Skip to main content
Top
Published in: Molecular Pain 1/2012

Open Access 01-12-2012 | Research

Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala

Authors: Ayano Nakao, Yukari Takahashi, Masashi Nagase, Ryo Ikeda, Fusao Kato

Published in: Molecular Pain | Issue 1/2012

Login to get access

Abstract

Background

Neurons in the capsular part of the central nucleus of the amygdala (CeC), a region also called "nociceptive amygdala," receive nociceptive information from the dorsal horn via afferent pathways relayed from the lateral parabrachial nucleus (LPB). As the central amygdala is known to be involved in the acquisition and expression of emotion, this pathway is thought to play central roles in the generation of affective responses to nociceptive inputs. Excitatory synaptic transmission between afferents arising from the LPB and these CeC neurons is potentiated in arthritic, visceral, neuropathic, inflammatory and muscle pain models. In neuropathic pain models following spinal nerve ligation (SNL), in which we previously showed a robust LPB-CeC potentiation, the principal behavioral symptom is tactile allodynia triggered by non-C-fiber low-threshold mechanoreceptor afferents. Conversely, recent anatomical studies have revealed that most of the spinal neurons projecting to the LPB receive C-fiber afferent inputs. Here, we examined the hypothesis that these C-fiber-mediated inputs are necessary for the full establishment of robust synaptic potentiation of LPB-CeC transmission in the rats with neuropathic pain.

Results

Postnatal capsaicin treatment, which has been shown to denervate the C-fibers expressing transient receptor potential vanilloid type-1 (TRPV1) channels, completely abolished eye-wiping responses to capsaicin eye instillation in rats, but this treatment did not affect mechanical allodynia in the nerve-ligated animals. However, the postnatal capsaicin treatment prevented LPB-CeC synaptic potentiation after SNL, unlike in the vehicle-treated rats, primarily due to the decreased incidence of potentiated transmission by elimination of TRPV1-expressing C-fiber afferents.

