Pathophysiology of Headache Past and Present
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1 Headache ISSN C 2007 the Author doi: /j x Journal compilation C 2007 American Headache Society Published by Blackwell Publishing Pathophysiology of Headache Past and Present Michael A. Moskowitz, MD, M.Sc. (Hon) (Headache 2007;47 [Suppl 1]:S58-S63) In 1979 my laboratory published its first article on migraine in The Lancet, and it was entitled Neurotransmitters and the fifth cranial nerve: Is there a relation to the headache phase of migraine? 1 In this article, we hypothesized that the trigeminal nerve was a critical component in the pathogenesis of migraine. At that time, the sensory innervation to the blood vessels of the circle of Willis was unknown. We believed that such a pathway, if it existed, may contain vasoactive neuropeptides such as substance P which would be released into the meninges. Because hemicranial pain was so prevalent in many migraineurs, we wondered whether or not peptide neurotransmitters might be implicated in an ipsilaterally projecting pathway from the trigeminal ganglia to the meninges and its blood vessels. The headache phase of migraine may develop as a result of an abnormal interaction and perhaps abnormal release of vasoactive neurotransmitters from terminals of the trigeminal nerve with surrounding large intracranial and extracranial blood vessels. These blood vessels, which dilate during the headache phase of migraine, are thought to receive axonal projections from all three divisions of the trigeminal nerve. Substance P, a potent vasodilating peptide, seems to be released from From the Harvard-MIT Division of Health Science and Technology, Cambridge, MA, USA; and Stroke and Neurovascular Regulation Laboratory, Massachusetts General Hospital, Charlestown, MA, USA. Address all correspondence to Dr. Michael A. Moskowitz, Massachusetts General Hospital, th Street, Room 6403, Stroke and Neurovascular Regulation Laboratory, Charlestown, MA , USA. trigeminal nerve endings in response to nervous stimulation and is involved in the transmission of painful stimuli within the periphery. The abnormal release of Substance P, or as yet unidentified peptides or other transmitters from the fifth cranial nerve, may explain both the hemicranial pain and the vasodilation, which are characteristics of the headache phase of migraine. Evidence that peptides and other transmitters participate in the pathophysiology of migrainous headaches might suggest new strategies for the prophylaxis and treatment. 1 For the next 15 years, our lab s research work focused on defining the anatomy, identifying the peptide transmitters, defining the receptor populations expressed on primary afferents, and building models, which may impact the treatment of humans. The term trigeminovascular system was coined in In 1984 we published the Neurobiology of vascular head pain 3 in which we considered the impact of the release of vasodilating peptides and the permeability promoting peptide. Stimulation of the trigeminal ganglia causes the release of peptides within the TVS. Among trigeminal axons projecting into the meninges, calcitonin gene related peptide (CGRP) immunoreactive neurons predominate (40% of all cells), whereas a smaller number of neurons contains substance P (SP, 18%), nitric oxide synthase (NOS, 15%), and other. 4 CGRP and SP potently relax the human middle meningeal artery in vitro. 5 Even though CGRP (and subsequent vasodilatation) does not reportedly excite or directly sensitize meningeal nociceptors, 6 it can indicate migraine attacks. 7 Possibly, the involvement of CGRP in migraine depends upon its role as a central neurotransmitter rather than through vasodilation and S58
2 Headache S59 activation of meningeal nociceptors. 8 In fact, a recent clinical trial with a neuropeptide receptor antagonist (CGRP) successfully aborted migraine headaches; 9 thus, CGRP is an important therapeutic target for acute migraine treatment. We also speculated on the possible existence of prejunctional 5-HT receptor populations and their importance to migraine, which also foreshadowed the development of a 5-HT 1F receptor agonist. In 1984, possible triggers of the trigeminal system and initiators of pain were discussed as summarized below: Spreading depression and vascular headaches it is reasonable to postulate that the headaches in classic migraine are initiated by activity within the central nervous system. Stress, trauma, or brain injury provoke, initiate, or relate temporally to their onset. Sleep tends to alleviate or terminate vascular headaches but is associated with the onset of cluster headaches. The brain appears to trigger migraine headaches because cortical spreading depression is the most common initiating event in migraine attacks. Somewhat paradoxically, Leao reported rapid and marked dilation of pial arteries and veins shortly after the onset of electrical inactivity, which is a part of this wave of spreading depression. Extracellular concentrations of potassium reach as high as 60 mm and have been measured in tandem with the wave of spreading depression. These increases are sufficient to depolarize trigeminal nerve fibers surrounding pial arteries, and could provide one mechanism linking the aura and painful phase of migraine headaches. 3 In fact, defining events that initiate an attack by triggering the trigeminal nerve continue as a major focus of research today. We know that a propagating electrophysiological event such as cortical spreading depression (CSD), expressed clinically as an aura, develops in brain. 