Serotonergic modulation of spinal sensory circuits

Current Topics in Medicinal Chemistry

Volumn 6, Issue 18, 2006, Pages 1987-1996

  Lopez Garcia, José A ^a  

^a UNIVERSITY OF ALCALÁ   (Spain)

Author keywords

Analgesia; Dendrites; Dorsal horn neurones; NMDA transmission; Primary afferent depolarisation (PAD)

Indexed keywords

1 (2 METHOXYPHENYL) 4 (4 PHTHALIMIDOBUTYL)PIPERAZINE; 1 (3 CHLOROPHENYL)BIGUANIDE; 2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 4 IODO 2,5 DIMETHOXYAMPHETAMINE; 5 CARBAMOYLTRYPTAMINE; 5 METHOXY 3 (1,2,3,6 TETRAHYDRO 4 PYRIDYL) 1H INDOLE; ALPHA METHYLSEROTONIN; CAPSAICIN; CARRAGEENAN; CITALOPRAM; CYANOPINDOLOL; EXCITATORY AMINO ACID; F 13640; KETANSERIN; METITEPINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N TERT BUTYL 3 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL] 2 PHENYLPROPIONAMIDE; NEUROTRANSMITTER; RITANSERIN; SEROTONIN; SEROTONIN 1 RECEPTOR; SEROTONIN 1A AGONIST; SEROTONIN 2 RECEPTOR; SEROTONIN 3 ANTAGONIST; SEROTONIN 3 RECEPTOR; SEROTONIN UPTAKE INHIBITOR; SUMATRIPTAN; TROPISETRON; UNCLASSIFIED DRUG;

ADRENERGIC SYSTEM; ALLODYNIA; ANALGESIA; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; DRUG ANTAGONISM; DRUG RECEPTOR BINDING; ELECTROSTIMULATION; HYPERALGESIA; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR RECORDING; MOLECULAR INTERACTION; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE ENDING; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NERVOUS SYSTEM FUNCTION; NEUROPATHIC PAIN; NEUROTRANSMITTER RELEASE; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PRIMARY AFFERENT DEPOLARIZATION; PROTEIN FUNCTION; RECEPTOR OCCUPANCY; RECEPTOR SENSITIVITY; REGULATORY MECHANISM; REVIEW; SENSORY NERVE; SEROTONIN METABOLISM; SEROTONIN UPTAKE; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION; SOMATOSENSORY SYSTEM; SPINAL CORD DORSAL HORN; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION;

ANIMALS; NEURONS, AFFERENT; RECEPTORS, SEROTONIN; SEROTONIN; SPINAL CORD;

EID: 33749509564     PISSN: 15680266     EISSN: None     Source Type: Journal    
DOI: 10.2174/156802606778522159     Document Type: Review

References (82)

