Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Serotonergic Modulation of Nociceptive Circuits in Spinal Cord Dorsal Horn

Author(s): Rita Bardoni*

Volume 17, Issue 12, 2019

Page: [1133 - 1145] Pages: 13

DOI: 10.2174/1570159X17666191001123900

Price: $65

Abstract

Background: Despite the extensive number of studies performed in the last 50 years, aimed at describing the role of serotonin and its receptors in pain modulation at the spinal cord level, several aspects are still not entirely understood. The interpretation of these results is often complicated by the use of different pain models and animal species, together with the lack of highly selective agonists and antagonists binding to serotonin receptors.

Method: In this review, a search has been conducted on studies investigating the modulatory action exerted by serotonin on specific neurons and circuits in the spinal cord dorsal horn. Particular attention has been paid to studies employing electrophysiological techniques, both in vivo and in vitro.

Conclusion: The effects of serotonin on pain transmission in dorsal horn depend on several factors, including the type of receptors activated and the populations of neurons involved. Recently, studies performed by activating and/or recording from identified neurons have importantly contributed to the understanding of serotonergic modulation on dorsal horn circuits.

Keywords: Pain, serotonin receptors, dorsal horn, descending modulation, electrophysiology, synaptic transmission.

« Previous Next »
Graphical Abstract

[1]
Fields, H.L.; Heinricher, M.M.; Mason, P. Neurotransmitters in nociceptive modulatory circuits. Annu. Rev. Neurosci., 1991, 14, 219-245.
[http://dx.doi.org/10.1146/annurev.ne.14.030191.001251] [PMID: 1674413]
[2]
Kwiat, G.C.; Basbaum, A.I. The origin of brainstem noradrenergic and serotonergic projections to the spinal cord dorsal horn in the rat. Somatosens. Mot. Res., 1992, 9(2), 157-173.
[http://dx.doi.org/10.3109/08990229209144768] [PMID: 1354402]
[3]
Kato, G.; Yasaka, T.; Katafuchi, T.; Furue, H.; Mizuno, M.; Iwamoto, Y.; Yoshimura, M. Direct GABAergic and glycinergic inhibition of the substantia gelatinosa from the rostral ventromedial medulla revealed by in vivo patch-clamp analysis in rats. J. Neurosci., 2006, 26(6), 1787-1794.
[http://dx.doi.org/10.1523/JNEUROSCI.4856-05.2006] [PMID: 16467527]
[4]
Gautier, A.; Geny, D.; Bourgoin, S.; Bernard, J.F.; Hamon, M. Differential innervation of superficial versus deep laminae of the dorsal horn by bulbo-spinal serotonergic pathways in the rat. IBRO Rep., 2017, 2, 72-80.
[http://dx.doi.org/10.1016/j.ibror.2017.04.001] [PMID: 30135935]
[5]
Marlier, L.; Sandillon, F.; Poulat, P.; Rajaofetra, N.; Geffard, M.; Privat, A. Serotonergic innervation of the dorsal horn of rat spinal cord: light and electron microscopic immunocytochemical study. J. Neurocytol., 1991, 20(4), 310-322.
[http://dx.doi.org/10.1007/BF01235548] [PMID: 2051177]
[6]
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. Neuroscience, 1993, 52(1), 143-157.
[http://dx.doi.org/10.1016/0306-4522(93)90189-M] [PMID: 8381923]
[7]
Hentall, I.D.; Pinzon, A.; Noga, B.R. Spatial and temporal patterns of serotonin release in the rat’s lumbar spinal cord following electrical stimulation of the nucleus raphe magnus. Neuroscience, 2006, 142(3), 893-903.
[http://dx.doi.org/10.1016/j.neuroscience.2006.06.038] [PMID: 16890366]
[8]
Yoshimura, M.; Furue, H. Mechanisms for the anti-nociceptive actions of the descending noradrenergic and serotonergic systems in the spinal cord. J. Pharmacol. Sci., 2006, 101(2), 107-117.
[http://dx.doi.org/10.1254/jphs.CRJ06008X] [PMID: 16766858]
[9]
Attal, N.; Cruccu, G.; Baron, R.; Haanpää, M.; Hansson, P.; Jensen, T.S.; Nurmikko, T. EFNS guidelines on the pharmacological treatment of neuropathic pain: 2010 revision. Eur. J. Neurol., 2010, 17(9), 1113-e88.
[http://dx.doi.org/10.1111/j.1468-1331.2010.02999.x] [PMID: 20402746]
[10]
Hayashida, K.I.; Obata, H. Strategies to treat chronic pain and strengthen impaired descending noradrenergic inhibitory system. Int. J. Mol. Sci., 2019, 20(4), 822.
[http://dx.doi.org/10.3390/ijms20040822] [PMID: 30769838]
[11]
Marlier, L.; Teilhac, J.R.; Cerruti, C.; Privat, A. Autoradiographic mapping of 5-HT1, 5-HT1A, 5-HT1B and 5-HT2 receptors in the rat spinal cord. Brain Res., 1991, 550(1), 15-23.
[http://dx.doi.org/10.1016/0006-8993(91)90400-P] [PMID: 1832328]
[12]
Thor, K.B.; Nickolaus, S.; Helke, C.J. Autoradiographic localization of 5-hydroxytryptamine1A, 5-hydroxytryptamine1B and 5-hydroxytryptamine1C/2 binding sites in the rat spinal cord. Neuroscience, 1993, 55(1), 235-252.
[http://dx.doi.org/10.1016/0306-4522(93)90469-V] [PMID: 8350989]
[13]
Perrin, F.E.; Gerber, Y.N.; Teigell, M.; Lonjon, N.; Boniface, G.; Bauchet, L.; Rodriguez, J.J.; Hugnot, J.P.; Privat, A.M. Anatomical study of serotonergic innervation and 5-HT(1A) receptor in the human spinal cord. Cell Death Dis., 2011, 2 e218
[http://dx.doi.org/10.1038/cddis.2011.98] [PMID: 21993394]
[14]
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(3), 287-295.
[http://dx.doi.org/10.1016/S0304-3959(02)00026-X] [PMID: 12127030]
[15]
Wang, Y.Y.; Wei, Y.Y.; Huang, J.; Wang, W.; Tamamaki, N.; Li, Y.Q.; Wu, S.X. Expression patterns of 5-HT receptor subtypes 1A and 2A on GABAergic neurons within the spinal dorsal horn of GAD67-GFP knock-in mice. J. Chem. Neuroanat., 2009, 38(1), 75-81.
[http://dx.doi.org/10.1016/j.jchemneu.2009.04.003] [PMID: 19409978]
[16]
Daval, G.; Vergé, D.; Basbaum, A.I.; Bourgoin, S.; Hamon, M. Autoradiographic evidence of serotonin1 binding sites on primary afferent fibres in the dorsal horn of the rat spinal cord. Neurosci. Lett., 1987, 83(1-2), 71-76.
