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Published in: Current Pain and Headache Reports 11/2014

01-11-2014 | Migraine (R Cowan, Section Editor)

Update on Animal Models of Migraine

Authors: Marcela Romero-Reyes, Simon Akerman

Published in: Current Pain and Headache Reports | Issue 11/2014

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Abstract

Migraine is a severe and debilitating disorder of the brain that involves a constellation of neurological symptoms alongside head pain. Its pathophysiology is only beginning to be understood, and is thought to involve activation and sensitization of trigeminovascular nociceptive pathways that innervate the cranial vasculature, and activation of brain stem nuclei. Much of our understanding of migraine pathophysiology stems from research conducted in animal models over the last 30 years, and the development of unique assays in animals that try to model specific aspects of migraine pathophysiology related to particular symptoms. This review will highlight some of the latest findings from these established animal models, as well as discuss the latest in the development of novel approaches in animals to study migraine
Literature
1.
go back to reference Lipton RB, Bigal ME, Diamond M, Freitag F, Reed ML, Stewart WF. Migraine prevalence, disease burden, and the need for preventive therapy. Neurology. 2007;68(5):343–9.PubMedCrossRef Lipton RB, Bigal ME, Diamond M, Freitag F, Reed ML, Stewart WF. Migraine prevalence, disease burden, and the need for preventive therapy. Neurology. 2007;68(5):343–9.PubMedCrossRef
2.
go back to reference Headache Classification Committee of the International Headache Society. The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia. 2013;33(9):629–808.CrossRef Headache Classification Committee of the International Headache Society. The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia. 2013;33(9):629–808.CrossRef
3.
go back to reference Akerman S, Holland PR, Goadsby PJ. Diencephalic and brainstem mechanisms in migraine. Nat Rev Neurosci. 2011;12(10):570–84.PubMedCrossRef Akerman S, Holland PR, Goadsby PJ. Diencephalic and brainstem mechanisms in migraine. Nat Rev Neurosci. 2011;12(10):570–84.PubMedCrossRef
4.
5.
go back to reference Noseda R, Burstein R. Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, CSD, sensitization and modulation of pain. Pain. 2013. Noseda R, Burstein R. Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, CSD, sensitization and modulation of pain. Pain. 2013.
6.
go back to reference Bernstein C, Burstein R. Sensitization of the trigeminovascular pathway: perspective and implications to migraine pathophysiology. J Clin Neurol. 2012;8(2):89–99.PubMedCrossRefPubMedCentral Bernstein C, Burstein R. Sensitization of the trigeminovascular pathway: perspective and implications to migraine pathophysiology. J Clin Neurol. 2012;8(2):89–99.PubMedCrossRefPubMedCentral
7.
go back to reference Goadsby PJ, Lipton RB, Ferrari MD. Migraine–current understanding and treatment. N Engl J Med. 2002;346(4):257–70.PubMedCrossRef Goadsby PJ, Lipton RB, Ferrari MD. Migraine–current understanding and treatment. N Engl J Med. 2002;346(4):257–70.PubMedCrossRef
8.
go back to reference Penfield W, McNaughton F. Dural headache and innervation of the dura mater. Arch Neurol Psychiatry. 1940;44:43–75.CrossRef Penfield W, McNaughton F. Dural headache and innervation of the dura mater. Arch Neurol Psychiatry. 1940;44:43–75.CrossRef
9.
go back to reference Ray BS, Wolff HG. Experimental studies on headache. Pain sensitive structures of the head and their significance in headache. Arch Surg. 1940;41:813–56.CrossRef Ray BS, Wolff HG. Experimental studies on headache. Pain sensitive structures of the head and their significance in headache. Arch Surg. 1940;41:813–56.CrossRef
10.
go back to reference McNaughton FL, Feindel W. Innervation of intracranial structures: a reappraisal. In: Rose FC, editor. Physiological aspects of clinical neurology. Oxford: Blackwell Scientific; 1977. p. 279–93. McNaughton FL, Feindel W. Innervation of intracranial structures: a reappraisal. In: Rose FC, editor. Physiological aspects of clinical neurology. Oxford: Blackwell Scientific; 1977. p. 279–93.
11.
go back to reference Lambert GA, Goadsby PJ, Zagami AS, Duckworth JW. Comparative effects of stimulation of the trigeminal ganglion and the superior sagittal sinus on cerebral blood flow and evoked potentials in the cat. Brain Res. 1988;453(1–2):143–9.PubMedCrossRef Lambert GA, Goadsby PJ, Zagami AS, Duckworth JW. Comparative effects of stimulation of the trigeminal ganglion and the superior sagittal sinus on cerebral blood flow and evoked potentials in the cat. Brain Res. 1988;453(1–2):143–9.PubMedCrossRef
12.
go back to reference Hoskin KL, Zagami AS, Goadsby PJ. Stimulation of the middle meningeal artery leads to Fos expression in the trigeminocervical nucleus: a comparative study of monkey and cat. J Anat. 1999;194(Pt4):579–88.PubMedCrossRefPubMedCentral Hoskin KL, Zagami AS, Goadsby PJ. Stimulation of the middle meningeal artery leads to Fos expression in the trigeminocervical nucleus: a comparative study of monkey and cat. J Anat. 1999;194(Pt4):579–88.PubMedCrossRefPubMedCentral
13.
go back to reference Strassman AM, Raymond SA, Burstein R. Sensitization of meningeal sensory neurons and the origin of headaches. Nature. 1996;384(6609):560–4.PubMedCrossRef Strassman AM, Raymond SA, Burstein R. Sensitization of meningeal sensory neurons and the origin of headaches. Nature. 1996;384(6609):560–4.PubMedCrossRef
14.