Conclusions

C-fiber-mediated afferents in the nerve-ligated animals may be a required facilitator of the establishment of nerve injury-evoked synaptic potentiation in the CeC. These inputs might play essential roles in the chronic pain-induced plastic changes in the central network linking nociception and negative emotion.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, et al.: Innate versus learned odour processing in the mouse olfactory bulb. Nature 2007, 450: 503–508. 10.1038/nature06281CrossRefPubMed Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, et al.: Innate versus learned odour processing in the mouse olfactory bulb. Nature 2007, 450: 503–508. 10.1038/nature06281CrossRefPubMed
2.
go back to reference Fontanini A, Grossman SE, Figueroa JA, Katz DB: Distinct subtypes of basolateral amygdala taste neurons reflect palatability and reward. J Neurosci 2009, 29: 2486–2495. 10.1523/JNEUROSCI.3898-08.2009PubMedCentralCrossRefPubMed Fontanini A, Grossman SE, Figueroa JA, Katz DB: Distinct subtypes of basolateral amygdala taste neurons reflect palatability and reward. J Neurosci 2009, 29: 2486–2495. 10.1523/JNEUROSCI.3898-08.2009PubMedCentralCrossRefPubMed
3.
go back to reference Darwin C, Darwin F: The Expression of the Emotions in Man and Animals. 2nd edition. Cambridge University Press, London; 2009.CrossRef Darwin C, Darwin F: The Expression of the Emotions in Man and Animals. 2nd edition. Cambridge University Press, London; 2009.CrossRef
4.
go back to reference Meyerhof W: Elucidation of mammalian bitter taste. Rev Physiol Biochem Pharmacol 2005, 154: 37–72.PubMed Meyerhof W: Elucidation of mammalian bitter taste. Rev Physiol Biochem Pharmacol 2005, 154: 37–72.PubMed
6.
go back to reference Todd AJ, Puskar Z, Spike RC, Hughes C, Watt C, Forrest L: Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. J Neurosci 2002, 22: 4103–4113.PubMed Todd AJ, Puskar Z, Spike RC, Hughes C, Watt C, Forrest L: Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. J Neurosci 2002, 22: 4103–4113.PubMed
7.
go back to reference Gauriau C, Bernard JF: Pain pathways and parabrachial circuits in the rat. Exp Physiol 2002, 87: 251–258. 10.1113/eph8702357CrossRefPubMed Gauriau C, Bernard JF: Pain pathways and parabrachial circuits in the rat. Exp Physiol 2002, 87: 251–258. 10.1113/eph8702357CrossRefPubMed
8.
go back to reference Sarhan M, Freund-Mercier MJ, Veinante P: Branching patterns of parabrachial neurons projecting to the central extended amgydala: single axonal reconstructions. J Comp Neurol 2005, 491: 418–442. 10.1002/cne.20697CrossRefPubMed Sarhan M, Freund-Mercier MJ, Veinante P: Branching patterns of parabrachial neurons projecting to the central extended amgydala: single axonal reconstructions. J Comp Neurol 2005, 491: 418–442. 10.1002/cne.20697CrossRefPubMed
9.
go back to reference Dong YL, Fukazawa Y, Wang W, Kamasawa N, Shigemoto R: Differential postsynaptic compartments in the laterocapsular division of the central nucleus of amygdala for afferents from the parabrachial nucleus and the basolateral nucleus in the rat. J Comp Neurol 2010, 518: 4771–4791. 10.1002/cne.22487CrossRefPubMed Dong YL, Fukazawa Y, Wang W, Kamasawa N, Shigemoto R: Differential postsynaptic compartments in the laterocapsular division of the central nucleus of amygdala for afferents from the parabrachial nucleus and the basolateral nucleus in the rat. J Comp Neurol 2010, 518: 4771–4791. 10.1002/cne.22487CrossRefPubMed
10.
go back to reference Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates. Sixth Edition, Academic Press; 2008. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates. Sixth Edition, Academic Press; 2008.
11.