1. Millan, M.J. Descending Control of Pain. Prog. Neurobiol. 2002, 66, 355-474.
2. Hamon, M.; Collin, E.; Chantrel, D.; Daval, G.; Verge, D.; Burgoin, S.; Cesselin, F. Serotonin Receptors and the Modulation of Pain. In Serotonin and Pain; Besson, J.M.; Ed.; Elsevier Science Publishers B.V.: Berlin, 1990; pp 53-72.
3. Hamon M; Burgoing, S. Serotonin and its Receptors in Pain Control. In Novel Aspects of Pain Management: Opioides and Beyond; Sawinok,J. and Cowan, A. Eds; Wiley-Liss, Inc: 1999; pp 203-228.
4. Reynolds, D. V. Surgery in the Rat During Electrical Analgesia Induced by Focal Brain Stimulation. Science 1969, 164, 444-445.
5. Besson, J. M.; Chaouch, A. Peripheral and Spinal Mechanisms of Nociception. Physiol. Rev. 1987, 67, 67-186.
6. Willis, W. D. Anatomy and Physiology of Descending Control of Nociceptive Responses of Dorsal Horn Neurones: Comprehensive Review. Prog. Brain Res. 1988, 77, 1-29.
7. Basbaum, A. I.; Fields, H. L. Endogenous Pain Control Mechanisms: Review and Hypothesis. Ann. Neurol. 1978, 4, 451-462.
8. Roberts, M.H.T.; Llewelyn M.B. The Supraspinal Control of Pain. Bioscience 1982, 32, 587-594.
9. Le Bars, D. Serotonin and Pain. In Neuronal Serotonin; Osborne N.N.; Hamon, M.; Eds.; John Wiley and Sons Ltd.: Chichester, 1988; pp 171-229.
10. Porreca, F.; Ossipov, M.H.; Gebbart, G.F. Chronic Pain and Medullary Descending Facilitation. Trends Neurosci. 2002, 25, 319-325.
11. Ren, K.; Dubner, R. Descending Modulation in Persistent Pain: an update. Pain 2002, 100, 1-6.
12. Lima, D.; Almeida, A. The Medullary Dorsal Reticular Nucleus as a Pronociceptive Centre of the Pain Control System. Prog. Neurobiol. 2002, 66, 81-108.
13. Suzuki, R.; Rygh, L.J.; Dickenson, A.H. Bad News from the Brain: Descending 5-HT Pathways that Control Spinal Pain Processing. Trends Pharmacol. Sci. 2004, 25, 613-617.
14. Sorkin, L.S.; McAdoo, D.J.; Willis, W.D. Release of Serotonin Following Brainstem Stimulation: Correlation with Inhibition of Nociceptive Dorsal Horn Neurons. In Serotonin and Pain; Besson, J.M.; Ed.; Elsevier Science Publishers B.V.: Berlin, 1990; pp 105-115.
15. Zhang, Y.Q.; Gao, X.; Zhang, L.M.; Wu, G.C. The Release of Serotonin in Rat Spinal Dorsal Horn and Periaqueductal Gray Following Carrageenan Inflammation. Neuroreport 2000, 11, 3539-3543.
16. Willis, W.D.; Coggeshall, R.E. Sensory mechanisms of the spinal cord. Kluber Academic/Plenum Publishers: New York, 2004.
17. Jacobs, B.L.; Martin-Cora, F.J.; Fornal, C.A. Activity of Medullary Serotonergic Neurons in Freely Moving Animals. Brain Res. Rev. 2002, 40, 45-52.
18. Fields, H.L.; Heinricher, M.M.; Mason, P. Neurotransmitters in Nociceptive Modulatory Circuits. Annu. Rev. Neurosci. 1991, 14, 219-245.
19. Mason, P. Central Mechanisms of Pain Modulation. Curr. Opin. Neurobiol. 1999, 9, 436-441.
20. Ridet, J.L.; Rajaofetra, N.; Teilhac, J.R.; Geffard, M.; Privat, A. Evidence for Nonsynaptic Serotonergic and Noradrenergic Innervation of the Rat Dorsal Horn and Possible Involvement of Neuron-Glia Interactions. Neurosci, 1993, 52, 143-157.
21. Agnati, L.F.; Zoli, M.; Strömberg, I.; Fuxe, K. Intercellular Communication in the Brain: Wiring Versus Volume Transmission. Neurosci. 1995, 69, 711-726.
22. Headley, P.M.; Duggan, A.W.; Griersmith, B.T. Selective Reduction by Noradrenaline and 5-Hydroxytryptamine of Nociceptive Responses of Cat Dorsal Horn Neurones. Brain Res. 1978, 145, 185-189.
23. Lopez-Garcia, J.A.; King, A.E. Pre- and Post-Synaptic Actions of 5-Hydroxytryptamine in the Rat Lumbar Dorsal Horn In Vitro: Implications for Somatosensory Transmission. Eur. J. Neurosci. 1996, 8, 2188-2197.