go back to reference Strecker T, Dux M, Messlinger K. Increase in meningeal blood flow by nitric oxide - interaction with calcitonin gene-related peptide receptor and prostaglandin synthesis inhibition. Cephalalgia. 2002;22(3):233–41.PubMedCrossRef Strecker T, Dux M, Messlinger K. Increase in meningeal blood flow by nitric oxide - interaction with calcitonin gene-related peptide receptor and prostaglandin synthesis inhibition. Cephalalgia. 2002;22(3):233–41.PubMedCrossRef
15.
go back to reference Kurosawa M, Messlinger K, Pawlak M, Schmidt RF. Increase of meningeal blood flow after electrical stimulation of rat dura mater encephali: mediation by calcitonin gene-related peptide. Br J Pharmacol. 1995;114(7):1397–402.PubMedCrossRefPubMedCentral Kurosawa M, Messlinger K, Pawlak M, Schmidt RF. Increase of meningeal blood flow after electrical stimulation of rat dura mater encephali: mediation by calcitonin gene-related peptide. Br J Pharmacol. 1995;114(7):1397–402.PubMedCrossRefPubMedCentral
16.
go back to reference Akerman S, Holland PR, Hoffmann J. Pearls and pitfalls in experimental in vivo models of migraine: Dural trigeminovascular nociception. Cephalalgia. 2013;33(8):577–92.PubMedCrossRef Akerman S, Holland PR, Hoffmann J. Pearls and pitfalls in experimental in vivo models of migraine: Dural trigeminovascular nociception. Cephalalgia. 2013;33(8):577–92.PubMedCrossRef
17.
18.
go back to reference Bergerot A, Holland PR, Akerman S, Bartsch T, Ahn AH, Maassenvandenbrink A, et al. Animal models of migraine: looking at the component parts of a complex disorder. Eur J Neurosci. 2006;24(6):1517–34.PubMedCrossRef Bergerot A, Holland PR, Akerman S, Bartsch T, Ahn AH, Maassenvandenbrink A, et al. Animal models of migraine: looking at the component parts of a complex disorder. Eur J Neurosci. 2006;24(6):1517–34.PubMedCrossRef
20.
go back to reference Afridi SK, Giffin NJ, Kaube H, Friston KJ, Ward NS, Frackowiak RS, et al. A positron emission tomographic study in spontaneous migraine. Arch Neurol. 2005;62(8):1270–5.PubMedCrossRef Afridi SK, Giffin NJ, Kaube H, Friston KJ, Ward NS, Frackowiak RS, et al. A positron emission tomographic study in spontaneous migraine. Arch Neurol. 2005;62(8):1270–5.PubMedCrossRef
21.
go back to reference Burstein R, Jakubowski M, Garcia-Nicas E, Kainz V, Bajwa Z, Hargreaves R, et al. Thalamic sensitization transforms localized pain into widespread allodynia. Ann Neurol. 2010;68(1):81–91.PubMedCrossRefPubMedCentral Burstein R, Jakubowski M, Garcia-Nicas E, Kainz V, Bajwa Z, Hargreaves R, et al. Thalamic sensitization transforms localized pain into widespread allodynia. Ann Neurol. 2010;68(1):81–91.PubMedCrossRefPubMedCentral
22.
go back to reference Denuelle M, Fabre N, Payoux P, Chollet F, Geraud G. Hypothalamic activation in spontaneous migraine attacks. Headache. 2007;47(10):1418–26.PubMed Denuelle M, Fabre N, Payoux P, Chollet F, Geraud G. Hypothalamic activation in spontaneous migraine attacks. Headache. 2007;47(10):1418–26.PubMed
23.
go back to reference Weiller C, May A, Limmroth V, Juptner M, Kaube H, Schayck RV, et al. Brain stem activation in spontaneous human migraine attacks. Nat Med. 1995;1(7):658–60.PubMedCrossRef Weiller C, May A, Limmroth V, Juptner M, Kaube H, Schayck RV, et al. Brain stem activation in spontaneous human migraine attacks. Nat Med. 1995;1(7):658–60.PubMedCrossRef
24.
go back to reference Goadsby PJ, Charbit AR, Andreou AP, Akerman S, Holland PR. Neurobiology of migraine. Neuroscience. 2009;161(2):327–41.PubMedCrossRef Goadsby PJ, Charbit AR, Andreou AP, Akerman S, Holland PR. Neurobiology of migraine. Neuroscience. 2009;161(2):327–41.PubMedCrossRef
25.•
go back to reference Lambert GA, Hoskin KL, Michalicek J, Panahi SE, Truong L, Zagami AS. Stimulation of dural vessels excites the SI somatosensory cortex of the cat via a relay in the thalamus. Cephalalgia. 2013. doi:10.1177/0333102413508239. Alongside 26, the first studies to how patients can localize their pain to specific cranial regions, through activation of specific cortical regions. Lambert GA, Hoskin KL, Michalicek J, Panahi SE, Truong L, Zagami AS. Stimulation of dural vessels excites the SI somatosensory cortex of the cat via a relay in the thalamus. Cephalalgia. 2013. doi:10.​1177/​0333102413508239​. Alongside 26, the first studies to how patients can localize their pain to specific cranial regions, through activation of specific cortical regions.