[http://dx.doi.org/10.1016/0304-3940(87)90218-7] [PMID: 3441302]
[17]
Laporte, A.M.; Fattaccini, C.M.; Lombard, M.C.; Chauveau, J.; Hamon, M. Effects of dorsal rhizotomy and selective lesion of serotonergic and noradrenergic systems on 5-HT1A, 5-HT1B, and 5-HT3 receptors in the rat spinal cord. J. Neural Transm. (Vienna), 1995, 100(3), 207-223.
[http://dx.doi.org/10.1007/BF01276459] [PMID: 8748667]
[18]
Pompeiano, M.; Palacios, J.M.; Mengod, G. Distribution and cellular localization of mRNA coding for 5-HT1A receptor in the rat brain: Correlation with receptor binding. J. Neurosci., 1992, 12(2), 440-453.
[http://dx.doi.org/10.1523/JNEUROSCI.12-02-00440.1992] [PMID: 1531498]
[19]
Pierce, P.A.; Xie, G.X.; Levine, J.D.; Peroutka, S.J. 5-Hydroxytryptamine receptor subtype messenger RNAs in rat peripheral sensory and sympathetic ganglia: A polymerase chain reaction study. Neuroscience, 1996, 70(2), 553-559.
[http://dx.doi.org/10.1016/0306-4522(95)00329-0] [PMID: 8848158]
[20]
Nicholson, R.; Small, J.; Dixon, A.K.; Spanswick, D.; Lee, K. Serotonin receptor mRNA expression in rat dorsal root ganglion neurons. Neurosci. Lett., 2003, 337(3), 119-122.
[http://dx.doi.org/10.1016/S0304-3940(02)01256-9] [PMID: 12536038]
[21]
Maeshima, T.; Ito, R.; Hamada, S.; Senzaki, K.; Hamaguchi-Hamada, K.; Shutoh, F.; Okado, N. The cellular localization of 5-HT2A receptors in the spinal cord and spinal ganglia of the adult rat. Brain Res., 1998, 797(1), 118-124.
[http://dx.doi.org/10.1016/S0006-8993(98)00360-6] [PMID: 9630559]
[22]
Okamoto, K.; Imbe, H.; Morikawa, Y.; Itoh, M.; Sekimoto, M.; Nemoto, K.; Senba, E. 5-HT2A receptor subtype in the peripheral branch of sensory fibers is involved in the potentiation of inflammatory pain in rats. Pain, 2002, 99(1-2), 133-143.
[http://dx.doi.org/10.1016/S0304-3959(02)00070-2] [PMID: 12237191]
[23]
Van Steenwinckel, J.; Noghero, A.; Thibault, K.; Brisorgueil, M.J.; Fischer, J.; Conrath, M. The 5-HT2A receptor is mainly expressed in nociceptive sensory neurons in rat lumbar dorsal root ganglia. Neuroscience, 2009, 161(3), 838-846.
[http://dx.doi.org/10.1016/j.neuroscience.2009.03.087] [PMID: 19362128]
[24]
Doly, S.; Madeira, A.; Fischer, J.; Brisorgueil, M.J.; Daval, G.; Bernard, R.; Vergé, D.; Conrath, M. The 5-HT2A receptor is widely distributed in the rat spinal cord and mainly localized at the plasma membrane of postsynaptic neurons. J. Comp. Neurol., 2004, 472(4), 496-511.
[http://dx.doi.org/10.1002/cne.20082] [PMID: 15065122]
[25]
Maxishima, M.; Shiga, T.; Shutoh, F.; Hamada, S.; Maeshima, T.; Okado, N. Serotonin 2A receptor-like immunoreactivity is detected in astrocytes but not in oligodendrocytes of rat spinal cord. Brain Res., 2001, 889(1-2), 270-273.
[http://dx.doi.org/10.1016/S0006-8993(00)03150-4] [PMID: 11166718]
[26]
Millan, M.J. Descending control of pain. Prog. Neurobiol., 2002, 66(6), 355-474.
[http://dx.doi.org/10.1016/S0301-0082(02)00009-6] [PMID: 12034378]
[27]
Pompeiano, M.; Palacios, J.M.; Mengod, G. Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res. Mol. Brain Res., 1994, 23(1-2), 163-178.
[http://dx.doi.org/10.1016/0169-328X(94)90223-2] [PMID: 8028479]
[28]
Fonseca, M.I.; Ni, Y.G.; Dunning, D.D.; Miledi, R. Distribution of serotonin 2A, 2C and 3 receptor mRNA in spinal cord and medulla oblongata. Brain Res. Mol. Brain Res., 2001, 89(1-2), 11-19.
[http://dx.doi.org/10.1016/S0169-328X(01)00049-3] [PMID: 11311971]
[29]
Ren, L.Q.; Wienecke, J.; Chen, M.; Møller, M.; Hultborn, H.; Zhang, M. The time course of serotonin 2C receptor expression after spinal transection of rats: An immunohistochemical study. Neuroscience, 2013, 236, 31-46.
[http://dx.doi.org/10.1016/j.neuroscience.2012.12.063] [PMID: 23337537]
[30]
Kidd, E.J.; Laporte, A.M.; Langlois, X.; Fattaccini, C.M.; Doyen, C.; Lombard, M.C.; Gozlan, H.; Hamon, M. 5-HT3 receptors in the rat central nervous system are mainly located on nerve fibres and terminals. Brain Res., 1993, 612(1-2), 289-298.
[http://dx.doi.org/10.1016/0006-8993(93)91674-H] [PMID: 8330206]
[31]
Tecott, L.H.; Maricq, A.V.; Julius, D. Nervous system distribution of the serotonin 5-HT3 receptor mRNA. Proc. Natl. Acad. Sci. USA, 1993, 90(4), 1430-1434.
[http://dx.doi.org/10.1073/pnas.90.4.1430] [PMID: 8434003]
[32]
Kia, H.K.; Miquel, M.C.; McKernan, R.M.; Laporte, A.M.; Lombard, M.C.; Bourgoin, S.; Hamon, M.; Vergé, D. Localization of 5-HT3 receptors in the rat spinal cord: immunohistochemistry and in situ hybridization. Neuroreport, 1995, 6(2), 257-261.
[http://dx.doi.org/10.1097/00001756-199501000-00008] [PMID: 7756605]
[33]
Morales, M.; Battenberg, E.; Bloom, F.E. Distribution of neurons expressing immunoreactivity for the 5HT3 receptor subtype in the rat brain and spinal cord. J. Comp. Neurol., 1998, 402(3), 385-401.
