Vol 81, No 4 (2022)
Review article
Published online: 2021-10-28
The posterior cranial fossa’s dura mater innervation and its clinical implication in headache: a comprehensive review
Abstract
The pathophysiology of migraines and headaches has been a point of interest in research as they affect a large subset of the population, and the exact mechanism is still unclear. There is evidence implicating the dura mater and its innervation as contributing factors, especially at the posterior cranial fossa. Many modes of innervation have been identified, including the dorsal root ganglion, superior cervical ganglion, vagus nerve, trigeminal nerve, hypoglossal nerve, and glossopharyngeal nerve. While the exact method of innervation is still under investigation, there is strong evidence suggesting that different types of headaches (migraine vs. occipital vs. cervicogenic) are due to specific nerves and inflammatory mediators that contribute to the dura mater in some way. By understanding how these innervation patterns manifest clinically, the course of treatment can be tailored based on the physiological aetiology. Here, we present a comprehensive literature review of the current research regarding the innervation of the dura mater of the posterior cranial fossa and its clinical implications.
Keywords: anatomynervescraniummeningesheadache
References
- Adeeb N, Mortazavi MM, Tubbs RS, et al. The cranial dura mater: a review of its history, embryology, and anatomy. Childs Nerv Syst. 2012; 28(6): 827–837.
- Al-Zahrawi AZ. The father of surgery. ANZ J Surg. 2007; 77(A83).
- Ambroise P. The Works of Ambrose Parey, Chyrurgeon to Henry II, Francis II, Charles IX, and Henry III, Kings of France. J Hindmarsh, London 1691.
- Asghar MS, Hansen AE, Kapijimpanga T, et al. Dilation by CGRP of middle meningeal artery and reversal by sumatriptan in normal volunteers. Neurology. 2010; 75(17): 1520–1526.
- Avona A, Burgos-Vega C, Burton MD, et al. Dural calcitonin gene-related peptide produces female-specific responses in rodent migraine models. J Neurosci. 2019; 39(22): 4323–4331.
- Berge JK, Bergman RA. Variations in size and in symmetry of foramina of the human skull. Clin Anat. 2001; 14(6): 406–413.
- Bigalke H. Botulinum toxin: application, safety, and limitations. Curr Top Microbiol Immunol. 2013; 364: 307–317.
- Biondi DM, Biondi DM, Biondi DM. Cervicogenic headache: mechanisms, evaluation, and treatment strategies. J Am Osteopath Assoc. 2000; 100(9 Suppl): S7–S14.
- Bogduk N, Windsor M, Inglis A. The innervation of the cervical intervertebral discs. Spine (Phila Pa 1976). 1988; 13(1): 2–8.
- Bogduk N. Cervicogenic headache: anatomic basis and pathophysiologic mechanisms. Curr Pain Headache Rep. 2001; 5(4): 382–386.
- Burgos-Vega CC, Quigley LD, Avona A, et al. Dural stimulation in rats causes brain-derived neurotrophic factor-dependent priming to subthreshold stimuli including a migraine trigger. Pain. 2016; 157(12): 2722–2730.
- Burnstock G, Krügel U, Abbracchio MP, et al. Purinergic signalling: from normal behaviour to pathological brain function. Prog Neurobiol. 2011; 95(2): 229–274.
- Chouret EE. The greater occipital neuralgia headache. Headache. 1967; 7(1): 33–34.
- Dimitriadou V, Buzzi MG, Moskowitz MA, et al. Trigeminal sensory fiber stimulation induces morphological changes reflecting secretion in rat dura mater mast cells. Neuroscience. 1991; 44(1): 97–112.
- Dimitriadou V, Rouleau A, Tuong MDT, et al. Functional relationships between sensory nerve fibers and mast cells of dura mater in normal and inflammatory conditions. Neuroscience. 1997; 77(3): 829–839.
- Durham PL, Cady R, Cady R. Regulation of calcitonin gene-related peptide secretion from trigeminal nerve cells by botulinum toxin type A: implications for migraine therapy. Headache. 2004; 44(1): 35–42.
