Different forms of glycine- and GABA A-receptor mediated inhibitory synaptic transmission in mouse superficial and deep dorsal horn neurons

Molecular Pain

Volumn 5, Issue , 2009, Pages

  Anderson, Wayne B ^a   Graham, Brett A ^a   Beveridge, Natalie J ^a   Tooney, Paul A ^a   Brichta, Alan M ^a   Callister, Robert J ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CANNABINOID; GLYCINE RECEPTOR;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; C57BL MOUSE; DRUG EFFECT; ELECTROPHYSIOLOGY; FEMALE; GENETICS; IN VITRO STUDY; MALE; METABOLISM; MOUSE; PATCH CLAMP; PHYSIOLOGY; POLYMERASE CHAIN REACTION; POSTERIOR HORN CELL; SYNAPTIC TRANSMISSION;

ANIMALS; CANNABINOIDS; ELECTROPHYSIOLOGY; FEMALE; MALE; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PATCH-CLAMP TECHNIQUES; POLYMERASE CHAIN REACTION; POSTERIOR HORN CELLS; RECEPTORS, GABA-A; RECEPTORS, GLYCINE; SYNAPTIC TRANSMISSION;

EID: 75549085146     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-5-65     Document Type: Article

References (83)

1. Willis WD, Coggeshall RE. Sensory Mechanisms of the Spinal Cord 2004, New York: Kluwer Academic/Plenum Publishers, 3.
2. Todd AJ, Koerber HR. Neuroanatomical substrates of spinal nociception. Wall and Melzack's Textbook of Pain 2006, 73-90. Philadelphia: Elsevier Churchill Livingston, McMahon SB, Koltzenburg M, 5.
3. Brown AG. The dorsal horn of the spinal cord. Q J Exp Physiol 1982, 67:193-212.
4. Light AR, Perl ER. Re-examination of the dorsal root projection to the spinal dorsal horn including observations on the differential termination of coarse and fine fibers. J Comp Neurol 1979, 186:117-131. 10.1002/cne.901860202, 447880.
5. Light AR, Perl ER. Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 1979, 186:133-150. 10.1002/cne.901860203, 109477.
6. Christensen BN, Perl ER. Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J Neurophysiol 1970, 33:293-307.
7. Sugiura Y, Lee CL, Perl ER. Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. Science 1986, 234:358-361. 10.1126/science.3764416, 3764416.
8. Tuckett RP, Wei JY. Response to an itch-producing substance in cat. I. Cutaneous receptor populations with myelinated axons. Brain Res 1987, 413:87-94. 10.1016/0006-8993(87)90156-9, 3594260.
9. Tuckett RP, Wei JY. Response to an itch-producing substance in cat. II. Cutaneous receptor populations with unmyelinated axons. Brain Res 1987, 413:95-103. 10.1016/0006-8993(87)90157-0, 3594261.
10. Vallbo AB, Olausson H, Wessberg J. Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin. J Neurophysiol 1999, 81:2753-2763.
11. Koerber HR, Woodbury CJ. Comprehensive phenotyping of sensory neurons using an ex vivo somatosensory system. Physiol Behav 2002, 77:589-594. 10.1016/S0031-9384(02)00904-6, 12527004.
12. Koerber HR, Brown PB. Quantitative analysis of dorsal horn cell receptive fields following limited deafferentation. J Neurophysiol 1995, 74:2065-2076.
13. Woolf CJ. Central terminations of cutaneous mechanoreceptive afferents in the rat lumbar spinal cord. J Comp Neurol 1987, 261:105-119. 10.1002/cne.902610109, 3624538.
14. Craig ADB. Pain mechanisms: labeled lines versus convergence in central processing. Ann Rev Neurosci 2003, 26:1-30. 10.1146/annurev.neuro.26.041002.131022, 12651967.
15. Klop EM, Mouton LJ, Hulsebosch R, Boers J, Holstege G. In cat four times as many lamina I neurons project to the parabrachial nuclei and twice as many to the periaqueductal gray as to the thalamus. Neuroscience 2005, 134:189-197. 10.1016/j.neuroscience.2005.03.035, 15953685.