[http://dx.doi.org/10.1002/(SICI)1096-9861(19981221)402:3<385:AID-CNE7>3.0.CO;2-Q] [PMID: 9853906]
[34]
Conte, D.; Legg, E.D.; McCourt, A.C.; Silajdzic, E.; Nagy, G.G.; Maxwell, D.J. Transmitter content, origins and connections of axons in the spinal cord that possess the serotonin (5-hydroxytryptamine) 3 receptor. Neuroscience, 2005, 134(1), 165-173.
[http://dx.doi.org/10.1016/j.neuroscience.2005.02.013] [PMID: 15975728]
[35]
Tsuchiya, M.; Yamazaki, H.; Hori, Y. Pre-enkephalinergic neurons express 5-HT3 receptors in the spinal cord dorsal horn: Single cell RT-PCR analysis. Neuroreport, 1999, 10(13), 2749-2753.
[http://dx.doi.org/10.1097/00001756-199909090-00010] [PMID: 10511434]
[36]
Huang, J.; Wang, Y.Y.; Wang, W.; Li, Y.Q.; Tamamaki, N.; Wu, S.X. 5-HT(3A) receptor subunit is expressed in a subpopulation of GABAergic and enkephalinergic neurons in the mouse dorsal spinal cord. Neurosci. Lett., 2008, 441(1), 1-6.
[http://dx.doi.org/10.1016/j.neulet.2008.04.105] [PMID: 18586398]
[37]
Al Ghamdi, K.S.; Polgár, E.; Todd, A.J. Soma size distinguishes projection neurons from neurokinin 1 receptor-expressing interneurons in lamina I of the rat lumbar spinal dorsal horn. Neuroscience, 2009, 164(4), 1794-1804.
[http://dx.doi.org/10.1016/j.neuroscience.2009.09.071] [PMID: 19800942]
[38]
Pierce, P.A.; Xie, G.X.; Meuser, T.; Peroutka, S.J. 5-Hydroxytryptamine receptor subtype messenger RNAs in human dorsal root ganglia: a polymerase chain reaction study. Neuroscience, 1997, 81(3), 813-819.
[http://dx.doi.org/10.1016/S0306-4522(97)00235-2] [PMID: 9316030]
[39]
Meuser, T.; Pietruck, C.; Gabriel, A.; Xie, G.X.; Lim, K.J.; Pierce Palmer, P. 5-HT7 receptors are involved in mediating 5-HT-induced activation of rat primary afferent neurons. Life Sci., 2002, 71(19), 2279-2289.
[http://dx.doi.org/10.1016/S0024-3205(02)02011-8] [PMID: 12215375]
[40]
Doly, S.; Fischer, J.; Brisorgueil, M.J.; Vergé, D.; Conrath, M. Pre- and postsynaptic localization of the 5-HT7 receptor in rat dorsal spinal cord: immunocytochemical evidence. J. Comp. Neurol., 2005, 490(3), 256-269.
[http://dx.doi.org/10.1002/cne.20667] [PMID: 16082681]
[41]
Brenchat, A.; Nadal, X.; Romero, L.; Ovalle, S.; Muro, A.; Sánchez-Arroyos, R.; Portillo-Salido, E.; Pujol, M.; Montero, A.; Codony, X.; Burgueño, J.; Zamanillo, D.; Hamon, M.; Maldonado, R.; Vela, J.M. Pharmacological activation of 5-HT7 receptors reduces nerve injury-induced mechanical and thermal hypersensitivity. Pain, 2010, 149(3), 483-494.
[http://dx.doi.org/10.1016/j.pain.2010.03.007] [PMID: 20399562]
[42]
Basbaum, A.I.; Fields, H.L. Endogenous pain control mechanisms: review and hypothesis. Ann. Neurol., 1978, 4(5), 451-462.
[http://dx.doi.org/10.1002/ana.410040511] [PMID: 216303]
[43]
Hammond, D.L.; Yaksh, T.L. Antagonism of stimulation-produced antinociception by intrathecal administration of methysergide or phentolamine. Brain Res., 1984, 298(2), 329-337.
[http://dx.doi.org/10.1016/0006-8993(84)91432-X] [PMID: 6326954]
[44]
el-Yassir, N.; Fleetwood-Walker, S.M.A.A. 5-HT1-type receptor mediates the antinociceptive effect of nucleus raphe magnus stimulation in the rat. Brain Res., 1990, 523(1), 92-99.
[http://dx.doi.org/10.1016/0006-8993(90)91639-X] [PMID: 2207694]
[45]
Zemlan, F.P.; Murphy, A.Z.; Behbehani, M.M. 5-HT1A receptors mediate the effect of the bulbospinal serotonin system on spinal dorsal horn nociceptive neurons. Pharmacology, 1994, 48(1), 1-10.
[http://dx.doi.org/10.1159/000139156] [PMID: 8309982]
[46]
Cui, M.; Feng, Y.; McAdoo, D.J.; Willis, W.D. Periaqueductal gray stimulation-induced inhibition of nociceptive dorsal horn neurons in rats is associated with the release of norepinephrine, serotonin, and amino acids. J. Pharmacol. Exp. Ther., 1999, 289(2), 868-876.
[PMID: 10215665]
[47]
Sorkin, L.S.; McAdoo, D.J.; Willis, W.D. Raphe magnus stimulation-induced antinociception in the cat is associated with release of amino acids as well as serotonin in the lumbar dorsal horn. Brain Res, 1993, 618, 95-108.
[48]
Zhuo, M.; Gebhart, G.F. Characterization of descending inhibition and facilitation from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Pain, 1990, 42(3), 337-350.
[http://dx.doi.org/10.1016/0304-3959(90)91147-B] [PMID: 1979161]
[49]
Buhler, A.V.; Choi, J.; Proudfit, H.K.; Gebhart, G.F. Neurotensin activation of the NTR1 on spinally-projecting serotonergic neurons in the rostral ventromedial medulla is antinociceptive. Pain, 2005, 114(1-2), 285-294.
[http://dx.doi.org/10.1016/j.pain.2004.12.031] [PMID: 15733655]
[50]
Cai, Y.Q.; Wang, W.; Hou, Y.Y.; Pan, Z.Z. Optogenetic activation of brainstem serotonergic neurons induces persistent pain sensitization. Mol. Pain, 2014, 10, 70.
[http://dx.doi.org/10.1186/1744-8069-10-70] [PMID: 25410898]
[51]
Wei, F.; Dubner, R.; Zou, S.; Ren, K.; Bai, G.; Wei, D.; Guo, W. Molecular depletion of descending serotonin unmasks its novel facilitatory role in the development of persistent pain. J. Neurosci., 2010, 30(25), 8624-8636.