- Dwek JR. The periosteum: what is it, where is it, and what mimics it in its absence? Skeletal Radiol. 2010; 39(4): 319–323.
- Ebersberger A. Physiology of meningeal innervation: aspects and consequences of chemosensitivity of meningeal nociceptors. Microsc Res Tech. 2001; 53(2): 138–146.
- Edmeads J. The cervical spine and headache. Neurology. 1988; 38(12): 1874–1878.
- Edvinsson L, Goadsby PJ. Neuropeptides in Migraine and Cluster Headache. Cephalalgia. 1994; 14(5): 320–327.
- Escher CM, Paracka L, Dressler D, et al. Botulinum toxin in the management of chronic migraine: clinical evidence and experience. Ther Adv Neurol Disord. 2017; 10(2): 127–135.
- GBD 2016 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017; 390(10100): 1211–1259.
- Greenberg RW, Lane EL, Cinnamon J, et al. The cranial meninges: anatomic considerations. Semin Ultrasound CT MR. 1994; 15(6): 454–465.
- Guyuron B, Riazi H, Long T, et al. Use of a Doppler signal to confirm migraine headache trigger sites. Plast Reconstr Surg. 2015; 135(4): 1109–1112.
- Guyuron B, Yohannes E, Miller R, et al. Electron microscopic and proteomic comparison of terminal branches of the trigeminal nerve in patients with and without migraine headaches. Plast Reconstr Surg. 2014; 134(5): 796e–805e.
- Hofmann E, Prescher A. The Clivus. Clinical Neuroradiology. 2012; 22(2): 123–139.
- Ignelzi RJ, Nyquist JK. Excitability changes in peripheral nerve fibers after repetitive electrical stimulation. Implications in pain modulation. J Neurosurg. 1979; 51(6): 824–833.
- Jabbari B. Botulinum neurotoxins in the treatment of refractory pain. Nat Clini Pract Neurol. 2008; 4(12): 676–685.
- Janis JE, Barker JC, Javadi C, et al. A review of current evidence in the surgical treatment of migraine headaches. Plast Reconstr Surg. 2014; 134(4 Suppl 2): 131S–141S.
- Johnston MM, Jordan SE, Charles AC. Pain referral patterns of the C1 to C3 nerves: implications for headache disorders. Ann Neurol. 2013; 74(1): 145–148.
- Karatas H, Erdener SE, Gursoy-Ozdemir Y, et al. Spreading depression triggers headache by activating neuronal Panx1 channels. Science. 2013; 339(6123): 1092–1095.
- Keller JT, Saunders MC, Beduk A, et al. Innervation of the posterior fossa dura of the cat. Brain Res Bull. 1985; 14(1): 97–102.
- Kemp WJ, Tubbs RS, Cohen-Gadol AA. The innervation of the cranial dura mater: neurosurgical case correlates and a review of the literature. World Neurosurg. 2012; 78(5): 505–510.
- Kerr RW. A mechanism to account for frontal headache in cases of posterior-fossa tumors. J Neurosurg. 1961; 18: 605–609.
- Khan S, Amin FM, Christensen CE, et al. Meningeal contribution to migraine pain: a magnetic resonance angiography study. Brain. 2019; 142(1): 93–102.
- Kimmel DL. Innervation of spinal dura mater and dura mater of the posterior cranial fossa. Neurology. 1961; 11: 800–809.
- Koehler PJ, Boes CJ. A history of non-drug treatment in headache, particularly migraine. Brain. 2010; 133(Pt 8): 2489–2500.
- Lassen LH, Haderslev PA, Jacobsen VB, et al. CGRP may play a causative role in migraine. Cephalalgia. 2002; 22(1): 54–61.
- Lee M, Lineberry K, Reed D, et al. The role of the third occipital nerve in surgical treatment of occipital migraine headaches. J Plast Reconstr Aesthet Surg. 2013; 66(10): 1335–1339.
