Skip to main content
Top
Published in: The Journal of Headache and Pain 6/2012

Open Access 01-08-2012 | Original

Brain-derived neurotrophic factor in primary headaches

Authors: Marlene Fischer, Georg Wille, Stephanie Klien, Hind Shanib, Dagny Holle, Charly Gaul, Gregor Broessner

Published in: The Journal of Headache and Pain | Issue 6/2012

Login to get access

Abstract

Brain derived neurotrophic factor (BDNF) is associated with pain modulation and central sensitization. Recently, a role of BDNF in migraine and cluster headache pathophysiology has been suspected due to its known interaction with calcitonin gene-related peptide. Bi-center prospective study was done enrolling four diagnostic groups: episodic migraine with and without aura, episodic cluster headache, frequent episodic tension-type headache, and healthy individuals. In migraineurs, venous blood samples were collected twice: outside and during migraine attacks prior to pain medication. In cluster headache patients serum samples were collected in and outside cluster bout. Analysis of BDNF was performed using enzyme-linked immunosorbent assay technique. Migraine patients revealed significantly higher BDNF serum levels during migraine attacks (n = 25) compared with headache-free intervals (n = 53, P < 0.01), patients with tension-type headache (n = 6, P < 0.05), and healthy controls (n = 22, P < 0.001). There was no significant difference between patients with migraine with aura compared with those without aura, neither during migraine attacks nor during headache-free periods. Cluster headache patients showed significantly higher BDNF concentrations inside (n = 42) and outside cluster bouts (n = 24) compared with healthy controls (P < 0.01, P < 0.05). BDNF is increased during migraine attacks, and in cluster headache, further supporting the involvement of BDNF in the pathophysiology of these primary headaches.
Literature
1.
go back to reference Lipton RB, Stewart WF, Scher AI (2001) Epidemiology and economic impact of migraine. Curr Med Res Opin 17(Suppl 1):s4–s12 (Epub 2002/12/05), 12463270, 10.1185/0300799039117005, (Epub 2002/12/05)CrossRefPubMed Lipton RB, Stewart WF, Scher AI (2001) Epidemiology and economic impact of migraine. Curr Med Res Opin 17(Suppl 1):s4–s12 (Epub 2002/12/05), 12463270, 10.1185/0300799039117005, (Epub 2002/12/05)CrossRefPubMed
2.
go back to reference Goadsby PJ, Lipton RB, Ferrari MD (2002) Migraine—current understanding and treatment. N Engl J Med 346(4):257–270 (Epub 2002/01/25), 11807151, 10.1056/NEJMra010917, 1:CAS:528:DC%2BD38XmslGgsQ%3D%3D, (Epub 2002/01/25)CrossRefPubMed Goadsby PJ, Lipton RB, Ferrari MD (2002) Migraine—current understanding and treatment. N Engl J Med 346(4):257–270 (Epub 2002/01/25), 11807151, 10.1056/NEJMra010917, 1:CAS:528:DC%2BD38XmslGgsQ%3D%3D, (Epub 2002/01/25)CrossRefPubMed
3.
go back to reference May A (2003) The trigeminovascular system in the human. Cerebral blood flow, functional imaging and primary headache. Nervenarzt 74(12):1067–1077, 14647907, 10.1007/s00115-003-1578-2, 1:STN:280:DC%2BD3srntVyiug%3D%3DCrossRefPubMed May A (2003) The trigeminovascular system in the human. Cerebral blood flow, functional imaging and primary headache. Nervenarzt 74(12):1067–1077, 14647907, 10.1007/s00115-003-1578-2, 1:STN:280:DC%2BD3srntVyiug%3D%3DCrossRefPubMed
4.
go back to reference Leone M, Bussone G (2009) Pathophysiology of trigeminal autonomic cephalalgias. Lancet Neurol 8(8):755–764, 19608101, 10.1016/S1474-4422(09)70133-4CrossRefPubMed Leone M, Bussone G (2009) Pathophysiology of trigeminal autonomic cephalalgias. Lancet Neurol 8(8):755–764, 19608101, 10.1016/S1474-4422(09)70133-4CrossRefPubMed
5.
