Laminar compartmentalization of GABAA-receptor subtypes in the spinal cord: An immunohistochemical study

Journal of Neuroscience

Volumn 16, Issue 1, 1996, Pages 283-297

  Bohlhalter, Stephan ^a,b   Weinmann, Oliver ^a   Mohler, Hanns ^a   Fritschy, Jean Marc ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Allodynia; Benzodiazepines; Inhibitory neurotransmission; Motoneurons; Pain control; Receptor subtypes

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; RECEPTOR SUBTYPE; RECEPTOR SUBUNIT;

ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD; ANIMAL; ANTIBODY SPECIFICITY; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; IMMUNOLOGY; NERVE CELL; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

ANIMALS; ANTIBODY SPECIFICITY; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SPINAL CORD;

EID: 0029670815     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-01-00283.1996     Document Type: Article

References (73)

1. Barber RP, Vaughn JE, Roberts E (1982) The cytoarchitecture of GABAergic neurons in rat spinal cord. Brain Res 238:305-328.
2. Barber RP, Vaughn JE, Saito K, McLaughlin BJ, Roberts E (1978) GABAergic terminals are presynaptic to primary afferent terminals in the substantia gelatinosa of the rat spinal cord. Brain Res 141:35-55.
3. Barker JL, Nicoll RA (1972) γ-Aminobutyric acid: role in primary afferent depolarization. Science 176:1043-1045.
4. Benavides J, Peny B, Ruano D, Vitorica J, Scatton B (1993) Comparative autoradiographic distribution of central omega (benzodiazepine) modulatory site subtypes with high, intermediate and low affinity for zolpidem and alpidem. Brain Res 604:240-250.
5. A-receptor in rat brain. J Receptor Res 11:407-424.
6. Benke D, Fritschy JM, Trzeciak A, Bannworth W, Mohler H (1994) Distribution, prevalence, and drug binding profile of γ-amino-butyric acid type A receptor subtypes differing in the β-subunit variant. J Biol Chem 269:27100-27107.
7. A-receptors at GABAergic synaptic contacts demonstrated by triple immunofluorescence staining. Brain Res 642:59-69.
8. Cattaert D, El Manira A, Clarac F (1991) Direct evidence for presynaptic inhibitory mechanisms in crayfish sensory afferents. J Neurophysiol 67:610-624.
9. Clavier N, Lombard M, Besson J (1992) Benzodiazepines and pain: effects of midazolam on the activites of nociceptive non-specific dorsal horn neurons in the rat spinal cord. Pain 48:61-71.
10. Duggan A, Foong F (1985) Bicuculline and spinal inhibition produced by dorsal column stimulation in the cat. Pain 22:249-259.
11. Eccles JC, Schmidt R, Willis WD (1963) Pharmacological studies on presynaptic inhibition. J Physiol (Lond) 168:500-530.
12. Evers P, Uylings HBM (1994) Microwave-stimulated antigen retrieval is pH and temperature dependent. J Histochem Cytochem 42:1555-1563.
13. A/benzodiazepine receptor. J Cell Biol 110:2043-2048.
14. Faull R, Villiger J (1986) Benzodiazepine receptors in the human spinal cord: a detailed anatomical and pharmacological study. Neuroscience 17:791-802.
15. Fritschy JM, Benke D, Mertens S, Bächi T, Mohler H (1992) Five subtypes of type A γ-aminobutyric acid receptors identified in neurons by double and triple immunofluorescence staining with subunit-specific antibodies. Proc Natl Acad Sci USA 89:6726-6730.
16. A-receptor subtypes during postnatal development: an immunohistochemical study. J Neurosci 14:5302-5324.
17. A-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154-194.
18. A receptor γ subunit mRNA in the rat dorsal root ganglion cells. Mol Brain Res 12:335-338.
19. A-receptor subtypes: differential associations of the α1-and α3-subunits with serotonergic and GABAergic neurons. Neuroscience 54:881-892.