24. Jordan, L.M.; Kenshalo, D.R.; Martin, R.F.; Haber, L.H.; Willis, W.D. Two Populations of Spinothalamic Tract Neurons with Opposite Responses to 5-Hydroxytryptamine. Brain Res. 1979 164, 342-346
25. Todd, A.J.; Millar, J. Receptive Fields and Responses to Ionophoretically Applied Noradrenaline and 5-Hydroxytryptamine of Units Recorded in Laminae I-III of Cat Dorsal Horn. Brain Res. 1993, 288, 159-167.
26. Alhaider, A.A.; Lei, S.Z.; Wilcox, G.L. Spinal 5-HT3 Receptor-mediated Antinociception: Possible Release of GABA. J. Neurosci. 1991, 11, 1881-1888.
27. Lu, Y; Pearl, E.R. Norepinephrine and Serotonin Effects in the Spinal Superficial Dorsal Horn Vary According to the Type of Neurone. Society for Neuroscience Abstracts, 2005, Abstract viewer 749.10.
28. Randic, M.; Yu, H.H. Effects of 5-Hydroxytryptamine and Bradykinin in Cat Dorsal Horn Neurones Activated by Noxious Stimuli. Brain Res. 1976, 111, 197-203.
29. Wallis, D. I.; Elliott, P. The Electrophysiology of 5-HT. In Serotonin: Molecular Biology, Receptors and Functional Effects; Fozard, J.R.; Saxena, P.R.; Eds.; Birkhauser Verlag Basel: Switzerland, 1991; pp 203-219.
30. Willis, W.D. Dorsal Root Potentials and Dorsal Root Reflexes: a Double-edged Sword. Exp. Brain Res. 1999, 124, 395-421.
31. Hentall, I.D.; Fields, H.L. Actions of Opiates, Substance P, and Serotonin on the Excitability of Primary Afferent Terminals and Observations on Interneuronal Activity in the Neonatal Rat's Dorsal Horn in Vitro. Neurosci. 1983, 9, 521-528.
32. Carstens, E.; Gilly, H.; Schreiber, H.; Zimmermann, M. Effects of Midbrain Stimulation and Iontophoretic Application of Serotonin, Noradrenaline, Morphine and GABA on Electrical Thresholds of Afferent C- and A- Fibre Terminals in Cat Spinal Cord. Neurosci. 1987, 21, 395-406.
33. 1A Receptors. Brain. Res. 1992, 585, 212-218.
34. Del Mar L.P.; Cardenas, C.G.; Scroggs, R.S. Serotonin Inhibits High-Threshold Ca2+ Channel Currents in Capsaicin-sensitive Acutely Isolated Adult Rat DRG Neurons. J. Neurophysiol. 1994, 72, 2551-2554.
35. 1A Receptors to N- and L-type Calcium Channels in C-like Rat Dorsal Root Ganglion Cells. J Neurophysiol. 1997, 77, 3284-3296.
36. Hori, Y.; Endo, K.; Takahashi, T. Long-lasting Synaptic Facilitation Induced by Serotonin in Superficial Dorsal Horn Neurones of the Rat Spinal Cord. J. Physiol. 1996, 492, 867-876.
37. Dougherty, P.M.; Palecek, J.; Paleckova, V.; Sorkin, L.S.; Willis, W.D. The role of NMDA and non-NMDA Excitatory amino acid receptors in the Excitation of Primate Spinothalamic Tract Neurons by Mechanical, Chemical, Thermal, and Electrical Stimuli. J. Neurosci. 1992, 12, 3025-3041.
38. King, A.E.; Lopez-Garcia, J.A. Excitatory Amino Acid Receptor-mediated Neurotransmission from Cutaneous Afferents in Rat Dorsal Horn in Vitro. J. Physiol. 1993, 472, 443-457.
39. Jordan, L.M.; Kenshalo, D.R.; Martin, R.F.; Habe, L.H.; Willis, W.D. Depression of Primate Spinothalamic Tract Neurons by Iontophoretic Application of 5-Hydroxytryptamine. Pain 1978, 5, 135-142.
40. Murase, K.; Randic, M.; Shirakasi, T.; Nakagawa, T.; Akaike, N. Serotonin Suppresses N-methyl-D-aspartate Responses in Acutely Isolated Spinal Dorsal Horn Neurons of the Rat. Brain Res. 1990, 525, 84-91.
41. Lopez-Garcia, J.A. Serotonergic Modulation of the Responses to Excitatory Amino Acids of Rat Dorsal Horn Neurons in Vitro: Implications for Somatosensory Transmission. Eur. J. Neurosci., 1998, 10, 1341-1349.
42. Chesnoy-Marchais, D.; Barhe, J.Y. Voltage-Dependent Block of the NMDA Responses by 5-HT Agonists in Ventral Spinal Cord Neurones. Br. J. Pharmacol., 1996, 117, 133-141.
43. Holohean, A.M.; Hackman, J.C. Mechanisms Intrinsic to 5-HT2B Receptor-Induced Potentiation of NMDA Receptor Responses in Frog Motoneurones. Br. J. Pharmacol., 2004, 143, 351-360.