go back to reference Lipsky RH, Marini AM (2007) Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Ann N Y Acad Sci 1122:130–143, 18077569, 10.1196/annals.1403.009, 1:CAS:528:DC%2BD1cXhtVOksLs%3DCrossRefPubMed Lipsky RH, Marini AM (2007) Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Ann N Y Acad Sci 1122:130–143, 18077569, 10.1196/annals.1403.009, 1:CAS:528:DC%2BD1cXhtVOksLs%3DCrossRefPubMed
6.
go back to reference Thompson SW, Bennett DL, Kerr BJ, Bradbury EJ, McMahon SB (1999) Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc Natl Acad Sci USA 96(14):7714–7718 Thompson SW, Bennett DL, Kerr BJ, Bradbury EJ, McMahon SB (1999) Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc Natl Acad Sci USA 96(14):7714–7718
7.
go back to reference Latremoliere A, Woolf CJ (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10(9):895–926, 19712899, 10.1016/j.jpain.2009.06.012PubMedCentralCrossRefPubMed Latremoliere A, Woolf CJ (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10(9):895–926, 19712899, 10.1016/j.jpain.2009.06.012PubMedCentralCrossRefPubMed
8.
go back to reference Buldyrev I, Tanner NM, Hsieh HY, Dodd EG, Nguyen LT, Balkowiec A (2006) Calcitonin gene-related peptide enhances release of native brain-derived neurotrophic factor from trigeminal ganglion neurons. J Neurochem 99(5):1338–1350, 17064360, 10.1111/j.1471-4159.2006.04161.x, 1:CAS:528:DC%2BD28XhtlCntrjIPubMedCentralCrossRefPubMed Buldyrev I, Tanner NM, Hsieh HY, Dodd EG, Nguyen LT, Balkowiec A (2006) Calcitonin gene-related peptide enhances release of native brain-derived neurotrophic factor from trigeminal ganglion neurons. J Neurochem 99(5):1338–1350, 17064360, 10.1111/j.1471-4159.2006.04161.x, 1:CAS:528:DC%2BD28XhtlCntrjIPubMedCentralCrossRefPubMed
9.
go back to reference Ichikawa H, Yabuuchi T, Jin HW, Terayama R, Yamaai T, Deguchi T et al (2006) Brain-derived neurotrophic factor-immunoreactive primary sensory neurons in the rat trigeminal ganglion and trigeminal sensory nuclei. Brain Res 1081(1):113–118, 16510129, 10.1016/j.brainres.2006.01.027, 1:CAS:528:DC%2BD28XjsFOntL8%3DCrossRefPubMed Ichikawa H, Yabuuchi T, Jin HW, Terayama R, Yamaai T, Deguchi T et al (2006) Brain-derived neurotrophic factor-immunoreactive primary sensory neurons in the rat trigeminal ganglion and trigeminal sensory nuclei. Brain Res 1081(1):113–118, 16510129, 10.1016/j.brainres.2006.01.027, 1:CAS:528:DC%2BD28XjsFOntL8%3DCrossRefPubMed
10.
go back to reference Balkowiec-Iskra E, Vermehren-Schmaedick A, Balkowiec A (2011) Tumor necrosis factor-alpha increases brain-derived neurotrophic factor expression in trigeminal ganglion neurons in an activity-dependent manner. Neuroscience 180:322–333, 21335064, 10.1016/j.neuroscience.2011.02.028, 1:CAS:528:DC%2BC3MXktF2gt7w%3DPubMedCentralCrossRefPubMed Balkowiec-Iskra E, Vermehren-Schmaedick A, Balkowiec A (2011) Tumor necrosis factor-alpha increases brain-derived neurotrophic factor expression in trigeminal ganglion neurons in an activity-dependent manner. Neuroscience 180:322–333, 21335064, 10.1016/j.neuroscience.2011.02.028, 1:CAS:528:DC%2BC3MXktF2gt7w%3DPubMedCentralCrossRefPubMed
11.