26.•
go back to reference Noseda R, Jakubowski M, Kainz V, Borsook D, Burstein R. Cortical projections of functionally identified thalamic trigeminovascular neurons: implications for migraine headache and its associated symptoms. J Neurosci. 2011;31(40):14204–17. Alongside 25, the first studies to how patients can localize their pain to specific cranial regions, through activation of specific cortical regions.PubMedCrossRefPubMedCentral Noseda R, Jakubowski M, Kainz V, Borsook D, Burstein R. Cortical projections of functionally identified thalamic trigeminovascular neurons: implications for migraine headache and its associated symptoms. J Neurosci. 2011;31(40):14204–17. Alongside 25, the first studies to how patients can localize their pain to specific cranial regions, through activation of specific cortical regions.PubMedCrossRefPubMedCentral
27.
go back to reference Goadsby PJ, Edvinsson L, Ekman R. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann Neurol. 1990;28(2):183–7.PubMedCrossRef Goadsby PJ, Edvinsson L, Ekman R. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann Neurol. 1990;28(2):183–7.PubMedCrossRef
28.
go back to reference Tuka B, Helyes Z, Markovics A, Bagoly T, Szolcsanyi J, Szabo N, et al. Alterations in PACAP-38-like immunoreactivity in the plasma during ictal and interictal periods of migraine patients. Cephalalgia. 2013;33(13):1085–95.PubMedCrossRef Tuka B, Helyes Z, Markovics A, Bagoly T, Szolcsanyi J, Szabo N, et al. Alterations in PACAP-38-like immunoreactivity in the plasma during ictal and interictal periods of migraine patients. Cephalalgia. 2013;33(13):1085–95.PubMedCrossRef
29.
go back to reference Zagami AS, Edvinsson L, Hoskin KL, Goadsby PJ. Stimulation of the superior sagittal sinus causes exracranial release of PACAP. Cephalalgia. 1995;14 Suppl 14:109. Zagami AS, Edvinsson L, Hoskin KL, Goadsby PJ. Stimulation of the superior sagittal sinus causes exracranial release of PACAP. Cephalalgia. 1995;14 Suppl 14:109.
30.
go back to reference Zagami AS, Goadsby PJ, Edvinsson L. Stimulation of the superior sagittal sinus in the cat causes release of vasoactive peptides. Neuropeptides. 1990;16(2):69–75.PubMedCrossRef Zagami AS, Goadsby PJ, Edvinsson L. Stimulation of the superior sagittal sinus in the cat causes release of vasoactive peptides. Neuropeptides. 1990;16(2):69–75.PubMedCrossRef
31.
go back to reference Burstein R, Yamamura H, Malick A, Strassman AM. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J-Neurophysiol. 1998;79(2):964–82.PubMed Burstein R, Yamamura H, Malick A, Strassman AM. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J-Neurophysiol. 1998;79(2):964–82.PubMed
32.
go back to reference Burstein R, Yarnitsky D, Goor-Aryeh I, Ransil BJ, Bajwa ZH. An association between migraine and cutaneous allodynia. Ann Neurol. 2000;47(5):614–24.PubMedCrossRef Burstein R, Yarnitsky D, Goor-Aryeh I, Ransil BJ, Bajwa ZH. An association between migraine and cutaneous allodynia. Ann Neurol. 2000;47(5):614–24.PubMedCrossRef
33.
go back to reference Bigal ME, Ashina S, Burstein R, Reed ML, Buse D, Serrano D, et al. Prevalence and characteristics of allodynia in headache sufferers: a population study. Neurology. 2008;70(17):1525–33.PubMedCrossRefPubMedCentral Bigal ME, Ashina S, Burstein R, Reed ML, Buse D, Serrano D, et al. Prevalence and characteristics of allodynia in headache sufferers: a population study. Neurology. 2008;70(17):1525–33.PubMedCrossRefPubMedCentral
34.••
go back to reference Noseda R, Kainz V, Jakubowski M, Gooley JJ, Saper CB, Digre K, et al. A neural mechanism for exacerbation of headache by light. Nat Neurosci. 2010;13(2):239–45. First studies to demonstrate the neural basis by photophobia in migraine, mediated by dural nociceptive afferents.PubMedCrossRefPubMedCentral Noseda R, Kainz V, Jakubowski M, Gooley JJ, Saper CB, Digre K, et al. A neural mechanism for exacerbation of headache by light. Nat Neurosci. 2010;13(2):239–45. First studies to demonstrate the neural basis by photophobia in migraine, mediated by dural nociceptive afferents.PubMedCrossRefPubMedCentral
35.
go back to reference Noseda R, Burstein R. Advances in understanding the mechanisms of migraine-type photophobia. Curr Opin Neurol. 2011;24(3):197–202.PubMedCrossRef Noseda R, Burstein R. Advances in understanding the mechanisms of migraine-type photophobia. Curr Opin Neurol. 2011;24(3):197–202.PubMedCrossRef
37.