go back to reference Neugebauer V, Li WD, Bird GC, Han JS: The amygdala and persistent pain. Neuroscientist 2004, 10: 221–234. 10.1177/1073858403261077CrossRefPubMed Neugebauer V, Li WD, Bird GC, Han JS: The amygdala and persistent pain. Neuroscientist 2004, 10: 221–234. 10.1177/1073858403261077CrossRefPubMed
12.
go back to reference Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A: Amygdala inhibitory circuits and the control of fear memory. Neuron 2009, 62: 757–771. 10.1016/j.neuron.2009.05.026CrossRefPubMed Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A: Amygdala inhibitory circuits and the control of fear memory. Neuron 2009, 62: 757–771. 10.1016/j.neuron.2009.05.026CrossRefPubMed
13.
14.
go back to reference Cheng SJ, Chen CC, Yang HW, Chang YT, Bai SW, Yen CT, Min MY: Role of extracellular signal-regulated kinase in synaptic transmission and plasticity of a nociceptive input on capsular central amygdaloid neurons in normal and acid-induced muscle pain mice. J Neurosci 2011, 31: 2258–2270. 10.1523/JNEUROSCI.5564-10.2011CrossRefPubMed Cheng SJ, Chen CC, Yang HW, Chang YT, Bai SW, Yen CT, Min MY: Role of extracellular signal-regulated kinase in synaptic transmission and plasticity of a nociceptive input on capsular central amygdaloid neurons in normal and acid-induced muscle pain mice. J Neurosci 2011, 31: 2258–2270. 10.1523/JNEUROSCI.5564-10.2011CrossRefPubMed
15.
go back to reference Ikeda R, Takahashi Y, Inoue K, Kato F: NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain. Pain 2007, 127: 161–172. 10.1016/j.pain.2006.09.003CrossRefPubMed Ikeda R, Takahashi Y, Inoue K, Kato F: NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain. Pain 2007, 127: 161–172. 10.1016/j.pain.2006.09.003CrossRefPubMed
16.
go back to reference Kim SH, Chung JM: An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50: 355–363. 10.1016/0304-3959(92)90041-9CrossRefPubMed Kim SH, Chung JM: An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50: 355–363. 10.1016/0304-3959(92)90041-9CrossRefPubMed
17.
go back to reference Ossipov MH, Bian D, Malan TP, Lai J, Porreca F: Lack of involvement of capsaicin-sensitive primary afferents in nerve-ligation injury induced tactile allodynia in rats. Pain 1999, 79: 127–133. 10.1016/S0304-3959(98)00187-0CrossRefPubMed Ossipov MH, Bian D, Malan TP, Lai J, Porreca F: Lack of involvement of capsaicin-sensitive primary afferents in nerve-ligation injury induced tactile allodynia in rats. Pain 1999, 79: 127–133. 10.1016/S0304-3959(98)00187-0CrossRefPubMed
18.
go back to reference Nagy JI, Iversen LL, Goedert M, Chapman D, Hunt SP: Dose-dependent effects of capsaicin on primary sensory neurons in the neonatal rat. J Neurosci 1983, 3: 399–406.PubMed Nagy JI, Iversen LL, Goedert M, Chapman D, Hunt SP: Dose-dependent effects of capsaicin on primary sensory neurons in the neonatal rat. J Neurosci 1983, 3: 399–406.PubMed
19.
go back to reference Holzer P, Jurna I, Gamse R, Lembeck F: Nociceptive threshold after neonatal capsaicin treatment. Eur J Pharmacol 1979, 58: 511–514. 10.1016/0014-2999(79)90327-3CrossRefPubMed Holzer P, Jurna I, Gamse R, Lembeck F: Nociceptive threshold after neonatal capsaicin treatment. Eur J Pharmacol 1979, 58: 511–514. 10.1016/0014-2999(79)90327-3CrossRefPubMed
20.
go back to reference Faulkner DC, Growcott JW: Effects of neonatal capsaicin administration on the nociceptive response of the rat to mechanical and chemical stimuli. J Pharm Pharmacol 1980, 32: 656–657.CrossRefPubMed Faulkner DC, Growcott JW: Effects of neonatal capsaicin administration on the nociceptive response of the rat to mechanical and chemical stimuli. J Pharm Pharmacol 1980, 32: 656–657.CrossRefPubMed
21.
go back to reference Nagy JI, Vincent SR, Staines WA, Fibiger HC, Reisine TD, Yamamura HI: Neurotoxic action of capsaicin on spinal substance P neurons. Brain Res 1980, 186: 435–444. 10.1016/0006-8993(80)90987-7CrossRefPubMed Nagy JI, Vincent SR, Staines WA, Fibiger HC, Reisine TD, Yamamura HI: Neurotoxic action of capsaicin on spinal substance P neurons. Brain Res 1980, 186: 435–444. 10.1016/0006-8993(80)90987-7CrossRefPubMed