go back to reference Lemos C, Mendonca D, Pereira-Monteiro J, Barros J, Sequeiros J, Alonso I et al (2010) BDNF and CGRP interaction: implications in migraine susceptibility. Cephalalgia 30(11):1375–1382, 20959432, 10.1177/0333102410368443CrossRefPubMed Lemos C, Mendonca D, Pereira-Monteiro J, Barros J, Sequeiros J, Alonso I et al (2010) BDNF and CGRP interaction: implications in migraine susceptibility. Cephalalgia 30(11):1375–1382, 20959432, 10.1177/0333102410368443CrossRefPubMed
12.
go back to reference International Headache Society (2004) The international classification of headache disorders: 2nd edition. Cephalalgia 24(Suppl 1):9–160 International Headache Society (2004) The international classification of headache disorders: 2nd edition. Cephalalgia 24(Suppl 1):9–160
13.
go back to reference Merighi A, Salio C, Ghirri A, Lossi L, Ferrini F, Betelli C et al (2008) BDNF as a pain modulator. Prog Neurobiol 85(3):297–317, 18514997, 10.1016/j.pneurobio.2008.04.004, 1:CAS:528:DC%2BD1cXosVymurg%3DCrossRefPubMed Merighi A, Salio C, Ghirri A, Lossi L, Ferrini F, Betelli C et al (2008) BDNF as a pain modulator. Prog Neurobiol 85(3):297–317, 18514997, 10.1016/j.pneurobio.2008.04.004, 1:CAS:528:DC%2BD1cXosVymurg%3DCrossRefPubMed
14.
go back to reference Cirulli F, Berry A, Alleva E (2000) Intracerebroventricular administration of brain-derived neurotrophic factor in adult rats affects analgesia and spontaneous behaviour but not memory retention in a Morris Water Maze task. Neurosci Lett 287(3):207–210, 10863031, 10.1016/S0304-3940(00)01173-3, 1:CAS:528:DC%2BD3cXktV2qu70%3DCrossRefPubMed Cirulli F, Berry A, Alleva E (2000) Intracerebroventricular administration of brain-derived neurotrophic factor in adult rats affects analgesia and spontaneous behaviour but not memory retention in a Morris Water Maze task. Neurosci Lett 287(3):207–210, 10863031, 10.1016/S0304-3940(00)01173-3, 1:CAS:528:DC%2BD3cXktV2qu70%3DCrossRefPubMed
15.
go back to reference Altar CA, Siuciak JA, Wright P, Ip NY, Lindsay RM, Wiegand SJ (1994) In situ hybridization of trkB and trkC receptor mRNA in rat forebrain and association with high-affinity binding of [125I]BDNF, [125I]NT-4/5 and [125I]NT-3. Eur J Neurosci 6(9):1389–1405, 8000564, 10.1111/j.1460-9568.1994.tb01001.x, 1:STN:280:DyaK2M%2FptlKntg%3D%3DCrossRefPubMed Altar CA, Siuciak JA, Wright P, Ip NY, Lindsay RM, Wiegand SJ (1994) In situ hybridization of trkB and trkC receptor mRNA in rat forebrain and association with high-affinity binding of [125I]BDNF, [125I]NT-4/5 and [125I]NT-3. Eur J Neurosci 6(9):1389–1405, 8000564, 10.1111/j.1460-9568.1994.tb01001.x, 1:STN:280:DyaK2M%2FptlKntg%3D%3DCrossRefPubMed
16.
go back to reference Fukuhara K, Ishikawa K, Yasuda S, Kishishita Y, Kim HK, Kakeda T et al (2011) Intracerebroventricular 4-methylcatechol (4-MC) ameliorates chronic pain associated with depression-like behavior via induction of brain-derived neurotrophic factor (BDNF). Cell Mol Neurobiol (Epub 27 Dec 2011) Fukuhara K, Ishikawa K, Yasuda S, Kishishita Y, Kim HK, Kakeda T et al (2011) Intracerebroventricular 4-methylcatechol (4-MC) ameliorates chronic pain associated with depression-like behavior via induction of brain-derived neurotrophic factor (BDNF). Cell Mol Neurobiol (Epub 27 Dec 2011)
17.