[http://dx.doi.org/10.1523/JNEUROSCI.5389-09.2010] [PMID: 20573908]
[52]
Zhao, Z.Q.; Chiechio, S.; Sun, Y.G.; Zhang, K.H.; Zhao, C.S.; Scott, M.; Johnson, R.L.; Deneris, E.S.; Renner, K.J.; Gereau, R.W., IV; Chen, Z.F. Mice lacking central serotonergic neurons show enhanced inflammatory pain and an impaired analgesic response to antidepressant drugs. J. Neurosci., 2007, 27(22), 6045-6053.
[http://dx.doi.org/10.1523/JNEUROSCI.1623-07.2007] [PMID: 17537976]
[53]
Zhang, Z.; Cai, Y.Q.; Zou, F.; Bie, B.; Pan, Z.Z. Epigenetic suppression of GAD65 expression mediates persistent pain. Nat. Med., 2011, 17(11), 1448-1455.
[http://dx.doi.org/10.1038/nm.2442] [PMID: 21983856]
[54]
Wang, J.K. Antinociceptive effect of intrathecally administered serotonin. Anesthesiology, 1977, 47(3), 269-271.
[http://dx.doi.org/10.1097/00000542-197709000-00007] [PMID: 578085]
[55]
Hylden, J.L.; Wilcox, G.L. Intrathecal serotonin in mice: Analgesia and inhibition of a spinal action of substance P. Life Sci., 1983, 33(8), 789-795.
[http://dx.doi.org/10.1016/0024-3205(83)90785-3] [PMID: 6193388]
[56]
Schmauss, C.; Hammond, D.L.; Ochi, J.W.; Yaksh, T.L. Pharmacological antagonism of the antinociceptive effects of serotonin in the rat spinal cord. Eur. J. Pharmacol., 1983, 90(4), 349-357.
[http://dx.doi.org/10.1016/0014-2999(83)90556-3] [PMID: 6688398]
[57]
Xu, W.; Qiu, X.C.; Han, J.S. Serotonin receptor subtypes in spinal antinociception in the rat. J. Pharmacol. Exp. Ther., 1994, 269(3), 1182-1189.
[PMID: 8014862]
[58]
Eide, P.K.; Joly, N.M.; Hole, K. The role of spinal cord 5-HT1A and 5-HT1B receptors in the modulation of a spinal nociceptive reflex. Brain Res., 1990, 536(1-2), 195-200.
[http://dx.doi.org/10.1016/0006-8993(90)90025-7] [PMID: 2150769]
[59]
Nadeson, R.; Goodchild, C.S. Antinociceptive role of 5-HT1A receptors in rat spinal cord. Br. J. Anaesth., 2002, 88(5), 679-684.
[http://dx.doi.org/10.1093/bja/88.5.679] [PMID: 12067006]
[60]
Colpaert, F.C.; Tarayre, J.P.; Koek, W.; Pauwels, P.J.; Bardin, L.; Xu, X.J.; Wiesenfeld-Hallin, Z.; Cosi, C.; Carilla-Durand, E.; Assié, M.B.; Vacher, B. Large-amplitude 5-HT1A receptor activation: A new mechanism of profound, central analgesia. Neuropharmacology, 2002, 43(6), 945-958.
[http://dx.doi.org/10.1016/S0028-3908(02)00119-3] [PMID: 12423664]
[61]
Bardin, L.; Colpaert, F.C. Role of spinal 5-HT(1A) receptors in morphine analgesia and tolerance in rats. Eur. J. Pain, 2004, 8(3), 253-261.
[http://dx.doi.org/10.1016/j.ejpain.2003.09.002] [PMID: 15109976]
[62]
Bonnefont, J.; Chapuy, E.; Clottes, E.; Alloui, A.; Eschalier, A. Spinal 5-HT1A receptors differentially influence nociceptive processing according to the nature of the noxious stimulus in rats: Effect of WAY-100635 on the antinociceptive activities of paracetamol, venlafaxine and 5-HT. Pain, 2005, 114(3), 482-490.
[http://dx.doi.org/10.1016/j.pain.2005.01.019] [PMID: 15777873]
[63]
Kim, J.M.; Jeong, S.W.; Yang, J.; Lee, S.H.; Kim, W.M.; Jeong, S.; Bae, H.B.; Yoon, M.H.; Choi, J.I. Spinal 5-HT1A, not the 5-HT1B or 5-HT3 receptors, mediates descending serotonergic inhibition for late-phase mechanical allodynia of carrageenan-induced peripheral inflammation. Neurosci. Lett., 2015, 600, 91-97.
[http://dx.doi.org/10.1016/j.neulet.2015.05.058] [PMID: 26037417]
[64]
Buritova, J.; Larrue, S.; Aliaga, M.; Besson, J.M.; Colpaert, F. Effects of the high-efficacy 5-HT1A receptor agonist, F 13640 in the formalin pain model: A c-Fos study. Eur. J. Pharmacol., 2005, 514(2-3), 121-130.
[http://dx.doi.org/10.1016/j.ejphar.2005.03.016] [PMID: 15910798]
[65]
Kayser, V.; Elfassi, I.E.; Aubel, B.; Melfort, M.; Julius, D.; Gingrich, J.A.; Hamon, M.; Bourgoin, S. Mechanical, thermal and formalin-induced nociception is differentially altered in 5-HT1A-/-, 5-HT1B-/-, 5-HT2A-/-, 5-HT3A-/- and 5-HTT-/- knock-out male mice. Pain, 2007, 130(3), 235-248.
[http://dx.doi.org/10.1016/j.pain.2006.11.015] [PMID: 17250964]
[66]
Jennings, E.A.; Ryan, R.M.; Christie, M.J. Effects of sumatriptan on rat medullary dorsal horn neurons. Pain, 2004, 111(1-2), 30-37.
[http://dx.doi.org/10.1016/j.pain.2004.05.018] [PMID: 15327806]
[67]
Goadsby, P.J.; Akerman, S.; Storer, R.J. Evidence for postjunctional serotonin (5-HT1) receptors in the trigeminocervical complex. Ann. Neurol., 2001, 50(6), 804-807.
[http://dx.doi.org/10.1002/ana.10066] [PMID: 11761480]
[68]
Potrebic, S.; Ahn, A.H.; Skinner, K.; Fields, H.L.; Basbaum, A.I. Peptidergic nociceptors of both trigeminal and dorsal root ganglia express serotonin 1D receptors: implications for the selective antimigraine action of triptans. J. Neurosci., 2003, 23(34), 10988-10997.
[http://dx.doi.org/10.1523/JNEUROSCI.23-34-10988.2003] [PMID: 14645495]
[69]
Ahn, A.H.; Basbaum, A.I. Tissue injury regulates serotonin 1D receptor expression: Implications for the control of migraine and inflammatory pain. J. Neurosci., 2006, 26(32), 8332-8338.