22.
go back to reference Fu Y, Han J, Ishola T, Scerbo M, Adwanikar H, Ramsey C, Neugebauer V: PKA and ERK, but not PKC, in the amygdala contribute to pain-related synaptic plasticity and behavior. Mol Pain 2008, 4: 26. 10.1186/1744-8069-4-26PubMedCentralCrossRefPubMed Fu Y, Han J, Ishola T, Scerbo M, Adwanikar H, Ramsey C, Neugebauer V: PKA and ERK, but not PKC, in the amygdala contribute to pain-related synaptic plasticity and behavior. Mol Pain 2008, 4: 26. 10.1186/1744-8069-4-26PubMedCentralCrossRefPubMed
23.
go back to reference Jancso G, Kiraly E: Sensory neurotoxins: chemically induced selective destruction of primary sensory neurons. Brain Res 1981, 210: 83–89. 10.1016/0006-8993(81)90886-6CrossRefPubMed Jancso G, Kiraly E: Sensory neurotoxins: chemically induced selective destruction of primary sensory neurons. Brain Res 1981, 210: 83–89. 10.1016/0006-8993(81)90886-6CrossRefPubMed
24.
go back to reference Hao JX, Yu W, Xu XJ, Wiesenfeld-Hallin Z: Capsaicin-sensitive afferents mediate chronic cold, but not mechanical, allodynia-like behavior in spinally injured rats. Brain Res 1996, 722: 177–180. 10.1016/0006-8993(96)00216-8CrossRefPubMed Hao JX, Yu W, Xu XJ, Wiesenfeld-Hallin Z: Capsaicin-sensitive afferents mediate chronic cold, but not mechanical, allodynia-like behavior in spinally injured rats. Brain Res 1996, 722: 177–180. 10.1016/0006-8993(96)00216-8CrossRefPubMed
25.
go back to reference Yamamoto K, Noguchi J, Yamada C, Watabe AM, Kato F: Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat. BMC Neurosci 2010, 11: 134. 10.1186/1471-2202-11-S1-P134PubMedCentralCrossRefPubMed Yamamoto K, Noguchi J, Yamada C, Watabe AM, Kato F: Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat. BMC Neurosci 2010, 11: 134. 10.1186/1471-2202-11-S1-P134PubMedCentralCrossRefPubMed
26.
go back to reference Jancso G, Kiraly E, Jancso-Gabor A: Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 1977, 270: 741–743. 10.1038/270741a0CrossRefPubMed Jancso G, Kiraly E, Jancso-Gabor A: Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 1977, 270: 741–743. 10.1038/270741a0CrossRefPubMed
27.
go back to reference Nagy JI, Hunt SP, Iversen LL, Emson PC: Biochemical and anatomical observations on the degeneration of peptide-containing primary afferent neurons after neonatal capsaicin. Neuroscience 1981, 6: 1923–1934. 10.1016/0306-4522(81)90032-4CrossRefPubMed Nagy JI, Hunt SP, Iversen LL, Emson PC: Biochemical and anatomical observations on the degeneration of peptide-containing primary afferent neurons after neonatal capsaicin. Neuroscience 1981, 6: 1923–1934. 10.1016/0306-4522(81)90032-4CrossRefPubMed
28.
go back to reference Arvidsson J, Ygge J: A quantitative study of the effects of neonatal capsaicin treatment and of subsequent peripheral nerve transection in the adult rat. Brain Res 1986, 397: 130–136. 10.1016/0006-8993(86)91376-4CrossRefPubMed Arvidsson J, Ygge J: A quantitative study of the effects of neonatal capsaicin treatment and of subsequent peripheral nerve transection in the adult rat. Brain Res 1986, 397: 130–136. 10.1016/0006-8993(86)91376-4CrossRefPubMed
29.
go back to reference Woolf CJ, Doubell TP: The pathophysiology of chronic pain - increased sensitivity to low threshold A beta-fibre inputs. Curr Opin Neurobiol 1994, 4: 525–534. 10.1016/0959-4388(94)90053-1CrossRefPubMed Woolf CJ, Doubell TP: The pathophysiology of chronic pain - increased sensitivity to low threshold A beta-fibre inputs. Curr Opin Neurobiol 1994, 4: 525–534. 10.1016/0959-4388(94)90053-1CrossRefPubMed
30.
go back to reference Sandkuhler J: Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 2009, 89: 707–758. 10.1152/physrev.00025.2008CrossRefPubMed Sandkuhler J: Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 2009, 89: 707–758. 10.1152/physrev.00025.2008CrossRefPubMed