10,11 Several studies suggest that CSD is noxious and can trigger headaches (Fig. 1). Unfortunately, auras have not been defined or captured by high-resolution electrophysiological techniques. The strongest evidence was provided by indirect methods that assess flow or tissue oxygenation, albeit with high temporal and spatial resolution. Nevertheless, the depolarization and release of constituents from neurons and glia seem to be the candidate event occurring prior to onset of the headache and a trigger for headache. Fig 1. Schematic showing the potential pathophysiological relationships in migraine with aura. Susceptibility factors (genes) and specific triggering events within the environment alter the susceptibility to CSD and promote its initiation and propagation. Cortical spreading depression is accompanied by released constituents from brain and blood vessels that have been hypothesized to activate the trigeminal innervation of the meninges. This event is facilitated by protease alteration of basal lamina and other membrane proteins. Within brainstem, activation of trigeminal nucleus caudalis triggers the subsequent activation of preganglionic parasympathetic neurons and subsequently parasympathetic fibers innervating the meninges. The rostral transmission of information from the nucleus caudalis may lead to the generation of pain, whereas both the trigeminal and parasympathetic reflex cause meningeal dilation. Other triggers such as from the circulation or blood vessel wall may be important as well, and not require triggering factors released from brain to cause headache. A few years ago, Hadjikhani and colleagues reported the results of an MRI study in a patient who could induce his own migraine attack. 12 Using highresolution BOLD-MRI, BOLD, the basis for functional imaging, detects the ratio of non-paramagnetic oxygenated Hb to paramagnetic deoxy-hb. As a measure of oxygen delivery minus consumption, it is influenced by neuronal activity including flow, volume and oxygen consumption. Hadjikhani mapped changes within occipital cortex during visual aura. She found a marked perturbation or change in the BOLD signal, which developed sequentially along consecutive regions of calcarine cortex. This perturbation in the
3 S60 April 2007 BOLD signal was identical from voxel-to-voxel along calcarine cortex, differing only with respect to the time of onset, beginning posteriorly and spreading anteriorly. We inferred from this study that migraine aura is accompanied by a propagating brain event, which is retinotopically related to the visual percept (moving from central to peripheral visual fields). She interpreted the changes in BOLD signal as first, an increase in blood flow lasting a few minutes, followed by a longer lasting decrease in blood flow and vasodilation that dropped below baseline levels. This sequence of events is similar to what is observed during cortical spreading depression and documented repeatedly in rodent or cat cortex. Based on the propagation velocity (which is usually 2-3 mm per minute in the human and rat), and the pattern of vasodilation followed by vasoconstriction (characteristic of cortical spreading depression), it seemed reasonable to conclude that an event closely resembling cortical spreading depression was causing this patient s migraine visual aura. Additionally, spreading depression was reported to occur within the cerebellum in experimental studies at a characteristic rate of 2-3 mm per minute, 13 and has been identified in hippocampus, basal ganglia, and many other silent areas within cerebral cortex. What is the relevance of the spreading depression model to synaptic events that occur in the migraine brain? First, excitatory amino acid glutamate and the NMDA receptor are important. When injected or applied topically, excitatory amino acids trigger cortical spreading depression. As proposed by van Harreveld, 14 CSD propagation is based on glutamate release, and in fact, glutamate itself has been shown to induce SD when applied to the cortex. Since Marrannes et al confirmed that the NMDA-receptor is an important component in the generation and depropagation of SD and associated inward currents, a variety of NMDA-receptor antagonists have been shown to block cortical SD Moreover, CSD is triggered by energy failure as, for example, in stroke or trauma. Cortical spreading depression is triggered by ouabain, a digitalis-like compound that inhibits sodium-potassium ATPase, an important ion pump ridding the cell of Na+ in exchange for K +. Cortical spreading depression also causes hemiparesis in experimental animals that lasts for hours suggesting that it can cause neurological symptoms. A reason for discussing cortical spreading depression and glutamate relates to the question of how migraine may develop as a consequence of genetic mutations causing rare forms of migraine, and possibly by extrapolation to more common types. Familial hemiplegic migraine (type 1) is caused by a gain of function mutation in the α 1A subunit of calcium channel 19 that controls glutamate release into the synaptic cleft (so-called P/Q calcium channel). It also is associated with mutations in subunit proteins comprising sodium-potassium ATPase (type 2). 20 The life cycle of a glutamate molecule at the synapse is shown in Figure 2. Upon initiation of neuronal depolarization, voltage-sensitive calcium channels open. This allows calcium to enter the nerve ending, and glutamate is then released. Glutamate binds to the postsynaptic membrane receptor, and then is cleared from the synapse by the astrocyte transporters to terminate the depolarization response. The astrocyte has 2 important tasks. One is to rid itself of glutamate, which it does by recycling it and moving it back into the neuron. It must rid itself of sodium by exporting it in exchange for potassium ions. If the sodium-potassium pump fails, potassium accumulates extracellularly, and it levels are high enough, can initiate cortical spreading depression. High intracellular sodium prevents glutamate uptake by the transporter because the transporter is driven by a steep sodium gradient from outside to inside the cell. As a consequence of Na, K + pump failure, glutamate builds up in the synaptic cleft and extracellular potassium increases. Both are associated with the initiation of CSD. In fact, a knock-in mouse expressing the α 1A mutation shows an increased susceptibility to CSD. 22 CSD has been further implicated in migraine based on recently published data by Ayata and colleagues 23 showing that migraine prophylactic drugs block the susceptibility to CSD triggered by 2 different stimuli (chemical or electrical) in 2 different species (rats and mice). Acute treatment was not effective. Longer treatment duration corresponded to better CSD suppression. The 5 tested drugs (topiramate, propranolol, valproate, methysergide, and amitriptyline) are pharmacologically and chemically distinct.