[http://dx.doi.org/10.1523/JNEUROSCI.1989-06.2006] [PMID: 16899728]
[70]
Lucas-Osma, A.M.; Li, Y.; Murray, K.; Lin, S.; Black, S.; Stephens, M.J.; Ahn, A.H.; Heckman, C.J.; Fenrich, K.K.; Fouad, K.; Bennett, D.J. 5-HT1D receptors inhibit the monosynaptic stretch reflex by modulating C-fiber activity. J. Neurophysiol., 2019, 121(5), 1591-1608.
[http://dx.doi.org/10.1152/jn.00805.2018] [PMID: 30625007]
[71]
Sasaki, M.; Ishizaki, K.; Obata, H.; Goto, F. Effects of 5-HT2 and 5-HT3 receptors on the modulation of nociceptive transmission in rat spinal cord according to the formalin test. Eur. J. Pharmacol., 2001, 424(1), 45-52.
[http://dx.doi.org/10.1016/S0014-2999(01)01117-7] [PMID: 11470259]
[72]
Sasaki, M.; Obata, H.; Saito, S.; Goto, F. Antinociception with intrathecal alpha-methyl-5-hydroxytryptamine, a 5-hydroxytryptamine 2A/2C receptor agonist, in two rat models of sustained pain. Anesth. Analg., 2003, 96(4), 1072-1078.
[http://dx.doi.org/10.1213/01.ANE.0000050560.15341.A8] [PMID: 12651663]
[73]
Wattiez, A.S.; Pichon, X.; Dupuis, A.; Hernández, A.; Privat, A.M.; Aissouni, Y.; Chalus, M.; Pelissier, T.; Eschalier, A.; Marin, P.; Courteix, C. Disruption of 5-HT2A receptor-PDZ protein interactions alleviates mechanical hypersensitivity in carrageenan-induced inflammation in rats. PLoS One, 2013, 8(9)e74661
[http://dx.doi.org/10.1371/journal.pone.0074661] [PMID: 24058620]
[74]
Obata, H.; Saito, S.; Sasaki, M.; Ishizaki, K.; Goto, F. Antiallodynic effect of intrathecally administered 5-HT(2) agonists in rats with nerve ligation. Pain, 2001, 90(1-2), 173-179.
[http://dx.doi.org/10.1016/S0304-3959(00)00401-2] [PMID: 11166984]
[75]
Obata, H.; Saito, S.; Sakurazawa, S.; Sasaki, M.; Usui, T.; Goto, F. Antiallodynic effects of intrathecally administered 5-HT(2C) receptor agonists in rats with nerve injury. Pain, 2004, 108(1-2), 163-169.
[http://dx.doi.org/10.1016/j.pain.2003.12.019] [PMID: 15109520]
[76]
Nitanda, A.; Yasunami, N.; Tokumo, K.; Fujii, H.; Hirai, T.; Nishio, H. Contribution of the peripheral 5-HT 2A receptor to mechanical hyperalgesia in a rat model of neuropathic pain. Neurochem. Int., 2005, 47(6), 394-400.
[http://dx.doi.org/10.1016/j.neuint.2005.06.002] [PMID: 16051396]
[77]
Thibault, K.; Van Steenwinckel, J.; Brisorgueil, M.J.; Fischer, J.; Hamon, M.; Calvino, B.; Conrath, M. Serotonin 5-HT2A receptor involvement and Fos expression at the spinal level in vincristine-induced neuropathy in the rat. Pain, 2008, 140(2), 305-322.
[http://dx.doi.org/10.1016/j.pain.2008.09.006] [PMID: 18930597]
[78]
Van Steenwinckel, J.; Brisorgueil, M.J.; Fischer, J.; Vergé, D.; Gingrich, J.A.; Bourgoin, S.; Hamon, M.; Bernard, R.; Conrath, M. Role of spinal serotonin 5-HT2A receptor in 2′,3′-dideoxycytidine-induced neuropathic pain in the rat and the mouse. Pain, 2008, 137(1), 66-80.
[http://dx.doi.org/10.1016/j.pain.2007.08.014] [PMID: 17888573]
[79]
Glaum, S.R.; Proudfit, H.K.; Anderson, E.G. 5-HT3 receptors modulate spinal nociceptive reflexes. Brain Res., 1990, 510(1), 12-16.
[http://dx.doi.org/10.1016/0006-8993(90)90721-M] [PMID: 2322835]
[80]
Scott, J.A.; Wood, M.; Flood, P. The pronociceptive effect of ondansetron in the setting of P-glycoprotein inhibition. Anesth. Analg., 2006, 103(3), 742-746.
[http://dx.doi.org/10.1213/01.ane.0000228861.80314.22] [PMID: 16931690]
[81]
Paul, D.; Yao, D.; Zhu, P.; Minor, L.D.; Garcia, M.M. 5-hydroxytryptamine3 (5-HT3) receptors mediate spinal 5-HT antinociception: an antisense approach. J. Pharmacol. Exp. Ther., 2001, 298(2), 674-678.
[PMID: 11454930]
[82]
Horiuchi, H.; Ogata, T.; Morino, T.; Takeba, J.; Yamamoto, H. Serotonergic signaling inhibits hyperalgesia induced by spinal cord damage. Brain Res., 2003, 963(1-2), 312-320.
[http://dx.doi.org/10.1016/S0006-8993(02)04055-6] [PMID: 12560138]
[83]
Svensson, C.I.; Tran, T.K.; Fitzsimmons, B.; Yaksh, T.L.; Hua, X.Y. Descending serotonergic facilitation of spinal ERK activation and pain behavior. FEBS Lett., 2006, 580(28-29), 6629-6634.
[http://dx.doi.org/10.1016/j.febslet.2006.11.012] [PMID: 17113581]
[84]
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 nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. J. Neurosci., 2002, 22(3), 1010-1019.
[http://dx.doi.org/10.1523/JNEUROSCI.22-03-01010.2002] [PMID: 11826129]
[85]
Oatway, M.A.; Chen, Y.; Weaver, L.C. The 5-HT3 receptor facilitates at-level mechanical allodynia following spinal cord injury. Pain, 2004, 110(1-2), 259-268.
[http://dx.doi.org/10.1016/j.pain.2004.03.040] [PMID: 15275776]
[86]
Okazaki, R.; Namba, H.; Yoshida, H.; Okai, H.; Miura, T.; Kawamura, M. The antiallodynic effect of Neurotropin is mediated via activation of descending pain inhibitory systems in rats with spinal nerve ligation. Anesth. Analg., 2008, 107(3), 1064-1069.
[http://dx.doi.org/10.1213/ane.0b013e31817e7a59] [PMID: 18713930]
[87]
Peters, C.M.; Hayashida, K.; Ewan, E.E.; Nakajima, K.; Obata, H.; Xu, Q.; Yaksh, T.L.; Eisenach, J.C. Lack of analgesic efficacy of spinal ondansetron on thermal and mechanical hypersensitivity following spinal nerve ligation in the rat. Brain Res., 2010, 1352, 83-93.