go back to reference Zhang X, Xu Y, Wang J, Zhou Q, Pu S, Jiang W et al (2012) The effect of intrathecal administration of glial activation inhibitors on dorsal horn BDNF overexpression and hind paw mechanical allodynia in spinal nerve ligated rats. J Neural Transm 119(3):329–336, 21901501, 10.1007/s00702-011-0713-7, 1:CAS:528:DC%2BC38Xisl2ksbc%3DCrossRefPubMed Zhang X, Xu Y, Wang J, Zhou Q, Pu S, Jiang W et al (2012) The effect of intrathecal administration of glial activation inhibitors on dorsal horn BDNF overexpression and hind paw mechanical allodynia in spinal nerve ligated rats. J Neural Transm 119(3):329–336, 21901501, 10.1007/s00702-011-0713-7, 1:CAS:528:DC%2BC38Xisl2ksbc%3DCrossRefPubMed
18.
go back to reference Ulmann L, Hatcher JP, Hughes JP, Chaumont S, Green PJ, Conquet F et al (2008) Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci 28(44):11263–11268, 18971468, 10.1523/JNEUROSCI.2308-08.2008, 1:CAS:528:DC%2BD1cXhtlGltrfLCrossRefPubMed Ulmann L, Hatcher JP, Hughes JP, Chaumont S, Green PJ, Conquet F et al (2008) Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci 28(44):11263–11268, 18971468, 10.1523/JNEUROSCI.2308-08.2008, 1:CAS:528:DC%2BD1cXhtlGltrfLCrossRefPubMed
19.
go back to reference Goadsby PJ, Edvinsson L, Ekman R (1988) Release of vasoactive peptides in the extracerebral circulation of humans and the cat during activation of the trigeminovascular system. Ann Neurol 23(2):193–196, 2454066, 10.1002/ana.410230214, 1:CAS:528:DyaL1cXhsVeqsLo%3DCrossRefPubMed Goadsby PJ, Edvinsson L, Ekman R (1988) Release of vasoactive peptides in the extracerebral circulation of humans and the cat during activation of the trigeminovascular system. Ann Neurol 23(2):193–196, 2454066, 10.1002/ana.410230214, 1:CAS:528:DyaL1cXhsVeqsLo%3DCrossRefPubMed
20.
go back to reference Buzzi MG, Moskowitz MA (1992) The trigemino-vascular system and migraine. Pathol Biol (Paris) 40(4):313–317, 1:STN:280:DyaK38zlslClug%3D%3D Buzzi MG, Moskowitz MA (1992) The trigemino-vascular system and migraine. Pathol Biol (Paris) 40(4):313–317, 1:STN:280:DyaK38zlslClug%3D%3D
21.
go back to reference Tfelt-Hansen P, Le H (2009) Calcitonin gene-related peptide in blood: is it increased in the external jugular vein during migraine and cluster headache? A review. J Headache Pain 10(3):137–143, 19330286, 10.1007/s10194-009-0112-8, 1:CAS:528:DC%2BD1MXls1Oksb8%3DPubMedCentralCrossRefPubMed Tfelt-Hansen P, Le H (2009) Calcitonin gene-related peptide in blood: is it increased in the external jugular vein during migraine and cluster headache? A review. J Headache Pain 10(3):137–143, 19330286, 10.1007/s10194-009-0112-8, 1:CAS:528:DC%2BD1MXls1Oksb8%3DPubMedCentralCrossRefPubMed
22.
go back to reference Durham PL, Russo AF (2003) Stimulation of the calcitonin gene-related peptide enhancer by mitogen-activated protein kinases and repression by an antimigraine drug in trigeminal ganglia neurons. J Neurosci 23(3):807–815, 12574409, 1:CAS:528:DC%2BD3sXhtlOrsbY%3DPubMed Durham PL, Russo AF (2003) Stimulation of the calcitonin gene-related peptide enhancer by mitogen-activated protein kinases and repression by an antimigraine drug in trigeminal ganglia neurons. J Neurosci 23(3):807–815, 12574409, 1:CAS:528:DC%2BD3sXhtlOrsbY%3DPubMed
23.
