Characterization of silent afferents in the pelvic and splanchnic innervations of the mouse colorectum

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 1, 2011, Pages

  Feng, Bin ^a   Gebhart, G F ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Afferent fiber; Irritable bowel syndrome; Mechanically insensitive afferent; Sensitization; Visceral pain

Indexed keywords

ANIMAL TISSUE; ARTICLE; COLON; CONTROLLED STUDY; ELECTROSTIMULATION; ENTERITIS; ENVIRONMENT; EXPOSURE; HYPERSENSITIVITY; INTESTINE INNERVATION; IRRITABLE COLON; MALE; MECHANICAL STIMULATION; MECHANORECEPTOR; MOUSE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RECTUM; SENSORY NERVE; SPLANCHNIC NERVE;

ANIMALS; COLON; ELECTRIC STIMULATION; IRRITABLE BOWEL SYNDROME; MALE; MECHANORECEPTORS; MICE; MICE, INBRED C57BL; NEURONS, AFFERENT; PELVIS; PHYSICAL STIMULATION; SPLANCHNIC NERVES;

EID: 78650770420     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00406.2010     Document Type: Article

References (52)

1. Anand U, Otto WR, Facer P, Zebda N, Selmer I, Gunthorpe MJ, Chessell IP, Sinisi M, Birch R, Anand P. TRPA1 receptor localisation in the human peripheral nervous system and functional studies in cultured human and rat sensory neurons. Neurosci Lett 438: 221-227, 2008.
2. Berthoud HR, Blackshaw LA, Brookes SJ, Grundy D. Neuroanatomy of extrinsic afferents supplying the gastrointestinal tract. Neurogastroenterol Motil 16, Suppl 1: 28-33, 2004.
3. Bostock H, Campero M, Serra J, Ochoa J. Velocity recovery cycles of C fibres innervating human skin. J Physiol 553: 649-663, 2003. (Pubitemid 37527561)
4. Brierley SM, Carter R, Jones W III, Xu L, Robinson DR, Hicks GA, Gebhart GF, Blackshaw LA. Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol 567: 267-281, 2005. (Pubitemid 41167320)
5. Brierley SM, Hughes PA, Page AJ, Kwan KY, Martin CM, O'Donnell TA, Cooper NJ, Harrington AM, Adam B, Liebregts T, Holtmann G, Corey DP, Rychkov GY, Blackshaw LA. The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 137: 2084-2095, 2009.
6. Brierley SM, Jones RC III, Gebhart GF, Blackshaw LA. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127: 166-178, 2004.
7. Bueno L, Fioramonti J. Effects of inflammatory mediators on gut sensitivity. Can J Gastroenterol 13, Suppl A: 42A-46A, 1999.
8. Bueno L, Fioramonti J. Visceral perception: inflammatory and non-inflammatory mediators. Gut 51, Suppl 1: i19-i23, 2002.
9. Cervero F, Sann H. Mechanically evoked responses of afferent fibres innervating the guinea-pig's ureter: an in vitro study. J Physiol 412:245-266, 1989.
10. Christianson JA, McIlwrath SL, Koerber HR, Davis BM. Transient receptor potential vanilloid 1-immunopositive neurons in the mouse are more prevalent within colon afferents compared to skin and muscle afferents. Neuroscience 140: 247-257, 2006.
11. Coutinho SV, Su X, Sengupta JN, Gebhart GF. Role of sensitized pelvic nerve afferents from the inflamed rat colon in the maintenance of visceral hyperalgesia. Prog Brain Res 129: 375-387, 2000.
12. Feng B, Brumovsky PR, Gebhart GF. Differential roles of stretch-sensitive pelvic nerve afferents innervating mouse distal colon and rectum. Am J Physiol Gastrointest Liver Physiol 298: G402-G409, 2010.
13. Feng B, Gebhart GF. Silent afferents in the pelvic nerve innervation of the mouse colon (Abstract). Gastroenterology 136: A723, 2009.