16. Kobayashi Y. Distribution and morphology of spinothalamic tract neurons in the rat. Anat Embryol (Berl) 1998, 197:51-67. 10.1007/s004290050119, 9462858.
17. Willis WD, Zhang X, Honda CN, Giesler GJ. Projections from the marginal zone and deep dorsal horn to the ventrobasal nuclei of the primate thalamus. Pain 2001, 92:267-276. 10.1016/S0304-3959(01)00268-8, 11323148.
18. Lu Y, Perl ER. A Specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fiber input. J Neurosci 2003, 23:8752-8758.
19. Lu Y, Perl ER. Modular organization of excitatory circuits between neurons of the spinal superficial dorsal horn (laminae I and II). J Neurosci 2005, 25:3900-3907. 10.1523/JNEUROSCI.0102-05.2005, 15829642.
20. Schneider SP. Local circuit connections between hamster laminae III and IV dorsal horn neurons. J Neurophysiol 2008, 99:1306-1318. 10.1152/jn.00962.2007, 18184889.
21. Cronin JN, Bradbury EJ, Lidierth M. Laminar distribution of GABAA- and glycine-receptor mediated tonic inhibition in the dorsal horn of the rat lumbar spinal cord: effects of picrotoxin and strychnine on expression of Fos-like immunoreactivity. Pain 2004, 112:156-163. 10.1016/j.pain.2004.08.010, 15494196.
22. Harvey RJ, Depner UB, Wassle H, Ahmadi S, Heindl C, Reinold H, Smart TG, Harvey K, Schutz B, Abo-Salem OM, Zimmer A, Poisbeau P, Welzl H, Wolfer DP, Betz H, Zeilhofer HU, Muller U. GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science 2004, 304:884-887. 10.1126/science.1094925, 15131310.
23. Gilbert PE. A comparison of THC, nantradol, nabilone, and morphine in the chronic spinal dog. J Clin Pharmacol 1981, 21:311S-319S.
24. Smith PB, Martin BR. Spinal mechanisms of delta 9-tetrahydrocannabinol-induced analgesia. Brain Res 1992, 578:8-12. 10.1016/0006-8993(92)90222-U, 1324767.
25. Farquhar-Smith WP, Egertova M, Bradbury EJ, McMahon SB, Rice AS, Elphick MR. Cannabinoid CB(1) receptor expression in rat spinal cord. Mol Cell Neurosci 2000, 15:510-521. 10.1006/mcne.2000.0844, 10860578.
26. Richardson JD, Aanonsen L, Hargreaves KM. Hypoactivity of the spinal cannabinoid system results in NMDA-dependent hyperalgesia. J Neurosci 1998, 18:451-457.
27. Shen M, Piser TM, Seybold VS, Thayer SA. Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 1996, 16:4322-4334.
28. Lichtman AH, Martin BR. Cannabinoid-induced antinociception is mediated by a spinal alpha 2-noradrenergic mechanism. Brain Res 1991, 559:309-314. 10.1016/0006-8993(91)90017-P, 1665384.
29. Pugh G, Smith PB, Dombrowski DS, Welch SP. The role of endogenous opioids in enhancing the antinociception produced by the combination of delta 9-tetrahydrocannabinol and morphine in the spinal cord. J Pharmacol Exp Ther 1996, 279:608-616.
30. Reche I, Fuentes JA, Ruiz-Gayo M. A role for central cannabinoid and opioid systems in peripheral delta 9-tetrahydrocannabinol-induced analgesia in mice. Eur J Pharmacol 1996, 301:75-81. 10.1016/0014-2999(96)00045-3, 8773449.
31. Hejazi N, Zhou C, Oz M, Sun H, Ye JH, Zhang L. Delta9-tetrahydrocannabinol and endogenous cannabinoid anandamide directly potentiate the function of glycine receptors. Mol Pharmacol 2006, 69:991-997.