go back to reference Orita S, Eguchi Y, Kamoda H, Arai G, Ishikawa T, Miyagi M et al (2011) Brain-derived neurotrophic factor (BDNF) inhibition at the punctured intervertebral disc downregulates the production of calcitonin gene-related peptide (CGRP) in dorsal root ganglia in rats. Spine (Epub 5 May 2011) Orita S, Eguchi Y, Kamoda H, Arai G, Ishikawa T, Miyagi M et al (2011) Brain-derived neurotrophic factor (BDNF) inhibition at the punctured intervertebral disc downregulates the production of calcitonin gene-related peptide (CGRP) in dorsal root ganglia in rats. Spine (Epub 5 May 2011)
24.
go back to reference Moskowitz MA (1993) Neurogenic inflammation in the pathophysiology and treatment of migraine. Neurology 43(6 Suppl 3):S16–S20, 8389008, 1:STN:280:DyaK3s3nsFGhsA%3D%3DPubMed Moskowitz MA (1993) Neurogenic inflammation in the pathophysiology and treatment of migraine. Neurology 43(6 Suppl 3):S16–S20, 8389008, 1:STN:280:DyaK3s3nsFGhsA%3D%3DPubMed
25.
go back to reference Williamson DJ, Hargreaves RJ (2001) Neurogenic inflammation in the context of migraine. Microsc Res Tech 53(3):167–178, 11301492, 10.1002/jemt.1081, 1:CAS:528:DC%2BD3MXjvVKrur0%3DCrossRefPubMed Williamson DJ, Hargreaves RJ (2001) Neurogenic inflammation in the context of migraine. Microsc Res Tech 53(3):167–178, 11301492, 10.1002/jemt.1081, 1:CAS:528:DC%2BD3MXjvVKrur0%3DCrossRefPubMed
26.
go back to reference Tarsa L, Balkowiec-Iskra E, Kratochvil FJ III, Jenkins VK, McLean A, Brown AL et al (2010) Tooth pulp inflammation increases brain-derived neurotrophic factor expression in rodent trigeminal ganglion neurons. Neuroscience 167(4):1205–1215, 20223282, 10.1016/j.neuroscience.2010.03.002, 1:CAS:528:DC%2BC3cXlsFOhs7w%3DPubMedCentralCrossRefPubMed Tarsa L, Balkowiec-Iskra E, Kratochvil FJ III, Jenkins VK, McLean A, Brown AL et al (2010) Tooth pulp inflammation increases brain-derived neurotrophic factor expression in rodent trigeminal ganglion neurons. Neuroscience 167(4):1205–1215, 20223282, 10.1016/j.neuroscience.2010.03.002, 1:CAS:528:DC%2BC3cXlsFOhs7w%3DPubMedCentralCrossRefPubMed
27.
go back to reference Tanure MT, Gomez RS, Hurtado RC, Teixeira AL, Domingues RB (2010) Increased serum levels of brain-derived neurotropic factor during migraine attacks: a pilot study. J Headache Pain 11(5):427–430, 20556464, 10.1007/s10194-010-0233-0, 1:CAS:528:DC%2BC3cXhtFOqsr7JPubMedCentralCrossRefPubMed Tanure MT, Gomez RS, Hurtado RC, Teixeira AL, Domingues RB (2010) Increased serum levels of brain-derived neurotropic factor during migraine attacks: a pilot study. J Headache Pain 11(5):427–430, 20556464, 10.1007/s10194-010-0233-0, 1:CAS:528:DC%2BC3cXhtFOqsr7JPubMedCentralCrossRefPubMed
28.
go back to reference Bo SH, Davidsen EM, Gulbrandsen P, Dietrichs E, Bovim G, Stovner LJ et al (2009) Cerebrospinal fluid cytokine levels in migraine, tension-type headache and cervicogenic headache. Cephalalgia 29(3):365–372, 19175774, 10.1111/j.1468-2982.2008.01727.x, 1:STN:280:DC%2BD1M7kvV2ksQ%3D%3DCrossRefPubMed Bo SH, Davidsen EM, Gulbrandsen P, Dietrichs E, Bovim G, Stovner LJ et al (2009) Cerebrospinal fluid cytokine levels in migraine, tension-type headache and cervicogenic headache. Cephalalgia 29(3):365–372, 19175774, 10.1111/j.1468-2982.2008.01727.x, 1:STN:280:DC%2BD1M7kvV2ksQ%3D%3DCrossRefPubMed
29.