4 Headache S61 Fig 2. The relationship between glutamate, calcium channel, astrocytes, and the sodium potassium pump suggest how gain-offunction and loss-of-function mutations in specific genes may increase susceptibility toward CSD (from Moskowitz et al. Ann Neurol with permission). Cav2.1 channels are mainly located in presynaptic glutamatergic terminals and regulate neurotransmitter release as well as dendritic excitability. Presynaptic Ca-influx increases glutamate release and mutated calcium channels in FHM-1 show enhanced opening of Cav2.1 and increased glutamate release. Increased excitability in FHM-2 arises from sodium pump failure particularly in the astrocytic Na-K ATPase leading to augmented extracellular levels of potassium and glutamate. Both increased potassium and glutamate initiate cortical spreading depression. Although the precise mechanism(s) remain for study, these results may enable future research to identify specific cellular and molecular targets important in the design of more effective and safe prophylactic drugs. Historically, there have been 2 hypotheses regarding the pathogenesis of migraine. One is that migraine originates in the brainstem and the other is that it originates in the cortex. The 2 are not mutually exclusive. The brainstem hypothesis is supported by the concept of a key role for descending modulation, and a change in modulation from rostral structures, activating the brainstem leading to initiation of a migraine attack. Alternatively (or perhaps in addition), migraine may be initiated, at least in some, via a change in susceptibility to CSD. It may turn out that CSD can be modified by rostrally projecting pathways arising from the brainstem. The challenge is to establish this experimentally. There is strengthening evidence to suggest that CSD is a noxious event. Twelve years ago we reported that following CSD, the early immediate response gene c-fos was activated in lamina I, II of the trigeminal nucleus caudalis. 24 With the development of new optical imaging technology, we recently established a link between cortical spreading depression and activation of the trigeminal system. During CSD, blood flow and vessel caliber significantly increased within the middle meningeal artery, and this increase was due to a trigeminal autonomic brain stem-dependent reflex. This reflex is initiated by intense neuroglial depolarization that appears sufficient to drive trigeminal afferents terminating within the meninges and trigeminal nucleus caudalis. 25 To block this afferent autonomic reflex arc, we sectioned the trigeminal innervation and the efferent parasympathetic projections to the cortex. This autonomic loop may be one of the explanations for parasympathetic activation during cluster headache. 26 The precise cause for pain is not known. We postulated that a wave of CSD moves slowly along cortex releasing potassium, arachidonic acid, hydrogen ions, and nitric oxide. This leads to depolarization of the trigeminal afferent loop of the reflex arc (Fig. 3). This in turn leads to brainstem activation. Parasympathetic efferents and trigeminal activation cause vasodilation, and plasma leakage within the dura mater. 21
5 S62 April 2007 Fig 3. This illustration shows the relationship between the trigeminal nerve, meninges, brainstem, and parasympathetic efferents. Cortical spreading depression releases constituents into the brain, which approximates meningeal afferents and when critical levels are reached, discharges trigeminal fibers. This causes orthodromic transmission within trigeminovascular system to activate trigeminal nucleus caudalis and subsequently the parasympathetic efferents projecting from the sphenopalatine ganglion (Reprinted from Iadecola et al, ). Several mechanisms may enable levels of released brain and blood components to approximate and activate the trigeminovascular system during the aura. We explored the possibility that CSD increased proteases that degrade membrane proteins. During CSD, matrix metalloproteinases (MMP) degrade laminin, collagen type IV, a critical component of brain blood vessels. MMP-9 is activated within 15 minutes in blood vessels and lasts for many hours (12 hours). 27 In summary, the data suggest that migraine is a disturbance of the most important visceral organ, the brain. Cortical spreading depression appears to cause migraine visual aura. There may be cases of migraine without aura that are the consequence of CSD-like events within brain (see Woods et al 28 ). Therefore, it is important to improve upon the diagnosis of migraine and classify patients using criteria in addition to those elicited at the bedside. Conflict of Interest: None REFERENCES 1. Moskowitz MA, Reinhard JF Jr, Romero J, Melamed E, Pettibone DJ. Neurotransmitters and the fifth cranial nerve: Is there a relation to the headache phase of migraine? The Lancet. 1979;2:
6 Headache S63 2. Liu-Chen LY, Mayberg MR, Moskowitz MA. Immunohistochemical evidence for a substance P- containing trigeminovascular pathway to pial arteries in cats. Brain Res. 1983;268: Moskowitz MA. The neurobiology of vascular head pain. Ann Neurol. 1984;16: Edvinsson L. Sensory nerves in man and their role in primary headaches. Cephalalgia Sep;21(7): Jansen I, Uddman R, Ekman R, Olesen J, Ottosson A, Edvinsson L. Distribution and effects of neuropeptide Y, vasoactive intestinal peptide, substance P, and calcitonin gene-related peptide in human middle meningeal arteries: comparison with cerebral and temporal arteries. Peptides May-Jun;13(3): Levy D, Burstein R, Strassman AM. Calcitonin generelated peptide does not excite or sensitize meningeal nociceptors: implications for the pathophysiology of migraine. Ann Neurol Nov;58(5): Lassen LH, Haderslev PA, Jacobsen VB, Iversen HK, Sperling B, Olesen J. CGRP may play a causative role in migraine. Cephalalgia Feb;22(1): Strassman AM, Levy D. Response properties of dural nociceptors in relation to headache. J Neurophysiol Mar;95(3): Olesen J, Diener HC, Husstedt IW, et al. Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N Engl J Med. 2004;350: Olesen J, Larsen B, Lauritzen M. Focal hyperemia followed by spreading oligemia and impaired activation of rcbf in classic migraine. Ann Neurol. 1981;9: Cao Y, Welch KMA, Aurora S, et al. Functional MRI- BOLD of visually triggered headache in patients with migraine. Arch Neurol. 1999;56: Hadjikhani N, Sanchez Del Rio M, Wu O, et al. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA. 2001;98: Chen G, Dunbar RL, Gao W, Ebner TJ. Role of calcium, glutamate neurotransmission, and nitric oxide in spreading acidification and depression in the cerebellar cortex. J Neurosci. 2001;21: Van Harreveld A, Fifkova E. Glutamate release from the retina during spreading depression. J Neurobiol. 1970;2: Marrannes R, Willems R, De Prins E, Wauquier A. Evidence for a role of the N-methyl-D-aspartate (NMDA) receptor in cortical spreading depression in the rat. Brain Res Aug 9;457(2): Lauritzen M, Hansen AJ. The effect of glutamate receptor blockade on anoxic depolarization and cortical spreading depression. J Cereb Blood Flow Metab Mar;12(2): Anderson TR, Andrew RD. Spreading depression: imaging and blockade in the rat neocortical brain slice. J Neurophysiol Nov;88(5): Moskowitz MA, Bolay H, Dalkara T. Deciphering migraine mechanisms: Clues from familial hemiplegic migraine genotypes. Ann Neurol. 2004;55: Ophoff RA, Terwindt GM, Vergouwe MN, et al. Familial hemiplegic migraine and episodic ataxia type 2 are caused by mutations in the calcium channel gene CACNLIA4. Cell. 1996;87: De Fusco M, Marconi R, Silvestri L, et al. Haplioinsufficiency of ATP1A2 encoding the Na+/K+ pump alpha2 subunit gene is responsible for familial hemiplegic migraine type 2. Nat Genet. 2003;33: Iadecola C. From CSD to headache: A long and winding road. Nat Med. 2002;8: van den Maagdenbeurg AM, Pietrobon D, Pizzorusso T, et al. A Cacna1a knockin migrainene mouse model with increased susceptibility to cortical spreading depression. Neuron. 2004;41: Ayata C, Jin H, Kudo C, Dalkara T, Moskowitz MA. Suppression of cortical spreading depression in migraine prophylaxis. Ann Neurol Apr;59(4): Moskowitz MA, Nozaki K, Kraig RP. Neocortical spreading depression provokes the expression of c- fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J Neurosci. 1993;13: 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: Moskowitz MA. Cluster headache: Evidence for a pathophysiologic focus in the superior pericarotid cavernous sinus plexus. Headache. 1988;28: Gursoy-Ozdemir Y, Qiu J, Matsuoka N, et al. Cortical spreading depression activates and upregulates MMP-9. J Clin Invest. 2004;113: Woods RP, Iacoboni M, Mazziotta JC. Brief report: Bilateral spreading cerebral hypoperfusion during spontaneous migraine headache. N Engl J Med. 1994;331:
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