32. Lozovaya N, Yatsenko N, Beketov A, Tsintsadze T, Burnashev N. Glycine receptors in CNS neurons as a target for nonretrograde action of cannabinoids. J Neurosci 2005, 25:7499-7506. 10.1523/JNEUROSCI.0977-05.2005, 16107637.
33. Walsh MA, Graham BA, Brichta AM, Callister RJ. Evidence for a critical period in the development of excitability and potassium currents in mouse lumbar superficial dorsal horn neurons. J Neurophysiol 2009, 101:1800-1812. 10.1152/jn.90755.2008, 19176612.
34. Bekkers JM, Stevens CF. NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus. Nature 1989, 341:230-233. 10.1038/341230a0, 2571090.
35. Graham BA, Brichta AM, Schofield PR, Callister RJ. Altered potassium channel function in the superficial dorsal horn of the spastic mouse. J Physiol (Lond) 2007, 584:121-136. 10.1113/jphysiol.2007.138198, 2277054, 17690143.
36. Franklin KBJ, Paxinos G. Mouse Brain in Stereotaxic Coordinates 1997, San Deigo: Academic Press, 3.
37. Clements JD, Bekkers JM. Detection of spontaneous synaptic events with an optimally scaled template. Biophys J 1997, 73:220-229. 10.1016/S0006-3495(97)78062-7, 1180923, 9199786.
38. Callister RJ, Walmsley B. Amplitude and time course of evoked and spontaneous synaptic currents in rat submandibular ganglion cells. J Physiol (Lond) 1996, 490:149-157. 1158653, 8745284.
39. Graham BA, Schofield PR, Sah P, Callister RJ. Altered inhibitory synaptic transmission in superficial dorsal horn neurones in spastic and oscillator mice. J Physiol (Lond) 2003, 551:905-916. 10.1113/jphysiol.2003.049064, 2343288, 12837931.
40. Traynelis SF, Silver RA, Cull-Candy SG. Estimated conductance of glutamate receptor channels activated during EPSCs at the cerebellar mossy fiber-granule cell synapse. Neuron 1993, 11:279-289. 10.1016/0896-6273(93)90184-S, 7688973.
41. Beveridge NJ, Tooney PA, Carroll AP, Gardiner E, Bowden N, Scott RJ, Tran N, Dedova I, Cairns MJ. Dysregulation of miRNA 181b in the temporal cortex in schizophrenia. Hum Mol Genet 2008, 17:1156-1168. 10.1093/hmg/ddn005, 18184693.
42. Molander C, Xu Q, Grant G. The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 1984, 230:133-141. 10.1002/cne.902300112, 6512014.
43. Rexed B. The cytoarchitectonic organization of the spinal cord in the cat. J Comp Neurol 1952, 96:414-495. 10.1002/cne.900960303, 14946260.
44. Lozovaya N, Yatsenko N, Beketov A, Tsintsadze T, Burnashev N. Glycine Receptors in CNS Neurons as a Target for Nonretrograde Action of Cannabinoids. J Neurosci 2005, 25:7499-7506. 10.1523/JNEUROSCI.0977-05.2005, 16107637.
45. Chery N, Yu XH, de Koninck Y. Visualization of lamina I of the dorsal horn in live adult rat spinal cord slices. J Neurosci Methods 2000, 96:133-142. 10.1016/S0165-0270(99)00195-8, 10720677.
46. Todd AJ, Sullivan AC. Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 1990, 296:496-505. 10.1002/cne.902960312, 2358549.
47. Zeilhofer HU, Studler B, Arabadzisz D, Schweizer C, Ahmadi S, Layh B, Bosl MR, Fritschy JM. Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J Comp Neurol 2005, 482:123-141. 10.1002/cne.20349, 15611994.
48. Zeilhofer HU. The glycinergic control of spinal pain processing. Cell Mol Life Sci 2005, 62:2027-2035. 10.1007/s00018-005-5107-2, 15968463.