31.
go back to reference Seal RP, Wang X, Guan Y, Raja SN, Woodbury CJ, Basbaum AI, Edwards RH: Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 2009, 462: 651–655. 10.1038/nature08505PubMedCentralCrossRefPubMed Seal RP, Wang X, Guan Y, Raja SN, Woodbury CJ, Basbaum AI, Edwards RH: Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 2009, 462: 651–655. 10.1038/nature08505PubMedCentralCrossRefPubMed
32.
go back to reference Szallasi A, Joo F, Blumberg PM: Duration of desensitization and ultrastructural changes in dorsal root ganglia in rats treated with resiniferatoxin, an ultrapotent capsaicin analog. Brain Res 1989, 503: 68–72. 10.1016/0006-8993(89)91705-8CrossRefPubMed Szallasi A, Joo F, Blumberg PM: Duration of desensitization and ultrastructural changes in dorsal root ganglia in rats treated with resiniferatoxin, an ultrapotent capsaicin analog. Brain Res 1989, 503: 68–72. 10.1016/0006-8993(89)91705-8CrossRefPubMed
33.
go back to reference Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D: Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288: 306–313. 10.1126/science.288.5464.306CrossRefPubMed Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D: Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288: 306–313. 10.1126/science.288.5464.306CrossRefPubMed
34.
go back to reference Guo A, Simone DA, Stone LS, Fairbanks CA, Wang J, Elde R: Developmental shift of vanilloid receptor 1 (VR1) terminals into deeper regions of the superficial dorsal horn: correlation with a shift from TrkA to Ret expression by dorsal root ganglion neurons. Eur J Neurosci 2001, 14: 293–304. 10.1046/j.0953-816x.2001.01665.xCrossRefPubMed Guo A, Simone DA, Stone LS, Fairbanks CA, Wang J, Elde R: Developmental shift of vanilloid receptor 1 (VR1) terminals into deeper regions of the superficial dorsal horn: correlation with a shift from TrkA to Ret expression by dorsal root ganglion neurons. Eur J Neurosci 2001, 14: 293–304. 10.1046/j.0953-816x.2001.01665.xCrossRefPubMed
35.
go back to reference Lu CR, Hwang SJ, Phend KD, Rustioni A, Valtschanoff JG: Primary afferent terminals that express presynaptic NR1 in rats are mainly from myelinated, mechanosensitive fibers. J Comp Neurol 2003, 460: 191–202. 10.1002/cne.10632CrossRefPubMed Lu CR, Hwang SJ, Phend KD, Rustioni A, Valtschanoff JG: Primary afferent terminals that express presynaptic NR1 in rats are mainly from myelinated, mechanosensitive fibers. J Comp Neurol 2003, 460: 191–202. 10.1002/cne.10632CrossRefPubMed
36.
go back to reference Al-Khater KM, Todd AJ: Collateral projections of neurons in laminae I, III, and IV of rat spinal cord to thalamus, periaqueductal gray matter, and lateral parabrachial area. J Comp Neurol 2009, 515: 629–646. 10.1002/cne.22081PubMedCentralCrossRefPubMed Al-Khater KM, Todd AJ: Collateral projections of neurons in laminae I, III, and IV of rat spinal cord to thalamus, periaqueductal gray matter, and lateral parabrachial area. J Comp Neurol 2009, 515: 629–646. 10.1002/cne.22081PubMedCentralCrossRefPubMed
37.
go back to reference Shortland P, Kinnman E, Molander C: Sprouting of A-fibre primary afferents into lamina II in two rat models of neuropathic pain (vol 1, pg 215, 1997). Eur J Pain London 1998, 2: 91–91.CrossRef Shortland P, Kinnman E, Molander C: Sprouting of A-fibre primary afferents into lamina II in two rat models of neuropathic pain (vol 1, pg 215, 1997). Eur J Pain London 1998, 2: 91–91.CrossRef
38.
go back to reference Woolf CJ, Shortland P, Coggeshall RE: Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 1992, 355: 75–78. 10.1038/355075a0CrossRefPubMed Woolf CJ, Shortland P, Coggeshall RE: Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 1992, 355: 75–78. 10.1038/355075a0CrossRefPubMed