20. A-receptor subtypes in cholinergic and parvalbumin-positive neurons of the rat and marmoset medial-septum-diagonal band complex. Neuroscience 65:101-117.
21. Gmelin G, Zimmermann M (1983) Effects of γ-aminobutyrate and bicuculline on primary afferent depolarization of cutaneous fibres in the cat spinal cord. Neuroscience 10:869-874.
22. A-receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J Comp Neurol 353:553-571.
23. Holstege JC (1991) Ultrastructural evidence for GABAergic brainstem projections to spinal motoneurons in the rat. J Neurosci 11:159-167.
24. Hunt SP (1983) Cytochemistry of the spinal cord. In: Chemical neuroanatomy (Emson PC, ed), pp 53-84. New York: Raven.
25. Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577-580.
26. Jones BE, Holmes CJ, Rodrigues-Veiga E, Mainville L (1991) GABA-synthesizing neurons in the medulla: their relationship to serotonin-containing and spinally projecting neurons in the rat. J Comp Neurol 313:349-367.
27. Liu H, Llewellyn-Smith IJ, Pilowsky P, Basbaum AI (1992) Ultrastructural evidence for GABA-mediated disinhibitory circuits in the spinal cord of the cat. Neurosci Lett 138:183-187.
28. A receptor subunit mRNAs in rat spinal cord and dorsal root ganglia. J Comp Neurol 338:337-359.
29. A receptor channels. Annu Rev Neurosci 17:569-602.
30. Magoul R, Onteniente B, Geffard M, Calas A (1987) Anatomical distribution and ultrastructural organization of the GABAergic system in the rat spinal cord. An immunocytochemical study using anti-GABA antibodies. Neuroscience 20:1001-1009.
31. A-receptor: drug binding profile and distribution of receptors containing the α2-subunit in situ. J Receptor Res 13:467-477.
32. A receptor subtypes immunopurified from rat brain with α subunit-specific antibodies have unique pharmacological properties. Neuron 7:667-676.
33. Melzack R, Wall PD (1965) Pain mechanism: a new theory. Science 150:971-979.
34. A-receptor populations with novel subunit combination and drug binding profiles identified in brain by α5- and δ-subunit specific immunopurification. J Biol Chem 268:5965-5973.
35. A-receptors and anxiety: from neurobiology to treatment (Biggio G, Sanna E, Costa A, eds), pp 41-56. New York: Raven.
36. Molander CV, Xu Q, Grant G (1984) The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133-141.
37. Molander C, Xu Q, Rivero-Melian C, Grant G (1989) Cytoarchitectonic organization of the spinal cord in the rat: II. The cervical and upper thoracic cord. J Comp Neurol 289:375-385.
38. Nistri A (1983) Spinal cord pharmacology of GABA and chemically related amino acids. In: Handbook of the spinal cord. Vol. I: Pharmacology (Davidoff RE, ed), pp 45-104. New York: Marcel Dekker.
39. A-receptor subunit mRNAs in neurons of the rat spinal cord and dorsal root ganglia. Neuroscience 42:497-507.
40. A-receptor subunits in the rat CNS. J Comp Neurol 326:193-216.
41. Pole P (1982) Enhancement of GABAergic inhibition: a mechanism of action of benzodiazepines, phenobarbital, valproate and L-cycloserine in the cat spinal cord. Electroencephal Clin Neurophysiol Suppl 36:188-198.
42. A-benzodiazepine receptors produced in transfected cells. Science 245:1389-1392.
43. A-receptor α5-subunit creates novel type II benzodiazepine receptor pharmacology. J Neurochem 54:1802-1804.
44. A receptor subunit composition on the action of allosteric modulators of γ-aminobutyric acid-gated Cl currents. Mol Pharmacol 39:691-696.
45. Quevedo J, Eguibar JR, Jimenez P, Rudomin P (1992) Differential action of (-)-baclofen on the primary afferent depolarization produced by segmental and descending inputs. Exp Brain Res 91:29-45.