go back to reference Akerman S, Holland PR, Lasalandra MP, Goadsby PJ. Oxygen inhibits neuronal activation in the trigeminocervical complex after stimulation of trigeminal autonomic reflex, but not during direct dural activation of trigeminal afferents. Headache. 2009;49(8):1131–43.PubMedCrossRef Akerman S, Holland PR, Lasalandra MP, Goadsby PJ. Oxygen inhibits neuronal activation in the trigeminocervical complex after stimulation of trigeminal autonomic reflex, but not during direct dural activation of trigeminal afferents. Headache. 2009;49(8):1131–43.PubMedCrossRef
38.••
go back to reference Akerman S, Holland PR, Summ O, Lasalandra MP, Goadsby PJ. A translational in vivo model of trigeminal autonomic cephalalgias: therapeutic characterization. Brain. 2012;135(Pt 12):3664–75. Characterisation of an animal model of trigeminal autonomic cephalagias, with prominent trigeminovascular and autonomic features, and describes a novel locus for treatments through the parasympathetic outflow to the cranial vasculature.PubMedCrossRef Akerman S, Holland PR, Summ O, Lasalandra MP, Goadsby PJ. A translational in vivo model of trigeminal autonomic cephalalgias: therapeutic characterization. Brain. 2012;135(Pt 12):3664–75. Characterisation of an animal model of trigeminal autonomic cephalagias, with prominent trigeminovascular and autonomic features, and describes a novel locus for treatments through the parasympathetic outflow to the cranial vasculature.PubMedCrossRef
39.
go back to reference Spencer SE, Sawyer WB, Wada H, Platt KB, Loewy AD. CNS projections to the pterygopalatine parasympathetic preganglionic neurons in the rat: a retrograde transneuronal viral cell body labeling study. Brain Res. 1990;534(1–2):149–69.PubMed Spencer SE, Sawyer WB, Wada H, Platt KB, Loewy AD. CNS projections to the pterygopalatine parasympathetic preganglionic neurons in the rat: a retrograde transneuronal viral cell body labeling study. Brain Res. 1990;534(1–2):149–69.PubMed
40.
go back to reference Lai T-H, Fuh J-L, Wang S-J. Cranial autonomic symptoms in migraine: characteristics and comparison with cluster headache. J Neurol Neurosurg Psychiatry. 2009;80:1116–9.PubMedCrossRef Lai T-H, Fuh J-L, Wang S-J. Cranial autonomic symptoms in migraine: characteristics and comparison with cluster headache. J Neurol Neurosurg Psychiatry. 2009;80:1116–9.PubMedCrossRef
41.•
go back to reference Robert C, Bourgeais L, Arreto CD, Condes-Lara M, Noseda R, Jay T, et al. Paraventricular hypothalamic regulation of trigeminovascular mechanisms involved in headaches. J Neurosci. 2013;33(20):8827–40. Demonstrates paraventricular mediated modulation of nociceptive trigeminovascular neurons, with implications of hypothalamic nuclei involved in the triggering of migraine.PubMedCrossRef Robert C, Bourgeais L, Arreto CD, Condes-Lara M, Noseda R, Jay T, et al. Paraventricular hypothalamic regulation of trigeminovascular mechanisms involved in headaches. J Neurosci. 2013;33(20):8827–40. Demonstrates paraventricular mediated modulation of nociceptive trigeminovascular neurons, with implications of hypothalamic nuclei involved in the triggering of migraine.PubMedCrossRef
42.
go back to reference Rasmussen BK, Olesen J. Migraine with aura and migraine without aura: an epidemiological study. Cephalalgia. 1992;12:221–8.PubMedCrossRef Rasmussen BK, Olesen J. Migraine with aura and migraine without aura: an epidemiological study. Cephalalgia. 1992;12:221–8.PubMedCrossRef
43.
go back to reference Lashley KS. Patterns of cerebral integration indicated by the scotomas of migraine. Arch Neurol Psychiatr. 1941;46:331–9.CrossRef Lashley KS. Patterns of cerebral integration indicated by the scotomas of migraine. Arch Neurol Psychiatr. 1941;46:331–9.CrossRef
44.
go back to reference Lauritzen M. Pathophysiology of the migraine aura. The spreading depression theory. Brain. 1994;117(Pt 1):199–210.PubMedCrossRef Lauritzen M. Pathophysiology of the migraine aura. The spreading depression theory. Brain. 1994;117(Pt 1):199–210.PubMedCrossRef
45.
go back to reference Eikermann-Haerter K, Moskowitz MA. Animal models of migraine headache and aura. Curr Opin Neurol. 2008;21(3):294–300.PubMedCrossRef Eikermann-Haerter K, Moskowitz MA. Animal models of migraine headache and aura. Curr Opin Neurol. 2008;21(3):294–300.PubMedCrossRef
47.
go back to reference Olesen J, Larsen B, Lauritzen M. Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol. 1981;9(4):344–52.PubMedCrossRef Olesen J, Larsen B, Lauritzen M. Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol. 1981;9(4):344–52.PubMedCrossRef
48.
go back to reference Bolay H, Reuter U, Dunn AK, Huang Z, Boas DA, Moskowitz MA. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med. 2002;8(2):136–42.PubMedCrossRef Bolay H, Reuter U, Dunn AK, Huang Z, Boas DA, Moskowitz MA. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med. 2002;8(2):136–42.PubMedCrossRef
49.
go back to reference Zhang X, Levy D, Kainz V, Noseda R, Jakubowski M, Burstein R. Activation of central trigeminovascular neurons by cortical spreading depression. Ann Neurol. 2011;69(5):855–65.PubMedCrossRefPubMedCentral Zhang X, Levy D, Kainz V, Noseda R, Jakubowski M, Burstein R. Activation of central trigeminovascular neurons by cortical spreading depression. Ann Neurol. 2011;69(5):855–65.PubMedCrossRefPubMedCentral
50.