39.
go back to reference Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA: Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 2001, 21: RC140.PubMed Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA: Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 2001, 21: RC140.PubMed
40.
go back to reference Fukuoka T, Noguchi K: Contribution of the spared primary afferent neurons to the pathomechanisms of neuropathic pain. Mol Neurobiol 2002, 26: 57–67. 10.1385/MN:26:1:057CrossRefPubMed Fukuoka T, Noguchi K: Contribution of the spared primary afferent neurons to the pathomechanisms of neuropathic pain. Mol Neurobiol 2002, 26: 57–67. 10.1385/MN:26:1:057CrossRefPubMed
41.
go back to reference Keller AF, Beggs S, Salter MW, De Koninck Y: Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain. Mol Pain 2007, 3: 27. 10.1186/1744-8069-3-27PubMedCentralCrossRefPubMed Keller AF, Beggs S, Salter MW, De Koninck Y: Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain. Mol Pain 2007, 3: 27. 10.1186/1744-8069-3-27PubMedCentralCrossRefPubMed
42.
go back to reference Cortright DN, Crandall M, Sanchez JF, Zou T, Krause JE, White G: The tissue distribution and functional characterization of human VR1. Biochem Biophys Res Commun 2001, 281: 1183–1189. 10.1006/bbrc.2001.4482CrossRefPubMed Cortright DN, Crandall M, Sanchez JF, Zou T, Krause JE, White G: The tissue distribution and functional characterization of human VR1. Biochem Biophys Res Commun 2001, 281: 1183–1189. 10.1006/bbrc.2001.4482CrossRefPubMed
43.
go back to reference Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, Papp Z, Edes I, Csiba L, Blumberg PM: Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 2005, 135: 162–168.CrossRefPubMed Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, Papp Z, Edes I, Csiba L, Blumberg PM: Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 2005, 135: 162–168.CrossRefPubMed
44.
go back to reference Szabo T, Biro T, Gonzalez AF, Palkovits M, Blumberg PM: Pharmacological characterization of vanilloid receptor located in the brain. Brain Res Mol Brain Res 2002, 98: 51–57.CrossRefPubMed Szabo T, Biro T, Gonzalez AF, Palkovits M, Blumberg PM: Pharmacological characterization of vanilloid receptor located in the brain. Brain Res Mol Brain Res 2002, 98: 51–57.CrossRefPubMed
45.
go back to reference Sanchez JF, Krause JE, Cortright DN: The distribution and regulation of vanilloid receptor VR1 and VR1 5' splice variant RNA expression in rat. Neuroscience 2001, 107: 373–381. 10.1016/S0306-4522(01)00373-6CrossRefPubMed Sanchez JF, Krause JE, Cortright DN: The distribution and regulation of vanilloid receptor VR1 and VR1 5' splice variant RNA expression in rat. Neuroscience 2001, 107: 373–381. 10.1016/S0306-4522(01)00373-6CrossRefPubMed
46.
go back to reference Hori T, Tsuzuki S: Thermoregulation in adult rats which have been treated with capsaicin as neonates. Pflugers Arch 1981, 390: 219–223. 10.1007/BF00658265CrossRefPubMed Hori T, Tsuzuki S: Thermoregulation in adult rats which have been treated with capsaicin as neonates. Pflugers Arch 1981, 390: 219–223. 10.1007/BF00658265CrossRefPubMed
47.
go back to reference Zschenderlein C, Gebhardt C, von Bohlen Und Halbach O, Kulisch C, Albrecht D: Capsaicin-Induced Changes in LTP in the Lateral Amygdala Are Mediated by TRPV1. PLoS One 2011, 6: e16116. 10.1371/journal.pone.0016116PubMedCentralCrossRefPubMed Zschenderlein C, Gebhardt C, von Bohlen Und Halbach O, Kulisch C, Albrecht D: Capsaicin-Induced Changes in LTP in the Lateral Amygdala Are Mediated by TRPV1. PLoS One 2011, 6: e16116. 10.1371/journal.pone.0016116PubMedCentralCrossRefPubMed
48.