go back to reference Ishizaki K, Takeshima T, Fukuhara Y, Araki H, Nakaso K, Kusumi M et al (2005) Increased plasma transforming growth factor-beta1 in migraine. Headache 45(9):1224–1228, 16178953, 10.1111/j.1526-4610.2005.00246.xCrossRefPubMed Ishizaki K, Takeshima T, Fukuhara Y, Araki H, Nakaso K, Kusumi M et al (2005) Increased plasma transforming growth factor-beta1 in migraine. Headache 45(9):1224–1228, 16178953, 10.1111/j.1526-4610.2005.00246.xCrossRefPubMed
30.
go back to reference Leao AA (1944) Spreading depression of activity in the cerebral cortex. J Neurophysiol 7:359–390 Leao AA (1944) Spreading depression of activity in the cerebral cortex. J Neurophysiol 7:359–390
31.
go back to reference Olesen J, Larsen B, Lauritzen M (1981) Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol 9(4):344–352, 6784664, 10.1002/ana.410090406, 1:STN:280:DyaL3M7ot1yhsg%3D%3DCrossRefPubMed Olesen J, Larsen B, Lauritzen M (1981) Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol 9(4):344–352, 6784664, 10.1002/ana.410090406, 1:STN:280:DyaL3M7ot1yhsg%3D%3DCrossRefPubMed
32.
go back to reference Rangel YM, Kariko K, Harris VA, Duvall ME, Welsh FA (2001) Dose-dependent induction of mRNAs encoding brain-derived neurotrophic factor and heat-shock protein-72 after cortical spreading depression in the rat. Brain Res Mol Brain Res 88(1–2):103–112, 11295236, 10.1016/S0169-328X(01)00037-7, 1:CAS:528:DC%2BD3MXisVWgsrk%3DCrossRefPubMed Rangel YM, Kariko K, Harris VA, Duvall ME, Welsh FA (2001) Dose-dependent induction of mRNAs encoding brain-derived neurotrophic factor and heat-shock protein-72 after cortical spreading depression in the rat. Brain Res Mol Brain Res 88(1–2):103–112, 11295236, 10.1016/S0169-328X(01)00037-7, 1:CAS:528:DC%2BD3MXisVWgsrk%3DCrossRefPubMed
33.
go back to reference Kariko K, Harris VA, Rangel Y, Duvall ME, Welsh FA (1998) Effect of cortical spreading depression on the levels of mRNA coding for putative neuroprotective proteins in rat brain. J Cereb Blood Flow Metab 18(12):1308–1315, 9850143, 10.1097/00004647-199812000-00005, 1:CAS:528:DyaK1MXitVequg%3D%3DCrossRefPubMed Kariko K, Harris VA, Rangel Y, Duvall ME, Welsh FA (1998) Effect of cortical spreading depression on the levels of mRNA coding for putative neuroprotective proteins in rat brain. J Cereb Blood Flow Metab 18(12):1308–1315, 9850143, 10.1097/00004647-199812000-00005, 1:CAS:528:DyaK1MXitVequg%3D%3DCrossRefPubMed
34.
go back to reference Blandini F, Rinaldi L, Tassorelli C, Sances G, Motta M, Samuele A et al (2006) Peripheral levels of BDNF and NGF in primary headaches. Cephalalgia 26(2):136–142, 16426267, 10.1111/j.1468-2982.2005.01006.x, 1:STN:280:DC%2BD28%2Fptlentw%3D%3DCrossRefPubMed Blandini F, Rinaldi L, Tassorelli C, Sances G, Motta M, Samuele A et al (2006) Peripheral levels of BDNF and NGF in primary headaches. Cephalalgia 26(2):136–142, 16426267, 10.1111/j.1468-2982.2005.01006.x, 1:STN:280:DC%2BD28%2Fptlentw%3D%3DCrossRefPubMed
35.
