (C) afferent fibers. J. Neurophysiol. 1977, 40:1325-1338.
75. Kwan K.Y., Allchorne A.J., Vollrath M.A., Christensen A.P., Zhang D.S., Woolf C.J., Corey D.P. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 2006, 50:277-289.
76. LaMotte R.H., Mountcastle V.B. Capacities of humans and monkeys to discriminate vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychological measurements. J. Neurophysiol. 1975, 38:539-559.
77. LaMotte R.H., Friedman R.M., Lu C., Khalsa P.S., Srinivasan M.A. Raised object on a planar surface stroked across the fingerpad: responses of cutaneous mechanoreceptors to shape and orientation. J. Neurophysiol. 1998, 80:2446-2466.
78. 2Y-receptor activating molecules. Mol. Pharmacol. 2003, 64:785-795.
79. Leiser S.C., Moxon K.A. Responses of trigeminal ganglion neurons during natural whisking behaviors in the awake rat. Neuron 2007, 53:117-133.
80. Leung Y.Y., Bensmaia S.J., Hsiao S.S., Johnson K.O. Time-course of vibratory adaptation and recovery in cutaneous mechanoreceptive afferents. J. Neurophysiol. 2005, 94:3037-3045.
81. Lichtenstein S.H., Carvell G.E., Simons D.J. Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. Somatosens. Mot. Res. 1990, 7:47-65.
82. Light A.R., Perl E.R. Unmyelinated afferent fibers are not only for pain anymore. J. Comp. Neurol. 2003, 461:137-139.
83. Lin S.Y., Corey D.P. TRP channels in mechanosensation. Curr. Opin. Neurobiol. 2005, 15:350-357.
84. Liu Q., Vrontou S., Rice F.L., Zylka M.J., Dong X., Anderson D.J. Molecular genetic visualization of a rare subset of unmyelinated sensory neurons that may detect gentle touch. Nat. Neurosci. 2007, (Epub ahead of print).
85. Lucarz A., Brand G. Current considerations about Merkel cells. Eur. J. Cell. Biol. 2007, 5:243-251.
86. Lumpkin E.A., Caterina M.J. Mechanisms of sensory transduction in the skin. Nature 2007, 445:858-865.
87. Mannsfeldt A.G., Carroll P., Stucky C.L., Lewin G.R. Stomatin, a MEC-2 like protein, is expressed by mammalian sensory neurons. Mol. Cell. Neurosci. 1999, 13:391-404.
88. Marshall C.D., Amin H., Kovacs K.M., Lydersen C. Microstructure and innervation of the mystacial vibrissal follicle-sinus complex in bearded seals, Erignathus barbatus (Pinnipedia: Phocidae). Anat. Rec. A Discov. Mol. Cell Evol. Biol. 2006, 288:13-25.
89. Mehta S.B., Kleinfeld D. Frisking the whiskers: patterned sensory input in the rat vibrissa system. Neuron 2004, 41:181-184.
90. Mehta S.B., Whitmer D., Figueroa R., Williams B.A., Kleinfeld D. Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol. 2007, 5:e15.
91. Mitrirattanakul S., Ramakul N., Guerrero A.V., Matsuka Y., Ono T., Iwase H., Mackie K., Faull K.F., Spigelman I. Site-specific increases in peripheral cannabinoid receptors and their endogenous ligands in a model of neuropathic pain. Pain 2006, 126:102-114.
92. Mizumoto N., Mummert M.E., Shalhevet D., Takashima A. Keratinocyte ATP release assay for testing skin-irritating potentials of structurally diverse chemicals. J. Invest. Dermatol. 2003, 121:1066-1072.
93. Molliver D.C., Immke D.C., Fierro L., Paré M., Rice F.L., McCleskey E.W. ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol. Pain 2005, 1:35.
94. Mosconi T.M., Rice F.L. Sensory innervation of the mystacial pad fur of the ferret. Neurosci. Lett. 1991, 121:199-202.
95. Mosconi T.M., Rice F.L., Song M.J. Sensory innervation in the inner conical body of the vibrissal follicle-sinus complex of the rat. J. Comp. Neurol. 1993, 328:232-251.
96. Mountcastle V.B., Talbot W.H., Darian-Smith I., Kornhuber H.H. Neural basis of the sense of flutter-vibration. Science 1967, 155:597-600.