14. Feng B, La JH, Tanaka T, Gebhart GF. Silent afferents and colorectal hypersensitivity. Program No. 682.19/VV3. In: 2010 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience.
15. Gee MD, Lynn B, Cotsell B. Activity-dependent slowing of conduction velocity provides a method for identifying different functional classes of C-fibre in the rat saphenous nerve. Neuroscience 73: 667-675, 1996.
16. George A, Serra J, Navarro X, Bostock H. Velocity recovery cycles of single C fibres innervating rat skin. J Physiol 578: 213-232, 2007.
17. Grigg P, Schaible HG, Schmidt RF. Mechanical sensitivity of group III and IV afferents from posterior articular nerve in normal and inflamed cat knee. J Neurophysiol 55: 635-643, 1986.
18. Habler HJ, Janig W, Koltzenburg M. A novel type of unmyelinated chemosensitive nociceptor in the acutely inflamed urinary bladder. Agents Actions 25: 219-221, 1988.
19. Habler HJ, Janig W, Koltzenburg M. Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J Physiol 425: 545-562, 1990.
20. Handwerker HO, Kilo S, Reeh PW. Unresponsive afferent nerve fibres in the sural nerve of the rat. J Physiol 435: 229-242, 1991.
21. Hughes PA, Brierley SM, Martin CM, Brookes SJ, Linden DR, Blackshaw LA. Post-inflammatory colonic afferent sensitization: different subtypes, different pathways, and different time-courses. Gut 58: 1333-1341, 2009.
22. Janig W, Koltzenburg M. On the function of spinal primary afferent fibres supplying colon and urinary bladder. J Auton Nerv Syst 30 Suppl: S89-S96, 1990.
23. Jones RC III, Otsuka E, Wagstrom E, Jensen CS, Price MP, Gebhart GF. Short-term sensitization of colon mechanoreceptors is associated with long-term hypersensitivity to colon distention in the mouse. Gastroenterology 133: 184-194, 2007.
24. Jones RC III, Xu L, Gebhart GF. The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J Neurosci 25: 10981-10989, 2005. (Pubitemid 41692628)
25. Kessler W, Kirchhoff C, Reeh PW, Handwerker HO. Excitation of cutaneous afferent nerve endings in vitro by a combination of inflammatory mediators and conditioning effect of substance P. Exp Brain Res 91: 467-476, 1992.
26. Kress M, Koltzenburg M, Reeh PW, Handwerker HO. Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 68: 581-595, 1992.
27. Lynn PA, Blackshaw LA. In vitro recordings of afferent fibres with receptive fields in the serosa, muscle and mucosa of rat colon. J Physiol 518: 271-282, 1999.
28. McMahon SB, Morrison JF. Spinal neurones with long projections activated from the abdominal viscera of the cat. J Physiol 322: 1-20, 1982. (Pubitemid 12177734)
29. Mei N. Intestinal chemosensitivity. Physiol Rev 65: 211-237, 1985.
30. Mei N, Lucchini S. Current data and ideas on digestive sensitivity. J Auton Nerv Syst 41: 15-18, 1992. (Pubitemid 23000491)
31. Meyer RA, Davis KD, Cohen RH, Treede RD, Campbell JN. Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey. Brain Res 561: 252-261, 1991.
32. Neuhuber WL, Appelt M, Polak JM, Baier-Kustermann W, Abelli L, Ferri GL. Rectospinal neurons: cell bodies, pathways, immunocytochemistry and ultrastructure. Neuroscience 56: 367-378, 1993. (Pubitemid 23274756)
33. Page AJ, Martin CM, Blackshaw LA. Vagal mechanoreceptors and chemoreceptors in mouse stomach and esophagus. J Neurophysiol 87: 2095-2103, 2002.
34. Pogatzki EM, Gebhart GF, Brennan TJ. Characterization of Adelta- and C-fibers innervating the plantar rat hindpaw one day after an incision. J Neurophysiol 87: 721-731, 2002.