go back to reference Tietjen GE, Khubchandani J (2009) Platelet dysfunction and stroke in the female migraineur. Curr Pain Headache Rep 13(5):386–391, 19728966, 10.1007/s11916-009-0063-4CrossRefPubMed Tietjen GE, Khubchandani J (2009) Platelet dysfunction and stroke in the female migraineur. Curr Pain Headache Rep 13(5):386–391, 19728966, 10.1007/s11916-009-0063-4CrossRefPubMed
36.
go back to reference Goadsby PJ, Edvinsson L (1994) Human in vivo evidence for trigeminovascular activation in cluster headache. Neuropeptide changes and effects of acute attacks therapies. Brain 117(Pt 3):427–434, 7518321, 10.1093/brain/117.3.427CrossRefPubMed Goadsby PJ, Edvinsson L (1994) Human in vivo evidence for trigeminovascular activation in cluster headache. Neuropeptide changes and effects of acute attacks therapies. Brain 117(Pt 3):427–434, 7518321, 10.1093/brain/117.3.427CrossRefPubMed
37.
go back to reference Di Piero V, Fiacco F, Tombari D, Pantano P (1997) Tonic pain: a SPET study in normal subjects and cluster headache patients. Pain 70(2–3):185–191, 9150292, 10.1016/S0304-3959(96)03318-0CrossRefPubMed Di Piero V, Fiacco F, Tombari D, Pantano P (1997) Tonic pain: a SPET study in normal subjects and cluster headache patients. Pain 70(2–3):185–191, 9150292, 10.1016/S0304-3959(96)03318-0CrossRefPubMed
38.
go back to reference Ren K, Dubner R (2007) Pain facilitation and activity-dependent plasticity in pain modulatory circuitry: role of BDNF-TrkB signaling and NMDA receptors. Mol Neurobiol 35(3):224–235, 17917111, 10.1007/s12035-007-0028-8, 1:CAS:528:DC%2BD2sXht1aisbvMCrossRefPubMed Ren K, Dubner R (2007) Pain facilitation and activity-dependent plasticity in pain modulatory circuitry: role of BDNF-TrkB signaling and NMDA receptors. Mol Neurobiol 35(3):224–235, 17917111, 10.1007/s12035-007-0028-8, 1:CAS:528:DC%2BD2sXht1aisbvMCrossRefPubMed
39.
go back to reference Lu VB, Biggs JE, Stebbing MJ, Balasubramanyan S, Todd KG, Lai AY et al (2009) Brain-derived neurotrophic factor drives the changes in excitatory synaptic transmission in the rat superficial dorsal horn that follow sciatic nerve injury. J Physiol 587(Pt 5):1013–1032 (Epub 2009/01/07), 19124536, 10.1113/jphysiol.2008.166306, 1:CAS:528:DC%2BD1MXjslSmtbY%3D, (Epub 2009/01/07)PubMedCentralCrossRefPubMed Lu VB, Biggs JE, Stebbing MJ, Balasubramanyan S, Todd KG, Lai AY et al (2009) Brain-derived neurotrophic factor drives the changes in excitatory synaptic transmission in the rat superficial dorsal horn that follow sciatic nerve injury. J Physiol 587(Pt 5):1013–1032 (Epub 2009/01/07), 19124536, 10.1113/jphysiol.2008.166306, 1:CAS:528:DC%2BD1MXjslSmtbY%3D, (Epub 2009/01/07)PubMedCentralCrossRefPubMed
Metadata
Title
Brain-derived neurotrophic factor in primary headaches
Authors
Marlene Fischer
Georg Wille
Stephanie Klien
Hind Shanib
Dagny Holle
Charly Gaul
Gregor Broessner
Publication date
01-08-2012
Publisher
Springer Milan
Published in
The Journal of Headache and Pain / Issue 6/2012
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1007/s10194-012-0454-5

Other articles of this Issue 6/2012

The Journal of Headache and Pain 6/2012 Go to the issue

Letter to the Editor

Refractory periods in SUNCT