97. Nakamura F., Strittmatter S.M. P2Y1 purinergic receptors in sensory neurons: contribution to touch-induced impulse generation. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:10465-10470.
98. Olson T.H., Riedl M.S., Vulchanova L., Ortiz-Gonzalez X.R., Elde R. An acid sensing ion channel (ASIC) localizes to small primary afferent neurons in rats. Neuroreport 1998, 9:1109-1113.
99. Owsianik G., D'Hoedt D., Voets T., Nilius B. Structure-function relationship of the TRP channel superfamily. Rev. Physiol. Biochem. Pharmacol. 2006, 156:61-90.
100. Paré M., Albrecht P.J., Noto C.J., Bodkin N.L., Pittenger G.L., Schreyer D.J., Tigno X.T., Hansen B.C., Rice F.L. Differential hypertrophy and atrophy among all types of cutaneous innervation in the glabrous skin of the monkey hand during aging and naturally occurring type 2 diabetes. J. Comp. Neurol. 2007, 501:543-567.
101. Paré M., Behets C., Cornu O. Paucity of presumptive Ruffini corpuscles in the index finger pad of humans. J. Comp. Neurol. 2003, 456:260-266.
102. Paré M., Elde R., Mazurkiewicz J.E., Smith A.M., Rice F.L. The Meissner corpuscle revised: a multiafferented mechanoreceptor with nociceptor immunochemical properties. J. Neurosci. 2001, 21:7236-7246.
103. Paré M., Smith A.M., Rice F.L. Distribution and terminal arborizations of cutaneous mechanoreceptors in the glabrous finger pads of the monkey. J. Comp. Neurol. 2002, 445:347-359.
104. Patrizi G., Munger B.L. The ultrastructure and innervation of rat vibrissae. J. Comp. Neurol. 1966, 126:423-435.
105. Pawson L., Bolanowski S.J. Voltage-gated sodium channels are present on both the neural and capsular structures of Pacinian corpuscles. Somatosens. Mot. Res. 2002, 19:231-237.
106. Pawson L., Slepecky N.B., Bolanowski S.J. Immunocytochemical identification of proteins within the Pacinian corpuscle. Somatosens. Mot. Res. 2000, 17:159-170.
107. Peier A.M., Reeve A.J., Andersson D.A., Moqrich A., Earley T.J., Hergarden A.C., Story G.M., Colley S., Hogenesch J.B., McIntyre P., Bevan S., Patapoutian A. A heat-sensitive TRP channel expressed in keratinocytes. Science 2002, 296:2046-2049.
108. Perl E.R. Myelinated afferent fibres innervating the primate skin and their response to noxious stimuli. J. Physiol. 1968, 197:593-615.
109. Perl E.R. Afferent basis of nociception and pain: evidence from the characteristics of sensory receptors and their projections to the spinal dorsal horn. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 1980, 58:19-45.
110. Perl E.R. Cutaneous polymodal receptors: characteristics and plasticity. Prog. Brain Res. 1996, 113:21-37.
111. Petersen K.L., Rice F.L., Suess F., Berro M., Rowbotham M.C. Relief of post-herpetic neuralgia by surgical removal of painful skin. Pain 2002, 98:119-126.
112. Pomonis J.D., Rogers S.D., Peters C.M., Ghilardi J.R., Mantyh P.W. Expression and localization of endothelin receptors: implications for the involvement of peripheral glia in nociception. J. Neurosci. 2001, 21:999-1006.
113. Price M.P., Lewin G.R., McIlwrath S.L., Cheng C., Xie J., Heppenstall P.A., Stucky C.L., Mannsfeldt A.G., Brennan T.J., Drummond H.A., Qiao J., Benson C.J., Tarr D.E., Hrstka R.F., Yang B., Williamson R.A., Welsh M.J. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 2000, 407:1007-1011.
114. Rice F.L., Rasmusson D.D. Innervation of the digit on the forepaw of the raccoon. J. Comp. Neurol. 2000, 417:467-490.
115. Rice F.L., Fundin B.T., Arvidsson J., Aldskogius H., Johansson O. Comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat. J. Comp. Neurol. 1997, 385:149-184.
116. Rice F.L., Kinnman E., Aldskogius H., Johansson O., Arvidsson J. The innervation of the mystacial pad of the rat as revealed by PGP 9.5 immunofluorescence. J. Comp. Neurol. 1993, 337:366-385.