go back to reference Zhang X, Levy D, Noseda R, Kainz V, Jakubowski M, Burstein R. Activation of meningeal nociceptors by cortical spreading depression: implications for migraine with aura. J Neurosci. 2010;30(26):8807–14.PubMedCrossRefPubMedCentral Zhang X, Levy D, Noseda R, Kainz V, Jakubowski M, Burstein R. Activation of meningeal nociceptors by cortical spreading depression: implications for migraine with aura. J Neurosci. 2010;30(26):8807–14.PubMedCrossRefPubMedCentral
51.•
go back to reference Noseda R, Constandil L, Bourgeais L, Chalus M, Villanueva L. hanges of meningeal excitability mediated by corticotrigeminal networks: a link for the endogenous modulation of migraine pain. J Neurosci. 2010;30(43):14420–9. First study to demonstrate that CSD triggered in different cortical regions may inhibit or excite trigeminovascular noxious and innocuous responses.PubMedCrossRef Noseda R, Constandil L, Bourgeais L, Chalus M, Villanueva L. hanges of meningeal excitability mediated by corticotrigeminal networks: a link for the endogenous modulation of migraine pain. J Neurosci. 2010;30(43):14420–9. First study to demonstrate that CSD triggered in different cortical regions may inhibit or excite trigeminovascular noxious and innocuous responses.PubMedCrossRef
52.
go back to reference Lambert GA, Truong L, Zagami AS. Effect of cortical spreading depression on basal and evoked traffic in the trigeminovascular sensory system. Cephalalgia. 2011. Lambert GA, Truong L, Zagami AS. Effect of cortical spreading depression on basal and evoked traffic in the trigeminovascular sensory system. Cephalalgia. 2011.
53.
go back to reference Iversen HK, Olesen J, Tfelt-hansen P. Intravenous Nitroglycerin As an Experimental-Model of Vascular Headache - Basic Characteristics. Pain. 1989;38(1):17–24.PubMedCrossRef Iversen HK, Olesen J, Tfelt-hansen P. Intravenous Nitroglycerin As an Experimental-Model of Vascular Headache - Basic Characteristics. Pain. 1989;38(1):17–24.PubMedCrossRef
54.
go back to reference Schytz HW, Schoonman GG, Ashina M. What have we learnt from triggering migraine? Curr Opin Neurol. 2010;23(3):259–65.PubMedCrossRef Schytz HW, Schoonman GG, Ashina M. What have we learnt from triggering migraine? Curr Opin Neurol. 2010;23(3):259–65.PubMedCrossRef
56.
go back to reference Amin FM, Asghar MS, Hougaard A, Hansen AE, Larsen VA, de Koning PJ, et al. Magnetic resonance angiography of intracranial and extracranial arteries in patients with spontaneous migraine without aura: a cross-sectional study. Lancet Neurol. 2013;12(5):454–61.PubMedCrossRef Amin FM, Asghar MS, Hougaard A, Hansen AE, Larsen VA, de Koning PJ, et al. Magnetic resonance angiography of intracranial and extracranial arteries in patients with spontaneous migraine without aura: a cross-sectional study. Lancet Neurol. 2013;12(5):454–61.PubMedCrossRef
57.
go back to reference Schoonman GG, van der Grond J, Kortmann C, van der Geest RJ, Terwindt GM, Ferrari MD. Migraine headache is not associated with cerebral or meningeal vasodilatation–a 3T magnetic resonance angiography study. Brain. 2008;131(Pt 8):2192–200.PubMedCrossRef Schoonman GG, van der Grond J, Kortmann C, van der Geest RJ, Terwindt GM, Ferrari MD. Migraine headache is not associated with cerebral or meningeal vasodilatation–a 3T magnetic resonance angiography study. Brain. 2008;131(Pt 8):2192–200.PubMedCrossRef
58.
go back to reference Asghar MS, Hansen AE, Amin FM, van der Geest RJ, Koning P, Larsson HB, et al. Evidence for a vascular factor in migraine. Ann Neurol. 2011;69(4):635–45.PubMedCrossRef Asghar MS, Hansen AE, Amin FM, van der Geest RJ, Koning P, Larsson HB, et al. Evidence for a vascular factor in migraine. Ann Neurol. 2011;69(4):635–45.PubMedCrossRef
59.
go back to reference Storer RJ, Akerman S, Goadsby PJ. Calcitonin gene-related peptide (CGRP) modulates nociceptive trigeminovascular transmission in the cat. Br J Pharmacol. 2004;142(7):1171–81.PubMedCrossRefPubMedCentral Storer RJ, Akerman S, Goadsby PJ. Calcitonin gene-related peptide (CGRP) modulates nociceptive trigeminovascular transmission in the cat. Br J Pharmacol. 2004;142(7):1171–81.PubMedCrossRefPubMedCentral
60.
go back to reference Cumberbatch MJ, Williamson DJ, Mason GS, Hill RG, Hargreaves RJ. Dural vasodilation causes a sensitization of rat caudal trigeminal neurones in vivo that is blocked by a 5-HT1B/1D agonist. Br J Pharmacol. 1999;126(6):1478–86.PubMedCrossRefPubMedCentral Cumberbatch MJ, Williamson DJ, Mason GS, Hill RG, Hargreaves RJ. Dural vasodilation causes a sensitization of rat caudal trigeminal neurones in vivo that is blocked by a 5-HT1B/1D agonist. Br J Pharmacol. 1999;126(6):1478–86.PubMedCrossRefPubMedCentral
61.
go back to reference Levy D, Burstein R, Strassman AM. Calcitonin gene-related peptide does not excite or sensitize meningeal nociceptors: implications for the pathophysiology of migraine. Ann Neurol. 2005;58(5):698–705.PubMedCrossRef Levy D, Burstein R, Strassman AM. Calcitonin gene-related peptide does not excite or sensitize meningeal nociceptors: implications for the pathophysiology of migraine. Ann Neurol. 2005;58(5):698–705.PubMedCrossRef
62.