go back to reference Beggs S, Liu XJ, Kwan C, Salter MW: Peripheral nerve injury and TRPV1-expressing primary afferent C-fibers cause opening of the blood–brain barrier. Mol Pain 2010, 6: 74. 10.1186/1744-8069-6-74PubMedCentralCrossRefPubMed Beggs S, Liu XJ, Kwan C, Salter MW: Peripheral nerve injury and TRPV1-expressing primary afferent C-fibers cause opening of the blood–brain barrier. Mol Pain 2010, 6: 74. 10.1186/1744-8069-6-74PubMedCentralCrossRefPubMed
49.
go back to reference Price DD: Psychological and neural mechanisms of the affective dimension of pain. Science 2000, 288: 1769–1772. 10.1126/science.288.5472.1769CrossRefPubMed Price DD: Psychological and neural mechanisms of the affective dimension of pain. Science 2000, 288: 1769–1772. 10.1126/science.288.5472.1769CrossRefPubMed
50.
go back to reference Fontanini A, Katz DB: State-dependent modulation of time-varying gustatory responses. J Neurophysiol 2006, 96: 3183–3193. 10.1152/jn.00804.2006CrossRefPubMed Fontanini A, Katz DB: State-dependent modulation of time-varying gustatory responses. J Neurophysiol 2006, 96: 3183–3193. 10.1152/jn.00804.2006CrossRefPubMed
51.
go back to reference Zimmermann M: Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16: 109–110. 10.1016/0304-3959(83)90201-4CrossRefPubMed Zimmermann M: Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16: 109–110. 10.1016/0304-3959(83)90201-4CrossRefPubMed
52.
go back to reference Jancso G, Kiraly E, Jancso-Gabor A: Direct evidence for an axonal site of action of capsaicin. Naunyn Schmiedebergs Arch Pharmacol 1980, 313: 91–94. 10.1007/BF00505809CrossRefPubMed Jancso G, Kiraly E, Jancso-Gabor A: Direct evidence for an axonal site of action of capsaicin. Naunyn Schmiedebergs Arch Pharmacol 1980, 313: 91–94. 10.1007/BF00505809CrossRefPubMed
53.
go back to reference Gamse R, Lackner D, Gamse G, Leeman SE: Effect of capsaicin pretreatment on capsaicin-evoked release of immunoreactive somatostatin and substance P from primary sensory neurons. Naunyn Schmiedebergs Arch Pharmacol 1981, 316: 38–41. 10.1007/BF00507224CrossRefPubMed Gamse R, Lackner D, Gamse G, Leeman SE: Effect of capsaicin pretreatment on capsaicin-evoked release of immunoreactive somatostatin and substance P from primary sensory neurons. Naunyn Schmiedebergs Arch Pharmacol 1981, 316: 38–41. 10.1007/BF00507224CrossRefPubMed
54.
go back to reference Welk E, Fleischer E, Petsche U, Handwerker HO: Afferent C-fibres in rats after neonatal capsaicin treatment. Pflugers Arch 1984, 400: 66–71. 10.1007/BF00670538CrossRefPubMed Welk E, Fleischer E, Petsche U, Handwerker HO: Afferent C-fibres in rats after neonatal capsaicin treatment. Pflugers Arch 1984, 400: 66–71. 10.1007/BF00670538CrossRefPubMed
55.
go back to reference Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL: Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53: 55–63. 10.1016/0165-0270(94)90144-9CrossRefPubMed Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL: Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53: 55–63. 10.1016/0165-0270(94)90144-9CrossRefPubMed
56.
go back to reference Raastad M, Storm JF, Andersen P: Putative Single Quantum and Single Fibre Excitatory Postsynaptic Currents Show Similar Amplitude Range and Variability in Rat Hippocampal Slices. Eur J Neurosci 1992, 4: 113–117. 10.1111/j.1460-9568.1992.tb00114.xCrossRefPubMed Raastad M, Storm JF, Andersen P: Putative Single Quantum and Single Fibre Excitatory Postsynaptic Currents Show Similar Amplitude Range and Variability in Rat Hippocampal Slices. Eur J Neurosci 1992, 4: 113–117. 10.1111/j.1460-9568.1992.tb00114.xCrossRefPubMed
Metadata
Title
Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala
Authors
Ayano Nakao
Yukari Takahashi
Masashi Nagase
Ryo Ikeda
Fusao Kato
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Molecular Pain / Issue 1/2012
Electronic ISSN: 1744-8069
DOI
https://doi.org/10.1186/1744-8069-8-51

Other articles of this Issue 1/2012

Molecular Pain 1/2012 Go to the issue