[http://dx.doi.org/10.1016/j.brainres.2010.07.020] [PMID: 20637741]
[88]
Zuena, A.R.; Maftei, D.; Alemà, G.S.; Dal Moro, F.; Lattanzi, R.; Casolini, P.; Nicoletti, F. Multimodal antidepressant vortioxetine causes analgesia in a mouse model of chronic neuropathic pain. Mol. Pain, 2018. 141744806918808987
[http://dx.doi.org/10.1177/1744806918808987] [PMID: 30289053]
[89]
Brenchat, A.; Romero, L.; García, M.; Pujol, M.; Burgueño, J.; Torrens, A.; Hamon, M.; Baeyens, J.M.; Buschmann, H.; Zamanillo, D.; Vela, J.M. 5-HT7 receptor activation inhibits mechanical hypersensitivity secondary to capsaicin sensitization in mice. Pain, 2009, 141(3), 239-247.
[http://dx.doi.org/10.1016/j.pain.2008.11.009] [PMID: 19118950]
[90]
Viguier, F.; Michot, B.; Kayser, V.; Bernard, J.F.; Vela, J.M.; Hamon, M.; Bourgoin, S. GABA, but not opioids, mediates the anti-hyperalgesic effects of 5-HT7 receptor activation in rats suffering from neuropathic pain. Neuropharmacology, 2012, 63(6), 1093-1106.
[http://dx.doi.org/10.1016/j.neuropharm.2012.07.023] [PMID: 22820553]
[91]
Brenchat, A.; Zamanillo, D.; Hamon, M.; Romero, L.; Vela, J.M. Role of peripheral versus spinal 5-HT(7) receptors in the modulation of pain undersensitizing conditions. Eur. J. Pain, 2012, 16(1), 72-81.
[http://dx.doi.org/10.1016/j.ejpain.2011.07.004] [PMID: 21843960]
[92]
Viguier, F.; Michot, B.; Hamon, M.; Bourgoin, S. Multiple roles of serotonin in pain control mechanisms--implications of 5-HT7 and other 5-HT receptor types. Eur. J. Pharmacol., 2013, 716(1-3), 8-16.
[http://dx.doi.org/10.1016/j.ejphar.2013.01.074] [PMID: 23500207]
[93]
Rocha-González, H.I.; Meneses, A.; Carlton, S.M.; Granados-Soto, V. Pronociceptive role of peripheral and spinal 5-HT7 receptors in the formalin test. Pain, 2005, 117(1-2), 182-192.
[http://dx.doi.org/10.1016/j.pain.2005.06.011] [PMID: 16098671]
[94]
Amaya-Castellanos, E.; Pineda-Farias, J.B.; Castañeda-Corral, G.; Vidal-Cantú, G.C.; Murbartián, J.; Rocha-González, H.I.; Granados-Soto, V. Blockade of 5-HT7 receptors reduces tactile allodynia in the rat. Pharmacol. Biochem. Behav., 2011, 99(4), 591-597.
[http://dx.doi.org/10.1016/j.pbb.2011.06.005] [PMID: 21693130]
[95]
Todorovic, S.; Anderson, E.G. Serotonin preferentially hyperpolarizes capsaicin-sensitive C type sensory neurons by activating 5-HT1A receptors. Brain Res., 1992, 585(1-2), 212-218.
[http://dx.doi.org/10.1016/0006-8993(92)91209-W] [PMID: 1511304]
[96]
Robertson, B.; Bevan, S. Properties of 5-hydroxytryptamine3 receptor-gated currents in adult rat dorsal root ganglion neurones. Br. J. Pharmacol., 1991, 102(1), 272-276.
[http://dx.doi.org/10.1111/j.1476-5381.1991.tb12165.x] [PMID: 2043929]
[97]
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(5), 2551-2554.
[http://dx.doi.org/10.1152/jn.1994.72.5.2551] [PMID: 7884482]
[98]
Cardenas, C.G.; Del Mar, L.P.; Scroggs, R.S. Variation in serotonergic inhibition of calcium channel currents in four types of rat sensory neurons differentiated by membrane properties. J. Neurophysiol., 1995, 74(5), 1870-1879.
[http://dx.doi.org/10.1152/jn.1995.74.5.1870] [PMID: 8592180]
[99]
Cardenas, C.G.; Mar, L.P.; Vysokanov, A.V.; Arnold, P.B.; Cardenas, L.M.; Surmeier, D.J.; Scroggs, R.S. Serotonergic modulation of hyperpolarization-activated current in acutely isolated rat dorsal root ganglion neurons. J. Physiol., 1999, 518(Pt 2), 507-523.
[http://dx.doi.org/10.1111/j.1469-7793.1999.0507p.x] [PMID: 10381596]
[100]
Cardenas, L.M.; Cardenas, C.G.; Scroggs, R.S. 5HT increases excitability of nociceptor-like rat dorsal root ganglion neurons via cAMP-coupled TTX-resistant Na(+) channels. J. Neurophysiol., 2001, 86(1), 241-248.
[http://dx.doi.org/10.1152/jn.2001.86.1.241] [PMID: 11431505]
[101]
Rudomin, P.; Schmidt, R.F. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp. Brain Res., 1999, 129(1), 1-37.
[http://dx.doi.org/10.1007/s002210050933] [PMID: 10550500]
[102]
Bardoni, R.; Takazawa, T.; Tong, C.K.; Choudhury, P.; Scherrer, G.; Macdermott, A.B. Pre- and postsynaptic inhibitory control in the spinal cord dorsal horn. Ann. N. Y. Acad. Sci., 2013, 1279, 90-96.
[http://dx.doi.org/10.1111/nyas.12056] [PMID: 23531006]
[103]
Betelli, C.; MacDermott, A.B.; Bardoni, R. Transient, activity dependent inhibition of transmitter release from low threshold afferents mediated by GABAA receptors in spinal cord lamina III/IV. Mol. Pain, 2015, 11, 64.
[http://dx.doi.org/10.1186/s12990-015-0067-5] [PMID: 26463733]
[104]
Lopez-Garcia, J.A.; King, A.E. A novel methodology for simultaneous assessment of the effects of 5-hydroxytryptamine on primary afferent polarisation and synaptic transmission in rat dorsal horn neurones in vitro. J. Neurosci. Methods, 1996, 68(1), 1-6.
[http://dx.doi.org/10.1016/0165-0270(96)00037-4] [PMID: 8884606]
[105]
García-Ramírez, D.L.; Calvo, J.R.; Hochman, S.; Quevedo, J.N. Serotonin, dopamine and noradrenaline adjust actions of myelinated afferents via modulation of presynaptic inhibition in the mouse spinal cord. PLoS One, 2014, 9(2)e89999
[http://dx.doi.org/10.1371/journal.pone.0089999] [PMID: 24587177]
[106]
Khasabov, S.G.; Lopez-Garcia, J.A.; Asghar, A.U.; 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(4), 843-852.