46. Reichling D, Basbaum AI (1990) Contribution of brainstem GABAergic circuitry to descending antinociceptive controls: I. GABA-immunoreactive projection neurons in the periaqueductal gray and nucleus raphe magnus. J Comp Neurol 302:370-377.
47. Rodgers RJ, Randall JI (1987) Benzodiazepine ligands, nociception and defeat analgesia in male mice. Psychopharmacology 91:305-315.
48. A receptor channels of mouse spinal neurones in culture. J Physiol (Lond) 475:69-82.
49. Rosland F, Hunskaar S, Hole K (1987) The effect of diazepam on nociception in mice. Pharmacol Toxicol 61:111-115.
50. A/benzodiazepine receptor complex in the rat nervous system. J Neurochem 58:485-493.
51. Santi MR, Cox DH, Guidotti A (1988) Heterogeneity of γ-aminobutyric acid/benzodiazepine/β-carboline receptor complex in rat spinal cord. J Neurochem 50:1080-1086.
52. Schneider S, Fyffe R (1992) Involvement of GABA and glycine in recurrent inhibition of spinal motoneurons. J Neurophysiol 68:397-406.
53. A receptors and benzodiazepine receptors in the brain shown by monoclonal antibodies. Nature 314:168-171.
54. Schoeffler P, Auroy P, Bazin JE, Taxi J, Woda A (1991) Subarachnoid midazolam: histologic study in rats and report of its effect on chronic pain in humans. Reg Anesth 16:329-332.
55. Shi SR, Imam SA, Young L, Cote RJ, Taylor CR (1995) Antigen retrieval immunohistochemistry under the influence of pH using monoclonal antibodies. J Histochem Cytochem 43:193-201
56. A and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord. J Neurophysiol 72:169-179.
57. Sluka KA, Willis WD, Westlund KN (1993) Joint inflammation and hyperalgesia are reduced by bicuculline. NeuroReport 5:109-112.
58. B receptor antagonist in rats. J Pharmacol Exp Ther 271:76-82.
59. B receptors in presynaptic inhibition of Ia EPSPs in cat spinal motoneurones. J Physiol (Lond) 447:675-692.
60. Sumida T, Tagami M, Ide Y, Nagase M, Sekiyama H, Hanaoka K (1995) Intravenous midazolam suppresses noxiously evoked activity of spinal wide dynamic range neurons in cats. Anesth Analg 80:58-63.
61. Todd AJ, Spike RC (1993) The localization of classical transmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn. Prog Neurobiol 41:609-645.
62. Todd AJ, Sullivan AC (1990) Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 296:496-505.
63. Villiger JW (1984) CL 218,872 binding to benzodiazepine receptors in rat spinal cord: modulation by γ-aminobutyric acid and evidence for receptor heterogeneity. J Neurochem 43:903-905.
64. A receptors and benzodiazepine receptors in the human spinal cord: an autoradiographic and immunohistochemical study at the light and electron microscopic levels. Neuroscience 39:361-385.
65. Wall PD (1980) The substantia gelatinosa. A gate control mechanism set across sensory pathway. Trends Neurosci 3:221-224.
66. Willcockson WS, Chung JM, Hori Y, Lee KH, Willis WD (1984) Effects of iontophoretically released amino acids and amines on primate spinothalamic tract cells. J Neurosci 4:732-740.
67. A-receptor subunit mRNA in rat lumbar spinal cord. Mol Brain Res 10:179-183.
68. A-receptor channels: from subunits to functional entities. Curr Opin Neurobiol 2:263-269.
69. Woolf CJ, Doubell TP (1994) The pathophysiology of chronic pain - increased sensitivity to low threshold aβ-fiber inputs. Curr Opin Neurobiol 4:525-534.
70. Yaksh T (1989) 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 37:111-123.
71. Yamamoto T, Yaksh TL (1993) Effects of intrathecal strychnine and bicuculline on nerve compression-induced thermal hyperalgesia and selective antagonism by MK-801. Pain 54:79-84.
72. Young WS, Kuhar MJ (1980) Radiohistochemical localization of benzodiazepine receptors in rat brain. J Pharmacol Exp Ther 212:337-346.
73. A-benzodiazepine receptors by immunoaffinity chromatography. FEBS Lett 284:15-18.