- Levy D, Strassman AM. Mechanical response properties of A and C primary afferent neurons innervating the rat intracranial dura. J Neurophysiol. 2002; 88(6): 3021–3031.
- Levy D. Endogenous mechanisms underlying the activation and sensitization of meningeal nociceptors: the role of immunovascular interactions and cortical spreading depression. Curr Pain Headache Rep. 2012; 16: 270–277.
- Lim EC, Seet RC. Use of botulinum toxin in the neurology clinic. Nat Rev Neurol. 2010; 6(11): 624–636.
- Lv X, Wu Z, Li Y. Innervation of the cerebral dura mater. Neuroradiol J. 2014; 27(3): 293–298.
- Mahrhold S, Rummel A, Bigalke H, et al. The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves. FEBS Lett. 2006; 580(8): 2011–2014.
- Martin BC, Fagan PJ. The surgical therapy of certain occipital headaches. Plast Reconstr Surg. 1964; 33: 266–268.
- Melzack R, Wall PD. Pain mechanisms: a new theory. Science. 1965; 150(3699): 971–979.
- Mollendorff W. Ueber Hemikranie. Arch Pathol. 1967; 41: 385–395.
- Moskowitz MA. Neurogenic inflammation in the pathophysiology and treatment of migraine. Neurology. 1993; 43: S16–S20.
- Mosser SW, Guyuron B, Janis JE, et al. The anatomy of the greater occipital nerve: implications for the etiology of migraine headaches. Plast Reconstr Surg. 2004; 113(2): 693–7; discussion 698.
- Nabeshima S, Reese TS, Landis DM, et al. Junctions in the meninges and marginal glia. J Comp Neurol. 1975; 164(2): 127–169.
- Noseda R, Melo-Carrillo A, Nir RR, et al. Non-Trigeminal nociceptive innervation of the posterior dura: implications to occipital headache. J Neurosci. 2019; 39(10): 1867–1880.
- Obach TJ, Planas JM, Puig PR. Increase in PGE2 and TXA2 in the saliva of common migraine patients. Action of calcium channel blockers. Headache. 1989; 29(8): 498–501.
- Oh MY, Ortega J, Bellotte JB, et al. Peripheral nerve stimulation for the treatment of occipital neuralgia and transformed migraine using a c1-2-3 subcutaneous paddle style electrode: a technical report. Neuromodulation. 2004; 7(2): 103–112.
- Olesen J, Burstein R, Ashina M, et al. Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol. 2009; 8(7): 679–690.
- Olesen J, Iversen HK, Thomsen LL. Nitric oxide supersensitivity: a possible molecular mechanism of migraine pain. Neuroreport. 1993; 4(8): 1027–1030.
- Olesen J, Jansen-Olesen I. Nitric oxide mechanisms in migraine. Pathol Biol. 2000; 48: 648–657.
- Ottosson A, Edvinsson L. Release of histamine from dural mast cells by substance P and calcitonin gene-related peptide. Cephalalgia. 1997; 17(3): 166–174.
- Paemeleire K, Bartsch T. Occipital nerve stimulation for headache disorders. Neurotherapeutics. 2010; 7: 213–219.
- Page P. Cervicogenic headaches: an evidence-led approach to clinical management. Int J Sports Phys Ther. 2011; 6(3): 254–266.
- Palmisani S, Al-Kaisy A, Arcioni R, et al. A six year retrospective review of occipital nerve stimulation practice--controversies and challenges of an emerging technique for treating refractory headache syndromes. J Headache Pain. 2013; 14: 67.
- Patel N, Kirmi O. Anatomy and imaging of the normal meninges. Semin Ultrasound CT MR. 2009; 30(6): 559–564.
- Penfield W, McNaughton F. Dural headache and innervation of the dura mater. Arch Neurol Psychiatry. 1940; 44(1): 43.
- Perry CJ, Blake P, Buettner C, et al. Upregulation of inflammatory gene transcripts in periosteum of chronic migraineurs: Implications for extracranial origin of headache. Ann Neurol. 2016; 79(6): 1000–1013.