[http://dx.doi.org/10.1038/sj.bjp.0702592] [PMID: 10433490]
[107]
Ito, A.; Kumamoto, E.; Takeda, M.; Shibata, K.; Sagai, H.; Yoshimura, M. Mechanisms for ovariectomy-induced hyperalgesia and its relief by calcitonin: participation of 5-HT1A-like receptor on C-afferent terminals in substantia gelatinosa of the rat spinal cord. J. Neurosci., 2000, 20(16), 6302-6308.
[http://dx.doi.org/10.1523/JNEUROSCI.20-16-06302.2000] [PMID: 10934282]
[108]
Abe, K.; Kato, G.; Katafuchi, T.; Tamae, A.; Furue, H.; Yoshimura, M. Responses to 5-HT in morphologically identified neurons in the rat substantia gelatinosa in vitro. Neuroscience, 2009, 159(1), 316-324.
[http://dx.doi.org/10.1016/j.neuroscience.2008.12.021] [PMID: 19141313]
[109]
Lu, Y.; Perl, E.R. Selective action of noradrenaline and serotonin on neurones of the spinal superficial dorsal horn in the rat. J. Physiol., 2007, 582(Pt 1), 127-136.
[http://dx.doi.org/10.1113/jphysiol.2007.131565] [PMID: 17463043]
[110]
Yasaka, T.; Tiong, S.Y.; Hughes, D.I.; Riddell, J.S.; Todd, A.J. Populations of inhibitory and excitatory interneurons in lamina II of the adult rat spinal dorsal horn revealed by a combined electrophysiological and anatomical approach. Pain, 2010, 151(2), 475-488.
[http://dx.doi.org/10.1016/j.pain.2010.08.008] [PMID: 20817353]
[111]
Dickie, A.C.; Bell, A.M.; Iwagaki, N.; Polgár, E.; Gutierrez-Mecinas, M.; Kelly, R.; Lyon, H.; Turnbull, K.; West, S.J.; Etlin, A.; Braz, J.; Watanabe, M.; Bennett, D.L.H.; Basbaum, A.I.; Riddell, J.S.; Todd, A.J. Morphological and functional properties distinguish the substance P and gastrin-releasing peptide subsets of excitatory interneuron in the spinal cord dorsal horn. Pain, 2019, 160(2), 442-462.
[http://dx.doi.org/10.1097/j.pain.0000000000001406] [PMID: 30247267]
[112]
Smith, K.M.; Boyle, K.A.; Mustapa, M.; Jobling, P.; Callister, R.J.; Hughes, D.I.; Graham, B.A. Distinct forms of synaptic inhibition and neuromodulation regulate calretinin-positive neuron excitability in the spinal cord dorsal horn. Neuroscience, 2016, 326, 10-21.
[http://dx.doi.org/10.1016/j.neuroscience.2016.03.058] [PMID: 27045594]
[113]
Fukushima, T.; Ohtsubo, T.; Tsuda, M.; Yanagawa, Y.; Hori, Y. Facilitatory actions of serotonin type 3 receptors on GABAergic inhibitory synaptic transmission in the spinal superficial dorsal horn. J. Neurophysiol., 2009, 102(3), 1459-1471.
[http://dx.doi.org/10.1152/jn.91160.2008] [PMID: 19369358]
[114]
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(Pt 3), 867-876.
[http://dx.doi.org/10.1113/jphysiol.1996.sp021352] [PMID: 8734996]
[115]
Jeong, H.J.; Mitchell, V.A.; Vaughan, C.W. Role of 5-HT(1) receptor subtypes in the modulation of pain and synaptic transmission in rat spinal superficial dorsal horn. Br. J. Pharmacol., 2012, 165(6), 1956-1965.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01685.x] [PMID: 21950560]
[116]
Xie, D.J.; Uta, D.; Feng, P.Y.; Wakita, M.; Shin, M.C.; Furue, H.; Yoshimura, M. Identification of 5-HT receptor subtypes enhancing inhibitory transmission in the rat spinal dorsal horn in vitro. Mol. Pain, 2012, 8, 58.
[http://dx.doi.org/10.1186/1744-8069-8-58] [PMID: 22906126]
[117]
Li, H.; Lang, B.; Kang, J.F.; Li, Y.Q. Serotonin potentiates the response of neurons of the superficial laminae of the rat spinal dorsal horn to gamma-aminobutyric acid. Brain Res. Bull., 2000, 52(6), 559-565.
[http://dx.doi.org/10.1016/S0361-9230(00)00297-5] [PMID: 10974497]
[118]
Tomoyose, O.; Kodama, D.; Ono, H.; Tanabe, M. Presynaptic inhibitory effects of fluvoxamine, a selective serotonin reuptake inhibitor, on nociceptive excitatory synaptic transmission in spinal superficial dorsal horn neurons of adult mice. J. Pharmacol. Sci., 2014, 126(2), 136-145.
[http://dx.doi.org/10.1254/jphs.14127FP] [PMID: 25252797]
[119]
Jordan, L.M.; Kenshalo, D.R., Jr; Martin, R.F.; Haber, L.H.; Willis, W.D. Depression of primate spinothalamic tract neurons by iontophoretic application of 5-hydroxytryptamine. Pain, 1978, 5(2), 135-142.
[http://dx.doi.org/10.1016/0304-3959(78)90035-0] [PMID: 99715]
[120]
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(1), 185-189.
[http://dx.doi.org/10.1016/0006-8993(78)90809-0] [PMID: 638777]
[121]
el-Yassir, N.; Fleetwood-Walker, S.M.; Mitchell, R. Heterogeneous effects of serotonin in the dorsal horn of rat: the involvement of 5-HT1 receptor subtypes. Brain Res., 1988, 456(1), 147-158.
[http://dx.doi.org/10.1016/0006-8993(88)90356-3] [PMID: 2970278]
[122]
Liu, F.Y.; Qu, X.X.; Ding, X.; Cai, J.; Jiang, H.; Wan, Y.; Han, J.S.; Xing, G.G. Decrease in the descending inhibitory 5-HT system in rats with spinal nerve ligation. Brain Res., 2010, 1330, 45-60.
[123]
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., 1983, 288(1-2), 159-167.
[http://dx.doi.org/10.1016/0006-8993(83)90090-2] [PMID: 6661615]
[124]
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(1-2), 83-90.
[http://dx.doi.org/10.1016/0006-8993(94)91184-3] [PMID: 7834389]
[125]
Alhaider, A.A.; Lei, S.Z.; Wilcox, G.L. Spinal 5-HT3 receptor-mediated antinociception: Possible release of GABA. J. Neurosci., 1991, 11(7), 1881-1888.