44. Grudt, T.J.; Williams, J.T.; Travagli, R.A. Inhibition by 5-HT and Noradrenaline in Substantia Gelatinosa of Guinea-Pig Spinal Trigeminal Nucleus. J. Physiol., 1995, 485, 113-120.
45. Ma, R.C.; Dun, N.J. Excitation of Lateral Horn Neurons of the Neonatal Rat Spinal Cord by 5-Hydroxytryptamine. Devel. Brain Res. 1986, 24, 89-98.
46. 1 Receptor Subtypes. Brain Res. 1988, 456, 147-158.
47. 7 Receptors Mediate Depression of Spinal Nociceptive reflexes in vitro. Br. J. Pharmacol. 2002, 135, 935-942.
48. Arvieu, L.; Mauborgne, A; Bourgoin, S.; Oliver, C.; Feltz, P.; Hamon, M.; Cesselin, F. Sumatriptan Inhibits the Release of CGRP and Substance P from the Rat Spinal Cord. Neuroreport, 1996, 7, 1973-1976.
49. Hedo, G.; Ajubita, M.; Lopez-Garcia, J.A. Role of Serotonin 1A Receptors on the Modulation of Rat Spinal Mono-synaptic Reflexes in vitro. Neurosci. Lett. 2002, 334, 41-44.
50. You, H.J.; Colpaert, F.C.; Arendt-Nielsen, L. The Novel Analgesic and High-Efficacy 5-HT1A Receptor Agonist F13640 Inhibits Nociceptive Responses, Wind-up, and Afterdischarges in Spinal Neurons and Withdrawal reflexes. Exp. Neurol., 2005, 191, 174-183.
51. Ali, Z.; Wu, G.; Kozlov, A.; Barasi, S. The Actions of 5-HT1 Agonists and Antagonists on Nociceptive Processing in the Rat Spinal Cord: Results from Behavioural and Electrophysiological Studies. Brain Res. 1994, 661, 83-90.
52. Garraway, S.M.; Hochman, S. Pharmacological Characterization of Serotonin Receptor Subtypes Modulating Primary Afferent Input to Deep Dorsal Horn Neurons in the Neonatal Rat. Br. J. Pharmacol. 2001, 132, 1789-1798.
53. Manuel, N.A.; Wallis, D.I.; Crick, H. Ketanserin-sensitive Depressant Actions of 5-HT Receptor Agonists in the Neonatal Rat Spinal Cord. Br. J. Pharmacol. 1995, 116, 2647-2654.
54. Honda, M.; Tanabe, M.; Ono, M. Serotonergic Depression of Spinal Monosynaptic Transmission is Mediated by 5 HT1B Receptors. Eur. J. Pharmacol. 2003, 482, 155-161.
55. Honda, M.; Impida, K.; Tanabe, M.; Ono, H. Endogenously released 5-HT depresses the spinal monosynaptic reflex via 5-HT1D receptors. Eur. J. Pharmacol. 2004, 503, 55-61.
56. Elliott P.; Wallis, D.I. Serotonin and L-Norepinephrine as Mediators of Altered Excitability in Neonatal Rat Motoneurons Studied in Vitro. Neurosci. 1992, 47, 533-544.
57. Elliott P.; Wallis, D.I.; Foster, G.A.; Stringer, B.M. Ionic Mecahnisms Underlying Excitatory Effects of Serotonin on Embryonic Rat Motoneurns in Long-Term Culture. Neuroscience, 1999, 90, 1311-1323.
58. Honda, M.; Nishida, T.; Ono, H. Tricyclic Analoges Cyclobezaprine, Amitriptyline and Cyproheptadine Inhibit the Spinal Transmisi_aon Through 5-HT2 Receptors. Eur. J. Pharmacol. 2003, 458, 91-99.
59. Perrier, J.F.; Hounsgaard, J. 5-HT2 Receptors Promote Plateau Potentials in Turtle Spinal Motoneurons by Facilitating an L-type Calcium Current, J. Neurophysiol. 2003, 89, 954-959.
60. Crick, H.; Manuel, N.A.; Wallis, D.I. A novel 5-HT Receptor or a Combination of 5-HT Receptor Subtypes May Mediate Depression of a Spinal Monosypnaptic Reflex In Vitro. Neuropharmacol. 1994, 33, 897-904.
61. Machacek, D.W.; Garraway, S.M.; Shay, B.L.; Hochman, S. Serotonin 5-HT2 Receptor Activation Induces a Long-lasting Amplification of Spinal Reflex Actions in the Rat. J. Pysiol. 2001, 537, 201-7.
62. Peng, Y.B.; Lin, Q.; Willis, W.D. The Role of 5-HT3 Receptors in Periaqueductal Gray-induced Inhibition of Nociceptive Dorsal Horn Neurons in Rats. J. Pharmacol. Exp. Ther. 1996, 276, 116-124.