35. Price DD, Craggs JG, Zhou Q, Verne GN, Perlstein WM, Robinson ME. Widespread hyperalgesia in irritable bowel syndrome is dynamically maintained by tonic visceral impulse input and placebo/nocebo factors: evidence from human psychophysics, animal models, and neuroimaging. Neuroimage 47: 995-1001, 2009.
36. Ringkamp M, Johanek LM, Borzan J, Hartke TV, Wu G, Pogatzki-Zahn EM, Campbell JN, Shim B, Schepers RJ, Meyer RA. Conduction properties distinguish unmyelinated sympathetic efferent fibers and unmyelinated primary afferent fibers in the monkey. PLoS One 5: e9076, 2010.
37. Robinson DR, Gebhart GF. Inside information: the unique features of visceral sensation. Mol Interv 8: 242-253, 2008.
38. Schaible HG, Schmidt RF. Responses of fine medial articular nerve afferents to passive movements of knee joints. J Neurophysiol 49: 1118-1126, 1983.
39. Schmidt R, Schmelz M, Forster C, Ringkamp M, Torebjork E, Handwerker H. Novel classes of responsive and unresponsive C nociceptors in human skin. J Neurosci 15: 333-341, 1995.
40. Sengupta JN, Gebhart GF. Characterization of mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat. J Neurophysiol 71: 2046-2060, 1994. (Pubitemid 24184852)
41. Sengupta JN, Gebhart GF. Mechanosensitive properties of pelvic nerve afferent fibers innervating the urinary bladder of the rat. J Neurophysiol 72: 2420-2430, 1994. (Pubitemid 24362634)
42. Serra J, Campero M, Bostock H, Ochoa J. Two types of C nociceptors in human skin and their behavior in areas of capsaicin-induced secondary hyperalgesia. J Neurophysiol 91: 2770-2781, 2004. (Pubitemid 38649782)
43. Serra J, Campero M, Ochoa J, Bostock H. Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin. J Physiol 515: 799-811, 1999. (Pubitemid 29140114)
44. Sheehan D. The afferent nerve supply of the mesentery and its significance in the causation of abdominal pain. J Anat 67: 233-249, 1933.
45. Song X, Chen BN, Zagorodnyuk VP, Lynn PA, Blackshaw LA, Grundy D, Brunsden AM, Costa M, Brookes SJ. Identification of medium/high-threshold extrinsic mechanosensitive afferent nerves to the gastrointestinal tract. Gastroenterology 137: 274-284, 2009.
46. Su X, Gebhart GF. Mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat are polymodal in character. J Neurophysiol 80: 2632-2644, 1998. (Pubitemid 28546191)
47. Suckow SK, Caudle RM. Identification and immunohistochemical characterization of colospinal afferent neurons in the rat. Neuroscience 153: 803-813, 2008.
48. Verne GN, Robinson ME, Vase L, Price DD. Reversal of visceral and cutaneous hyperalgesia by local rectal anesthesia in irritable bowel syndrome (IBS) patients. Pain 105: 223-230, 2003. (Pubitemid 37173409)
49. Weidner C, Schmelz M, Schmidt R, Hansson B, Handwerker HO, Torebjork HE. Functional attributes discriminating mechano-insensitive and mechano-responsive C nociceptors in human skin. J Neurosci 19: 10184-10190, 1999. (Pubitemid 30226690)
50. Weidner C, Schmidt R, Schmelz M, Hilliges M, Handwerker HO, Torebjork HE. Time course of post-excitatory effects separates afferent human C fibre classes. J Physiol 527: 185-191, 2000. (Pubitemid 30649595)
51. Xu L, Gebhart GF. Characterization of mouse lumbar splanchnic and pelvic nerve urinary bladder mechanosensory afferents. J Neurophysiol 99: 244-253, 2008.
52. Zimmermann K, Hein A, Hager U, Kaczmarek JS, Turnquist BP, Clapham DE, Reeh PW. Phenotyping sensory nerve endings in vitro in the mouse. Nat Protoc 4: 174-196, 2009.