117. Roosterman D., Goerge T., Schneider S.W., Bunnett N.W., Steinhoff M. Neuronal control of skin function: the skin as a neuroimmunoendocrine organ. Physiol. Rev. 2006, 86:1309-1379.
118. Roudier-Pujol C., Rochat A., Escoubet B., Eugene E., Barrandon Y., Bonvalet J.P., Farman N. Differential expression of epithelial sodium channel subunit mRNAs in rat skin. J. Cell Sci. 1996, 109(Pt 2):379-385.
119. Sawynok J. Topical and peripherally acting analgesics. Pharmacol. Rev. 2003, 55:1-20.
120. Schulte-Pelkum N., Wieskotten S., Hanke W., Dehnhardt G., Mauck B. Tracking of biogenic hydrodynamic trails in harbour seals (Phoca vitulina). J. Exp. Biol. 2007, 210:781-787.
121. Shin J.B., Martinez-Salgado C., Heppenstall P.A., Lewin G.R. A T-type calcium channel required for normal function of a mammalian mechanoreceptor. Nat. Neurosci. 2003, 6:724-730.
122. Stone L.S., Broberger C., Vulchanova L., Wilcox G.L., Hokfelt T., Riedl M.S., Elde R. Differential distribution of alpha2A and alpha2C adrenergic receptor immunoreactivity in the rat spinal cord. J. Neurosci. 1998, 18:5928-5937.
123. Sukharev S., Corey D.P. Mechanosensitive channels: multiplicity of families and gating paradigms. Sci. STKE 2004 2004, re4.
124. Szwed M., Bagdasarian K., Ahissar E. Encoding of vibrissal active touch. Neuron 2003, 40:621-630.
125. Tachibana T., Endoh M., Nawa T. Immunohistochemical expression of G protein alpha-subunit isoforms in rat and monkey Merkel cell-neurite complexes. Histochem. Cell Biol. 2001, 116:205-213.
126. Takahashi-Iwanaga H. Calcium signaling in terminal Schwann cells associated with lanceolate sensory endings in rat vibrissae. Ital. J. Anat. Embryol. 2005, 110:19-24.
127. Takahashi-Iwanaga H., Habara Y. Oscillatory calcium responses mediated by P2Y2 purinergic receptors in terminal Schwann cells of longitudinal lanceolate endings isolated from rat vibrissae. J. Comp. Neurol. 2004, 475:416-425.
128. Takahashi-Iwanaga H., Shimoda H. The three-dimensional microanatomy of Meissner corpuscles in monkey palmar skin. J. Neurocytol. 2003, 32:363-371.
129. Tominaga M., Caterina M.J. Thermosensation and pain. J. Neurobiol. 2004, 61:3-12.
130. Tuttle R.S., McCleary M. Mesenteric baroreceptors. Am. J. Physiol. 1975, 229:1514-1519.
131. Vallbo A.B., Johansson R.S. Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. Hum. Neurobiol. 1984, 3:3-14.
132. 3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology 1997, 36:1229-1242.
133. Wang L., Hilliges M., Jernberg T., Wiegleb-Edstrom D., Johansson O. Protein gene product 9.5-immunoreactive nerve fibres and cells in human skin. Cell Tissue Res. 1990, 261:25-33.
134. Wetzel C., Hu J., Riethmacher D., Benckendorff A., Harder L., Eilers A., Moshourab R., Kozlenkov A., Labuz D., Caspani O., Erdmann B., Machelska H., Heppenstall P.A., Lewin G.R. A stomatin-domain protein essential for touch sensation in the mouse. Nature 2007, 445:206-209.
135. Winkelmann R.K., Osment L.S. The Vater-Pacinian corpuscle in the skin of the human finger tip. AMA Arch. Derm. 1956, 73:116-122.
136. Yohn J.J., Morelli J.G., Walchak S.J., Rundell K.B., Norris D.A., Zamora M.R. Cultured human keratinocytes synthesize and secrete endothelin-1. J. Invest. Dermatol. 1993, 100:23-26.
137. Zhou Q.L., Strichartz G., Davar G. Endothelin-1 activates ET(A) receptors to increase intracellular calcium in model sensory neurons. Neuroreport 2001, 12:3853-3857.
138. Zucker E., Welker W.I. Coding of somatic sensory input by vibrissae neurons in the rat's trigeminal ganglion. Brain Res. 1969, 12:138-156.
139. Zylka M.J., Rice F.L., Anderson D.J. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 2005, 45:17-25.