49. Mackie M, Hughes DI, Maxwell DJ, Tillakaratne NJ, Todd AJ. Distribution and colocalisation of glutamate decarboxylase isoforms in the rat spinal cord. Neuroscience 2003, 119:461-472. 10.1016/S0306-4522(03)00174-X, 12770560.
50. Inquimbert P, Rodeau JL, Schlichter R. Differential contribution of GABAergic and glycinergic components to inhibitory synaptic transmission in lamina II and laminae III-IV of the young rat spinal cord. Eur J Neurosci 2007, 26:2940-2949. 10.1111/j.1460-9568.2007.05919.x, 18001289.
51. Baccei ML, Fitzgerald M. Development of GABAergic and Glycinergic Transmission in the Neonatal Rat Dorsal Horn. J Neurosci 2004, 24:4749-4757. 10.1523/JNEUROSCI.5211-03.2004, 15152035.
52. Graham BA, Schofield PR, Sah P, Margrie TW, Callister RJ. Distinct Physiological Mechanisms Underlie Altered Glycinergic Synaptic Transmission in the Murine Mutants spastic, spasmodic, and oscillator. J Neurosci 2006, 26:4880-4890. 10.1523/JNEUROSCI.3991-05.2006, 16672662.
53. Singer JH, Talley EM, Bayliss DA, Berger AJ. Development of glycinergic synaptic transmission to rat brain stem motoneurons. J Neurophysiol 1998, 80:2608-2620.
54. Chery N, de Koninck Y. Junctional versus extrajunctional glycine and GABA(A) receptor-mediated IPSCs in identified lamina I neurons of the adult rat spinal cord. J Neurosci 1999, 19:7342-7355.
55. Takahashi T, Momiyama A. Single-channel currents underlying glycinergic inhibitory postsynaptic responses in spinal neurons. Neuron 1991, 7:965-969. 10.1016/0896-6273(91)90341-V, 1722412.
56. Lim R, Alvarez FJ, Walmsley B. Quantal size is correlated with receptor cluster area at glycinergic synapses in the rat brainstem. J Physiol (Lond) 1999, 516(Pt 2):505-512. 10.1111/j.1469-7793.1999.0505v.x, 2269264, 10087348.
57. Bohlhalter S, Weinmann O, Mohler H, Fritschy J. Laminar compartmentalization of GABAA-receptor subtypes in the spinal cord: an immunohistochemical study. J Neurosci 1996, 16:283-297.
58. Bosman LW, Heinen K, Spijker S, Brussaard AB. Mice lacking the major adult GABAA receptor subtype have normal number of synapses, but retain juvenile IPSC kinetics until adulthood. J Neurophysiol 2005, 94:338-346. 10.1152/jn.00084.2005, 15758057.
59. Brussaard AB, Kits KS, Baker RE, Willems WP, Leyting-Vermeulen JW, Voorn P, Smit AB, Bicknell RJ, Herbison AE. Plasticity in fast synaptic inhibition of adult oxytocin neurons caused by switch in GABA(A) receptor subunit expression. Neuron 1997, 19:1103-1114. 10.1016/S0896-6273(00)80401-8, 9390523.
60. Legendre P. The glycinergic inhibitory synapse. Cell Mol Life Sci 2001, 58:760-793. 10.1007/PL00000899, 11437237.
61. Lynch JW. Molecular structure and function of the glycine receptor chloride channel. Physiol Rev 2004, 84:1051-1095. 10.1152/physrev.00042.2003, 15383648.
62. Morisset V, Urban L. Cannabinoid-induced presynaptic inhibition of glutamatergic EPSCs in substantia gelatinosa neurons of the rat spinal cord. J Neurophysiol 2001, 86:40-48.
63. Twitchell W, Brown S, Mackie K. Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 1997, 78:43-50.
64. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, Freund TF. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 1999, 19:4544-4558.
65. Schlicker E, Kathmann M. Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 2001, 22:565-572. 10.1016/S0165-6147(00)01805-8, 11698100.