63. Khasabov, S.G.; Lopez-Garcia, J.A.; Asghar, A.U.R; King, A.E. Modulation of Afferent-evoked Neurotransmission by 5-HT3 Receptors in Young Rat Dorsal Horn Neurones in Vitro: a Putative Mechanism of 5-HT3 Induced Anti-nociception. Br. J. Pharmacol. 1999, 127, 843-852.
64. Ali, Z.; Wu, G.; Kozlov, A.; Barasi, S. The Role of 5-HT3 in Nociceptive Processing in the Rat Spinal Cord: Results from Behavioural and Electrophysiological Studies. Neurosci. Lett. 1996, 208, 203-207.
65. Yomono, H.S.; Suzuki, H.; Yoshioka, K. Serotonergic Fibers Induced a Long-lasting Inhibition of Monosynaptic Reflex in the Neonatal Rat Spinal Cord. Neurosci. 1992, 47, 521-531.
66. Wallis, D.I.; Wu, J.; Wang, X. Descending Inhibition in the Neonate Rat Spinal Cord is Mediated 5-HT. Neuropharmacol. 1993, 32, 73-83.
67. Martinez-Gomez, J.; Lopez-Garcia, J.A. Electrophysiological and Pharmacological Characterisation of Ascending Anterolatefal Axons in the in Vitro Mouse Spinal Cord. J. Neurosci. Methods 2005, 146, 84-90.
68. Woolf, C.J.; Salter, M.W. Neuronal Plasticity: Increasing the Gain in Pain. Science 2000, 288, 1765-1769.
69. Schaible, H.G.; Neugebauer, V.; Cervero, F.; Schmidt, R.F. Changes in Tonic Descending Inhibition of Spinal Neurons with Articular Input During the Development of Acute Arthritis in the Cat. J. Neurophysiol. 1991, 66, 1021-1032.
70. Zhang, Y.Q.; Gao, X.; Ji, G.C.; Huang, Y.L.; Wu, G.C.; Zhao, Z. Q. Expression of 5-HT1A Receptor mRNA in Rat Lumbar Spinal Dorsal Horn Neurons After Peripheral Inflammation. Pain 2002, 98, 287-295.
71. Colpaert, F.C.; Wu, W.P.; Hao, J.X.; Royer, I.; Sautel, F.; Wiesenfeld-Hallin, Z.; Xu, X.J. High-efficacy 5-HT1A Receptor Activation Causes a Curative-like Action on Allodynia in Rats with Spinal Cord Injury. Eur. J. Pharmacol. 2004, 497, 29-33.
72. Kayser, V.; Aubel, B.; Hamon, M.; Bourgoin, S. The Antimigraine 5-HT 1B/ 1D Receptor Agonists, Sumatriptan, Zolmitriptan and Dihydroergotamine, Attenuate Pain-related behaviour in a Rat Model of Trigeminal Neuropathic Pain. Br. J. Pharmacol. 2002, 137, 1287-1297.
73. Sanchez, A.; Niedbala, B.; Feria, M. Modulation of Neuropathic Pain in Rats by Intrathecally Injected Serotonergic Agonists. Neuroreport 1995, 6, 2585-2588.
74. Suzuki, R.; Morcuende, S.; Webber, M.; Hunt, S.P.; Dickenson, A.H. Superficial NK1-expressing Neurons Control Spinal Excitability Through Activation of Descending Pathways. Nat. Neurosci. 2002, 5, 1319-1326.
75. Cervero, F.; Laird, J.M. Mechanisms of Touch-evoked Pain (allodynia): A New Model. Pain 1997, 72, 288-289.
76. Zeitz, K.P.; Guy, N.; Malmberg, A.B.; Dirajlal, S.; Martin, W.J.; Sun, L.; Bonhaus, D.W.; Stucky, C. L.; Julius, D.; Basbaum, A.I. The 5-HT3 Subtype of Serotonin Receptor Contributes to Nociceptiye Processing Via a Novel Subset of Myelinated and Unmyelinated Nociceptors. J. Neurosc. 2002, 22, 1010-1019.
77. Bruce, J.C.; Oatway M.A.; Weaver L.C. Chronic Pain after Clip-compression Injury of the Rat Spinal Cord. Exp. Neurol. 2002, 178, 33-48.
78. Oatway, M.A.; Chen, Y.; Weaver, L.C. The 5-HT3 Receptor Facilitates at-level Mechanical Allodynia Following Spinal Cord Injury. Pain 2004, 110, 259-268.
79. Zhang, Y.; Yang, Z.; Gao, X.; Wu, G. The Role of 5-hydroxytryptamine1A and 5-hydroxytryptamine1B Receptors in Modulating Spinal Nociceptive Transmission in Normal and Carrageenan-injected Rats. Pain 2001, 92, 201-211.
80. Li, P.; Zhuo, M. Silent Glutamatergic Synapses and Nociception in Mammalian Spinal Cord. Nature 1998, 393, 695-698.
81. Kerchner, G.A.; Li, P.; Zhuo, M. Speaking Out of Turn: a Role for Silent Synapses in Pain. IUBMB Life 1999, 48, 251-256
82. Villalon, C.M.; Centurion, D.; Valdivia, L.F.; de Vries, P.; Saxena, P.R. Migraine: Pathophysiology, Pharmacology, Treatment and Future Trends. Curr. Vasc. Pharmacol., 2003, 1, 71-84.