go back to reference Koulchitsky S, Fischer MJ, De Col R, Schlechtweg PM, Messlinger K. Biphasic response to nitric oxide of spinal trigeminal neurons with meningeal input in rat–possible implications for the pathophysiology of headaches. J Neurophysiol. 2004;92(3):1320–8.PubMedCrossRef Koulchitsky S, Fischer MJ, De Col R, Schlechtweg PM, Messlinger K. Biphasic response to nitric oxide of spinal trigeminal neurons with meningeal input in rat–possible implications for the pathophysiology of headaches. J Neurophysiol. 2004;92(3):1320–8.PubMedCrossRef
63.
go back to reference Akerman S, Hoffmann J, Goadsby PJ. A Translational Approach to Studying Triptan-Induced Reversal of Established Central Sensitization of Trigeminovascular Neurons. Cephalalgia. 2013;33(8 (S1)):211. Akerman S, Hoffmann J, Goadsby PJ. A Translational Approach to Studying Triptan-Induced Reversal of Established Central Sensitization of Trigeminovascular Neurons. Cephalalgia. 2013;33(8 (S1)):211.
64.
go back to reference Akerman S, Goadsby PJ. Acute Anti-Migraine Treatments Abort Established Central Sensitization of Trigeminovascular Neurons: Validation of a Novel Translational Approach. Headache. 2014;54(S1):2–3. Akerman S, Goadsby PJ. Acute Anti-Migraine Treatments Abort Established Central Sensitization of Trigeminovascular Neurons: Validation of a Novel Translational Approach. Headache. 2014;54(S1):2–3.
65.
go back to reference Mogil JS, Davis KD, Derbyshire SW. The necessity of animal models in pain research. Pain. 2010;151(1):12–7.PubMedCrossRef Mogil JS, Davis KD, Derbyshire SW. The necessity of animal models in pain research. Pain. 2010;151(1):12–7.PubMedCrossRef
66.••
go back to reference Romero-Reyes M, Ye Y. Pearls and pitfalls in experimental in vivo models of headache: Conscious behavioral research. Cephalalgia. 2013;33(8):566–76. doi:10.1177/0333102412472557. A detailed review of the methodology of behavioral animal models of headache.PubMedCrossRef Romero-Reyes M, Ye Y. Pearls and pitfalls in experimental in vivo models of headache: Conscious behavioral research. Cephalalgia. 2013;33(8):566–76. doi:10.​1177/​0333102412472557​. A detailed review of the methodology of behavioral animal models of headache.PubMedCrossRef
67.
go back to reference Lipton RB, Bigal ME, Ashina S, Burstein R, Silberstein S, Reed ML, et al. Cutaneous allodynia in the migraine population. Ann Neurol. 2008;63(2):148–58.PubMedCrossRefPubMedCentral Lipton RB, Bigal ME, Ashina S, Burstein R, Silberstein S, Reed ML, et al. Cutaneous allodynia in the migraine population. Ann Neurol. 2008;63(2):148–58.PubMedCrossRefPubMedCentral
68.
go back to reference Edelmayer RM, Vanderah TW, Majuta L, Zhang ET, Fioravanti B, De Felice M, et al. Medullary pain facilitating neurons mediate allodynia in headache-related pain. Ann Neurol. 2009;65(2):184–93.PubMedCrossRefPubMedCentral Edelmayer RM, Vanderah TW, Majuta L, Zhang ET, Fioravanti B, De Felice M, et al. Medullary pain facilitating neurons mediate allodynia in headache-related pain. Ann Neurol. 2009;65(2):184–93.PubMedCrossRefPubMedCentral
70.
go back to reference Tfelt-Hansen P, Lous I, Olesen J. Prevalence and significance of muscle tenderness during common migraine attacks. Headache. 1981;21(2):49–54.PubMedCrossRef Tfelt-Hansen P, Lous I, Olesen J. Prevalence and significance of muscle tenderness during common migraine attacks. Headache. 1981;21(2):49–54.PubMedCrossRef
71.
go back to reference Oshinsky ML. Insights from experimental studies into allodynia and its treatment. Curr Pain Headache Rep. 2006;10(3):225–30.PubMedCrossRef Oshinsky ML. Insights from experimental studies into allodynia and its treatment. Curr Pain Headache Rep. 2006;10(3):225–30.PubMedCrossRef
72.
go back to reference Burstein R, Collins B, Jakubowski M. Defeating migraine pain with triptans: a race against the development of cutaneous allodynia. Ann Neurol. 2004;55(1):19–26.PubMedCrossRef Burstein R, Collins B, Jakubowski M. Defeating migraine pain with triptans: a race against the development of cutaneous allodynia. Ann Neurol. 2004;55(1):19–26.PubMedCrossRef
73.
go back to reference Daudia AT, Jones NS. Facial migraine in a rhinological setting. Clin Otolaryngol Allied Sci. 2002;27(6):521–5.PubMedCrossRef Daudia AT, Jones NS. Facial migraine in a rhinological setting. Clin Otolaryngol Allied Sci. 2002;27(6):521–5.PubMedCrossRef
75.
go back to reference Silberstein. Headache and other head pain. 7th ed. New York: Oxford University Press; 2001. Silberstein. Headache and other head pain. 7th ed. New York: Oxford University Press; 2001.