66. Vaughan CW, Christie MJ. Retrograde signalling by endocannabinoids. Handb Exp Pharmacol 2005, 367-383. full_text, 16596781.
67. Salio C, Fischer J, Franzoni MF, Conrath M. Pre- and postsynaptic localizations of the CB1 cannabinoid receptor in the dorsal horn of the rat spinal cord. Neuroscience 2002, 110:755-764. 10.1016/S0306-4522(01)00584-X, 11934482.
68. Yaksh TL. Behavioral and autonomic correlates of the tactile evoked allodynia produced by spinal glycine inhibition: effects of modulatory receptor systems and excitatory amino acid antagonists. Pain 1989, 37:111-123. 10.1016/0304-3959(89)90160-7, 2542867.
69. Sivilotti L, Woolf CJ. The contribution of GABAA and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord. J Neurophysiol 1994, 72:169-179.
70. Jennings EA, Vaughan CW, Roberts LA, Christie MJ. The actions of anandamide on rat superficial medullary dorsal horn neurons in vitro. J Physiol (Lond) 2003, 548:121-129. 10.1113/jphysiol.2002.035063, 2342784, 12562891.
71. Santos SFA, Rebelo S, Derkach VA, Safronov BV. Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat. J Physiol (Lond) 2007, 581:241-254. 10.1113/jphysiol.2006.126912, 2075233, 17331995.
72. Graham BA, Brichta AM, Callister RJ. Moving from an averaged to specific view of spinal cord pain processing circuits. J Neurophysiol 2007, 98:1057-1063. 10.1152/jn.00581.2007, 17567772.
73. Yang Z, Aubrey KR, Alroy I, Harvey RJ, Vandenberg RJ, Lynch JW. Subunit-specific modulation of glycine receptors by cannabinoids and N-arachidonyl-glycine. Biochem Pharmacol 2008, 76:1014-1023. 10.1016/j.bcp.2008.07.037, 18755158.
74. Diana MA, Levenes C, Mackie K, Marty A. Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 2002, 22:200-208.
75. Haefely W, Kulcsar A, Mohler H, Pieri L, Polc P, Schaffner R. Possible involvement of GABA in the central actions of benzodiazepines. Adv Biochem Psychopharmacol 1975, 131-151.
76. Lin LH, Whiting P, Harris RA. Molecular determinants of general anesthetic action: role of GABAA receptor structure. J Neurochem 1993, 60:1548-1553. 10.1111/j.1471-4159.1993.tb03320.x, 7681105.
77. Soldo BL, Proctor WR, Dunwiddie TV. Ethanol differentially modulates GABAA receptor-mediated chloride currents in hippocampal, cortical, and septal neurons in rat brain slices. Synapse 1994, 18:94-103. 10.1002/syn.890180204, 7839317.
78. Belelli D, Lambert JJ. Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 2005, 6:565-575. 10.1038/nrn1703, 15959466.
79. Hosie AM, Dunne EL, Harvey RJ, Smart TG. Zinc-mediated inhibition of GABA(A) receptors: discrete binding sites underlie subtype specificity. Nat Neurosci 2003, 6:362-369. 10.1038/nn1030, 12640458.
80. Sivilotti L, Woolf CJ. The contribution of GABA(A) and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord. J Neurophysiol 1994, 72:169-179.
81. Kontinen VK, Stanfa LC, Basu A, Dickenson AH. Electrophysiologic evidence for increased endogenous gabaergic but not glycinergic inhibitory tone in the rat spinal nerve ligation model of neuropathy. Anesthesiology 2001, 94:333-339. 10.1097/00000542-200102000-00024, 11176099.
82. Moore KA, Kohno T, Karchewski LA, Scholz J, Baba H, Woolf CJ. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci 2002, 22:6724-6731.
83. Ruscheweyh R, Sandkuhler J. Long-range oscillatory Ca2+ waves in rat spinal dorsal horn. Eur J Neurosci 2005, 22:1967-1976. 10.1111/j.1460-9568.2005.04393.x, 16262635.