[http://dx.doi.org/10.1523/JNEUROSCI.11-07-01881.1991] [PMID: 2066767]
[126]
Lin, Q.; Peng, Y.B.; Willis, W.D. Antinociception and inhibition from the periaqueductal gray are mediated in part by spinal 5-hydroxytryptamine(1A) receptors. J. Pharmacol. Exp. Ther., 1996, 276(3), 958-967.
[PMID: 8786576]
[127]
Gjerstad, J.; Tjolsen, A.; Hole, K. The effect of 5-HT1A receptor stimulation on nociceptive dorsal horn neurones in rats. Eur. J. Pharmacol., 1996, 318(2-3), 315-321.
[http://dx.doi.org/10.1016/S0014-2999(96)00819-9] [PMID: 9016920]
[128]
Gjerstad, J.; Tjølsen, A.; Hole, K. A dual effect of 5-HT1B receptor stimulation on nociceptive dorsal horn neurones in rats. Eur. J. Pharmacol., 1997, 335(2-3), 127-132.
[http://dx.doi.org/10.1016/S0014-2999(97)01183-7] [PMID: 9369364]
[129]
You, H.J.; Colpaert, F.C.; Arendt-Nielsen, L. The novel analgesic and high-efficacy 5-HT1A receptor agonist F 13640 inhibits nociceptive responses, wind-up, and after-discharges in spinal neurons and withdrawal reflexes. Exp. Neurol., 2005, 191(1), 174-183.
[http://dx.doi.org/10.1016/j.expneurol.2004.08.031] [PMID: 15589524]
[130]
Schwaller, F.; Kanellopoulos, A.H.; Fitzgerald, M. The developmental emergence of differential brainstem serotonergic control of the sensory spinal cord. Sci. Rep., 2017, 7(1), 2215.
[http://dx.doi.org/10.1038/s41598-017-02509-2] [PMID: 28533557]
[131]
Rahman, W.; Bannister, K.; Bee, L.A.; Dickenson, A.H. A pronociceptive role for the 5-HT2 receptor on spinal nociceptive transmission: an in vivo electrophysiological study in the rat. Brain Res., 2011, 1382, 29-36.
[http://dx.doi.org/10.1016/j.brainres.2011.01.057] [PMID: 21276431]
[132]
Liu, F.Y.; Xing, G.G.; Qu, X.X.; Xu, I.S.; Han, J.S.; Wan, Y. Roles of 5-hydroxytryptamine (5-HT) receptor subtypes in the inhibitory effects of 5-HT on C-fiber responses of spinal wide dynamic range neurons in rats. J. Pharmacol. Exp. Ther., 2007, 321(3), 1046-1053.
[http://dx.doi.org/10.1124/jpet.106.115204] [PMID: 17329553]
[133]
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(10), 2188-2197.
[http://dx.doi.org/10.1111/j.1460-9568.1996.tb00740.x] [PMID: 8921310]
[134]
Garraway, S.M.; Hochman, S. Modulatory actions of serotonin, norepinephrine, dopamine, and acetylcholine in spinal cord deep dorsal horn neurons. J. Neurophysiol., 2001, 86(5), 2183-2194.
[http://dx.doi.org/10.1152/jn.2001.86.5.2183] [PMID: 11698510]
[135]
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(8), 1789-1798.
[http://dx.doi.org/10.1038/sj.bjp.0703983] [PMID: 11309251]
[136]
Worsley, M.A.; Todd, A.J.; King, A.E. Serotoninergic-mediated inhibition of substance P sensitive deep dorsal horn neurons: a combined electrophysiological and morphological study in vitro. Exp. Brain Res., 2005, 160(3), 360-367.
[http://dx.doi.org/10.1007/s00221-004-2018-7] [PMID: 15448960]
[137]
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(4), 1341-1349.
[http://dx.doi.org/10.1046/j.1460-9568.1998.00153.x] [PMID: 9749788]
[138]
Murase, K.; Randic, M.; Shirasaki, 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(1), 84-91.
[http://dx.doi.org/10.1016/0006-8993(90)91323-9] [PMID: 2147117]
[139]
Shay, B.L.; Hochman, S. Serotonin alters multi-segmental convergence patterns in spinal cord deep dorsal horn and intermediate laminae neurons in an in vitro young rat preparation. Pain, 2002, 95(1-2), 7-14.
[http://dx.doi.org/10.1016/S0304-3959(01)00364-5] [PMID: 11790462]
[140]
Garraway, S.M.; Hochman, S. Serotonin increases the incidence of primary afferent-evoked long-term depression in rat deep dorsal horn neurons. J. Neurophysiol., 2001, 85(5), 1864-1872.
[http://dx.doi.org/10.1152/jn.2001.85.5.1864] [PMID: 11353003]
[141]
Liu, X.G.; Sandkühler, J. Long-term potentiation of C-fiber-evoked potentials in the rat spinal dorsal horn is prevented by spinal N-methyl-D-aspartic acid receptor blockage. Neurosci. Lett., 1995, 191(1-2), 43-46.
[http://dx.doi.org/10.1016/0304-3940(95)11553-0] [PMID: 7659287]
[142]
Liu, X.G.; Morton, C.R.; Azkue, J.J.; Zimmermann, M.; Sandkühler, J. Long-term depression of C-fibre-evoked spinal field potentials by stimulation of primary afferent A delta-fibres in the adult rat. Eur. J. Neurosci., 1998, 10(10), 3069-3075.
[http://dx.doi.org/10.1046/j.1460-9568.1998.00310.x] [PMID: 9786201]
[143]
Li, P.; Zhuo, M. Silent glutamatergic synapses and nociception in mammalian spinal cord. Nature, 1998, 393(6686), 695-698.
[http://dx.doi.org/10.1038/31496] [PMID: 9641681]
[144]
Zhuo, M. Descending facilitation. Mol. Pain, 2017, 131744806917699212
[http://dx.doi.org/10.1177/1744806917699212] [PMID: 28326945]
[145]
Zhao, Z.Q.; Liu, X.Y.; Jeffry, J.; Karunarathne, W.K.; Li, J.L.; Munanairi, A.; Zhou, X.Y.; Li, H.; Sun, Y.G.; Wan, L.; Wu, Z.Y.; Kim, S.; Huo, F.Q.; Mo, P.; Barry, D.M.; Zhang, C.K.; Kim, J.Y.; Gautam, N.; Renner, K.J.; Li, Y.Q.; Chen, Z.F. Descending control of itch transmission by the serotonergic system via 5-HT1A-facilitated GRP-GRPR signaling. Neuron, 2014, 84(4), 821-834.
[http://dx.doi.org/10.1016/j.neuron.2014.10.003] [PMID: 25453842]

Rights & Permissions Print Cite
Article Metrics
48
3
© 2024 Bentham Science Publishers | Privacy Policy