- Pickett A. Re-engineering clostridial neurotoxins for the treatment of chronic pain: current status and future prospects. BioDrugs. 2010; 24(3): 173–182.
- Popeney CA, Aló KM. Peripheral neurostimulation for the treatment of chronic, disabling transformed migraine. Headache. 2003; 43(4): 369–375.
- Purkiss J, Welch M, Doward S, et al. Capsaicin-stimulated release of substance P from cultured dorsal root ganglion neurons: involvement of two distinct mechanisms. Biochem Pharmacol. 2000; 59(11): 1403–1406.
- Rapidis AD. The therapeutic result of excision of the superficial temporal artery in atypical migraine. J Maxillofac Surg. 1976; 4(3): 182–188.
- Rennie C, Haffajee MR, Ebrahim MAA. The sinuvertebral nerves at the craniovertebral junction: a microdissection study. Clin Anat. 2013; 26(3): 357–366.
- Rifat SF, Moeller JL. Diagnosis and management of headache in the weight-lifting athlete. Curr Sports Med Rep. 2003; 2(5): 272–275.
- Rummel A. The long journey of botulinum neurotoxins into the synapse. Toxicon. 2015; 107(Pt A): 9–24.
- Sanniec K, Borsting E, Amirlak B. Decompression-Avulsion of the auriculotemporal nerve for treatment of migraines and chronic headaches. Plast Reconstr Surg Glob Open. 2016; 4(4): e678.
- Schueler M, Messlinger K, Dux M, et al. Extracranial projections of meningeal afferents and their impact on meningeal nociception and headache. Pain. 2013; 154(9): 1622–1631.
- Schueler M, Neuhuber WL, De Col R, et al. Innervation of rat and human dura mater and pericranial tissues in the parieto-temporal region by meningeal afferents. Headache. 2014; 54(6): 996–1009.
- Shevel E. A new minimally invasive technique for cauterizing the maxillary artery and its application in the treatment of cluster headache. J Oral Maxillofac Surg. 2013; 71(4): 677–681.
- Sjaastad O, Fredriksen TA. Cervicogenic headache: criteria, classification and epidemiology. Clin Exp Rheumatol. 2000; 18(2 Suppl 19): S3–S6.
- Struffert T. [Anatomy and malformations of the posterior cranial fossa]. Radiologe. 2016; 56(11): 960–966.
- Tepper SJ. History and review of anti-Calcitonin gene-related peptide (CGRP) therapies: from translational research to treatment. Headache. 2018; 58(Suppl 3): 238–275.
- Treleaven J, Jull G, Atkinson L. Cervical musculoskeletal dysfunction in post-concussional headache. Cephalalgia. 1994; 14(4): 273–279.
- Uebner M, Carr RW, Messlinger K, et al. Activity-dependent sensory signal processing in mechanically responsive slowly conducting meningeal afferents. J Neurophysiol. 2014; 112(12): 3077–3085.
- Wall PD. The gate control theory of pain mechanisms. A re-examination and re-statement. Brain. 1978; 101(1): 1–18.
- Welch MJ, Purkiss JR, Foster KA. Sensitivity of embryonic rat dorsal root ganglia neurons to Clostridium botulinum neurotoxins. Toxicon. 2000; 38(2): 245–258.
- Weiner RL, Reed KL. Peripheral neurostimulation for control of intractable occipital neuralgia. Neuromodulation. 1999; 2(3): 217–221.
- Yegutkin GG, Guerrero-Toro C, Kilinc E, et al. Nucleotide homeostasis and purinergic nociceptive signaling in rat meninges in migraine-like conditions. Purinergic Signal. 2016; 12(3): 561–574.
- Zakharov A, Vitale C, Kilinc E, et al. Hunting for origins of migraine pain: cluster analysis of spontaneous and capsaicin-induced firing in meningeal trigeminal nerve fibers. Front Cell Neurosci. 2015; 9: 287.