76.
go back to reference Stucky NL, Gregory E, Winter MK, He YY, Hamilton ES, McCarson KE, et al. Sex differences in behavior and expression of CGRP-related genes in a rodent model of chronic migraine. Headache. 2011;51(5):674–92.PubMedCrossRefPubMedCentral Stucky NL, Gregory E, Winter MK, He YY, Hamilton ES, McCarson KE, et al. Sex differences in behavior and expression of CGRP-related genes in a rodent model of chronic migraine. Headache. 2011;51(5):674–92.PubMedCrossRefPubMedCentral
77.
go back to reference Bates E, Nikai T, Brennan K, Fu YH, Charles A, Basbaum A et al. Sumatriptan alleviates nitroglycerin-induced mechanical and thermal allodynia in mice. Cephalalgia. 2009. Bates E, Nikai T, Brennan K, Fu YH, Charles A, Basbaum A et al. Sumatriptan alleviates nitroglycerin-induced mechanical and thermal allodynia in mice. Cephalalgia. 2009.
79.••
go back to reference Pradhan AA, Smith ML, Zyuzin J, Charles A. delta-Opioid receptor agonists inhibit migraine-related hyperalgesia, aversive state and cortical spreading depression in mice. Br J Pharmacol. 2014;171(9):2375–84. doi:10.1111/bph.12591. Use of conditioned place aversion in a model of chronic migraine with the use of NTG.PubMedCrossRef Pradhan AA, Smith ML, Zyuzin J, Charles A. delta-Opioid receptor agonists inhibit migraine-related hyperalgesia, aversive state and cortical spreading depression in mice. Br J Pharmacol. 2014;171(9):2375–84. doi:10.​1111/​bph.​12591. Use of conditioned place aversion in a model of chronic migraine with the use of NTG.PubMedCrossRef
81.
82.
go back to reference Backonja MM, Stacey B. Neuropathic pain symptoms relative to overall pain rating. J Pain. 2004;5(9):491–7.PubMedCrossRef Backonja MM, Stacey B. Neuropathic pain symptoms relative to overall pain rating. J Pain. 2004;5(9):491–7.PubMedCrossRef
83.•
go back to reference Romero-Reyes M, Akerman S, Nguyen E, Vijjeswarapu A, Hom B, Dong HW, et al. Spontaneous Behavioral Responses in the Orofacial Region: A Model of Trigeminal Pain in Mouse. Headache. 2013;53(1):137–51. Characteriation of spontaneous (non-evoked) grooming nociceptive behaviors in the orofacial region.PubMedCrossRefPubMedCentral Romero-Reyes M, Akerman S, Nguyen E, Vijjeswarapu A, Hom B, Dong HW, et al. Spontaneous Behavioral Responses in the Orofacial Region: A Model of Trigeminal Pain in Mouse. Headache. 2013;53(1):137–51. Characteriation of spontaneous (non-evoked) grooming nociceptive behaviors in the orofacial region.PubMedCrossRefPubMedCentral
84.•
go back to reference Melo-Carrillo A, Lopez-Avila A. A chronic animal model of migraine, induced by repeated meningeal nociception, characterized by a behavioral and pharmacological approach. Cephalalgia. 2013;33(13):1096–105. doi:10.1177/0333102413486320. Chronic model of migraine who presents spontaneos (non-evoked) behaviors as unilateral grooming in response to inflammatory soup infusion.PubMedCrossRef Melo-Carrillo A, Lopez-Avila A. A chronic animal model of migraine, induced by repeated meningeal nociception, characterized by a behavioral and pharmacological approach. Cephalalgia. 2013;33(13):1096–105. doi:10.​1177/​0333102413486320​. Chronic model of migraine who presents spontaneos (non-evoked) behaviors as unilateral grooming in response to inflammatory soup infusion.PubMedCrossRef
85.
go back to reference Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, et al. Coding of facial expressions of pain in the laboratory mouse. Nat Methods. 2010;7(6):447–9.PubMedCrossRef Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, et al. Coding of facial expressions of pain in the laboratory mouse. Nat Methods. 2010;7(6):447–9.PubMedCrossRef
86.
go back to reference van den Maagdenberg AM, Pietrobon D, Pizzorusso T, Kaja S, Broos LA, Cesetti T, et al. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron. 2004;41(5):701–10.PubMedCrossRef van den Maagdenberg AM, Pietrobon D, Pizzorusso T, Kaja S, Broos LA, Cesetti T, et al. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron. 2004;41(5):701–10.PubMedCrossRef
88.••
go back to reference Chanda ML, Tuttle AH, Baran I, Atlin C, Guindi D, Hathaway G, et al. Behavioral evidence for photophobia and stress-related ipsilateral head pain in transgenic Cacna1a mutant mice. Pain. 2013;154(8):1254–62. doi:10.1016/j.pain.2013.03.038. Multiple behavioral assessments including photophobia supporting Cacna1a mice as a reliable model to study migraine pathophysiology and to screen novel therapeutics.PubMedCrossRef Chanda ML, Tuttle AH, Baran I, Atlin C, Guindi D, Hathaway G, et al. Behavioral evidence for photophobia and stress-related ipsilateral head pain in transgenic Cacna1a mutant mice. Pain. 2013;154(8):1254–62. doi:10.​1016/​j.​pain.​2013.​03.​038. Multiple behavioral assessments including photophobia supporting Cacna1a mice as a reliable model to study migraine pathophysiology and to screen novel therapeutics.PubMedCrossRef
89.
go back to reference Okamoto K, Tashiro A, Chang Z, Bereiter DA. Bright light activates a trigeminal nociceptive pathway. Pain. 149(2):235-42. Okamoto K, Tashiro A, Chang Z, Bereiter DA. Bright light activates a trigeminal nociceptive pathway. Pain. 149(2):235-42.
90.
go back to reference Recober A, Kuburas A, Zhang Z, Wemmie JA, Anderson MG, Russo AF. Role of calcitonin gene-related peptide in light-aversive behavior: implications for migraine. J Neurosci. 2009;29(27):8798–804.PubMedCrossRefPubMedCentral Recober A, Kuburas A, Zhang Z, Wemmie JA, Anderson MG, Russo AF. Role of calcitonin gene-related peptide in light-aversive behavior: implications for migraine. J Neurosci. 2009;29(27):8798–804.PubMedCrossRefPubMedCentral
91.
go back to reference Recober A, Kaiser EA, Kuburas A, Russo AF. Induction of multiple photophobic behaviors in a transgenic mouse sensitized to CGRP. Neuropharmacology. 2009. Recober A, Kaiser EA, Kuburas A, Russo AF. Induction of multiple photophobic behaviors in a transgenic mouse sensitized to CGRP. Neuropharmacology. 2009.
92.
go back to reference Malick A, Jakubowski M, Elmquist JK, Saper CB, Burstein R. A neurohistochemical blueprint for pain-induced loss of appetite. Proc Natl Acad Sci U S A. 2001;98(17):9930–5.PubMedCrossRefPubMedCentral Malick A, Jakubowski M, Elmquist JK, Saper CB, Burstein R. A neurohistochemical blueprint for pain-induced loss of appetite. Proc Natl Acad Sci U S A. 2001;98(17):9930–5.PubMedCrossRefPubMedCentral
95.
go back to reference van den Maagdenberg AM, Pizzorusso T, Kaja S, Terpolilli N, Shapovalova M, Hoebeek FE, et al. High cortical spreading depression susceptibility and migraine-associated symptoms in Ca(v)2.1 S218L mice. Ann Neurol. 2010;67(1):85–98.PubMedCrossRef van den Maagdenberg AM, Pizzorusso T, Kaja S, Terpolilli N, Shapovalova M, Hoebeek FE, et al. High cortical spreading depression susceptibility and migraine-associated symptoms in Ca(v)2.1 S218L mice. Ann Neurol. 2010;67(1):85–98.PubMedCrossRef
97.
go back to reference Mathew R, Andreou AP, Chami L, Bergerot A, van den Maagdenberg AM, Ferrari MD, et al. Immunohistochemical characterization of calcitonin gene-related peptide in the trigeminal system of the familial hemiplegic migraine 1 knock-in mouse. Cephalalgia. 2011;31(13):1368–80. doi:10.1177/0333102411418847.PubMedCrossRef Mathew R, Andreou AP, Chami L, Bergerot A, van den Maagdenberg AM, Ferrari MD, et al. Immunohistochemical characterization of calcitonin gene-related peptide in the trigeminal system of the familial hemiplegic migraine 1 knock-in mouse. Cephalalgia. 2011;31(13):1368–80. doi:10.​1177/​0333102411418847​.PubMedCrossRef
98.
go back to reference Park J, Moon H, Akerman S, Holland PR, Lasalandra MP, Andreou AP, et al. Differential trigeminovascular nociceptive responses in the thalamus in the familial hemiplegic migraine 1 knock-in mouse: A Fos protein study. Neurobiol Dis. 2014;64:1–7.PubMedCrossRef Park J, Moon H, Akerman S, Holland PR, Lasalandra MP, Andreou AP, et al. Differential trigeminovascular nociceptive responses in the thalamus in the familial hemiplegic migraine 1 knock-in mouse: A Fos protein study. Neurobiol Dis. 2014;64:1–7.PubMedCrossRef
99.
go back to reference Xu Y, Padiath QS, Shapiro RE, Jones CR, Wu SC, Saigoh N, et al. Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature. 2005;434(7033):640–4. doi:10.1038/nature03453.PubMedCrossRef Xu Y, Padiath QS, Shapiro RE, Jones CR, Wu SC, Saigoh N, et al. Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature. 2005;434(7033):640–4. doi:10.​1038/​nature03453.PubMedCrossRef
100.••
go back to reference Brennan KC, Bates EA, Shapiro RE, Zyuzin J, Hallows WC, Huang Y, et al. Casein kinase idelta mutations in familial migraine and advanced sleep phase. Sci Transl Med. 2013;5(183):183ra56. 1-11. Demonstration of genetic link to migraine that is not related to familial hemiplegic migraine, but a sleep disorder, and the first characterisation of a mutant mouse carrying the human gene mutation and its migrainous phenotype.PubMedCrossRef Brennan KC, Bates EA, Shapiro RE, Zyuzin J, Hallows WC, Huang Y, et al. Casein kinase idelta mutations in familial migraine and advanced sleep phase. Sci Transl Med. 2013;5(183):183ra56. 1-11. Demonstration of genetic link to migraine that is not related to familial hemiplegic migraine, but a sleep disorder, and the first characterisation of a mutant mouse carrying the human gene mutation and its migrainous phenotype.PubMedCrossRef
Metadata
Title
Update on Animal Models of Migraine
Authors
Marcela Romero-Reyes
Simon Akerman
Publication date
01-11-2014
Publisher
Springer US
Published in
Current Pain and Headache Reports / Issue 11/2014
Print ISSN: 1531-3433
Electronic ISSN: 1534-3081
DOI
https://doi.org/10.1007/s11916-014-0462-z

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