Child's Nervous System

, 24:1289 | Cite as

The middle meningeal artery: from clinics to fossils

Original Paper

Abstract

Introduction

Although research today ranges from molecular to universe scale, many issues regarding gross anatomy remain totally neglected. Within the framework of the endocranial morphogenesis and evolution, understanding the role and variation of the middle meningeal artery relies upon the very limited, scattered, and descriptive information available. The meninges are supplied by branches originating from both the internal and external carotid arteries, often converging in the same networks and hence raising questions on the homology and embryogenesis of these vessels. The middle meningeal artery is often ligated during craniotomies, with no apparent impairment of the cerebral functional processes. The exact physiological role of this extended vascular system, together with the adaptations and selective pressure associated with its evolutionary characterization, have generally been ignored.

The middle meningeal vessels in nonhuman primates

Anthropologists have made many attempts to quantify and qualify the differences and variation between and within human and nonhuman primates, with scarce results due to the blurry morphology of the vascular networks. Living apes and humans probably have meningeal vessels originating from different embryogenetic processes, further hampering easy phylogenetic comparisons. Generally, monkeys and apes display a larger component derived from the internal carotid artery and its ophthalmic branch.

Evolution and morphological variation in fossil hominids

The fossil endocasts partially show the traces of the middle meningeal vessels, allowing some hypotheses on the evolution of these structures. In contrast with modern humans, some extinct groups show a dominance of the posterior branch over the anterior one. The most interesting features are associated with the variation of the middle branch, which supplies the parietal areas. In any case, the most striking difference between the modern and non-modern humans regard the definite increase in the number and complexity of the anastomoses and reticulation in the former. This may be either the simple result of a larger percentage of traces left by the soft tissue or be associated with a more developed vascular network.

Perspectives

Tools are needed to quantify and qualify the morphogenesis and variations of the middle meningeal artery. Supposing these vessels are not strictly necessary in the adult age, the evolutionary pressure shaping their structure may have been associated with early life stages. Apart from oxygenation, another function which deserves attention is thermoregulation, considering the metabolic loadings of the cerebral mass.

Keywords

Endocranium Vascular system Human evolution Paleoneurology 

References

  1. 1.
    Aiello L, Wheeler P (1995) The expensive-tissue hypothesis. Curr Anthropol 36:199–221CrossRefGoogle Scholar
  2. 2.
    Alberico A, Ward J, Choi S, Marmarou A, Young H (1987) Outcome after severe head injury. Relationship to mass lesions, diffuse injury, and ICP course in pediatric and adult patients. J Neurosurg 67:648–656PubMedCrossRefGoogle Scholar
  3. 3.
    Altmann F (1947) Anomalies of the internal carotid artery and its branches; their embryological and comparative anatomical significance. Report of a new case of persistent stapedial artery in man. Laryngoscope 57:313–339Google Scholar
  4. 4.
    Bastir M, Rosas A, O’Higgins P (2006) Craniofacial levels and the morphological maturation of the human skull. J Anat 209:637–654PubMedCrossRefGoogle Scholar
  5. 5.
    Begun D, Walker A (1993) The endocast. In: Walker A, Leakey R (eds) The Nariokotome Homo erectus skeleton. Springer-Verlag, Berlin, pp 326–358Google Scholar
  6. 6.
    Bookstein FL, Gunz P, Mitteroecker P, Prossinger H, Schaefer K, Seidler H (2003) Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution. J Hum Evol 44:167–187PubMedCrossRefGoogle Scholar
  7. 7.
    Bräuer G, Groden C, Gröning F, Kroll A, Kupczik K, Mbua E, Pommert A, Schiemann T (2004) Virtual study of the endocranial morphology of the matrix-filled cranium from Eliye Springs, Kenya. Anat Rec A276:113–133CrossRefGoogle Scholar
  8. 8.
    Bricolo A, Pasut L (1984) Extradural hematoma: toward zero mortality. A prospective study. Neurosurgery 14:8–12Google Scholar
  9. 9.
    Broadfield DC, Holloway RL, Mowbray K, Silvers A, Yuan MS, Márquez S (2001) Endocast of Sambungmacan 3 (Sm 3): a new Homo erectus from Indonesia. Anat Rec 262:369–379PubMedCrossRefGoogle Scholar
  10. 10.
    Bruner E (2003) Fossil traces of the human thought: paleoneurology and the evolution of the genus Homo. Riv Antropol 81:29–56Google Scholar
  11. 11.
    Bruner E (2004) Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo. J Hum Evol 47:279–303PubMedCrossRefGoogle Scholar
  12. 12.
    Bruner E (2004) Models for Natural History. J Anthropol Sci 82:11–18Google Scholar
  13. 13.
    Bruner E (2007) Cranial shape and size variation in human evolution: structural and functional perspectives. Child’s Nerv Sys 23:1357–1365CrossRefGoogle Scholar
  14. 14.
    Bruner E (2008) Comparing endocranial form and shape differences in modern humans and Neandertal: a geometric approach. PaleoAnthropology 2008:93–106Google Scholar
  15. 15.
    Bruner E (2008) The evolution of the parietal cortical areas in the human genus: between structure and cognition”. In: D Broadfield, M Yuan, K Schick, N Toth (eds) Human brain evolving. Bloomington, the Stone Age Institute (in press)Google Scholar
  16. 16.
    Bruner E, Manzi G (2008) Paleoneurology of an “early” xhal: endocranial size, shape, and features of Saccopastore 1. J Hum Evol 54:729–742PubMedCrossRefGoogle Scholar
  17. 17.
    Bruner E, Averini M, Manzi G (2003) Endocranial traits. Prevalence and distribution in a recent human population. Eur J Anat 7:23–33Google Scholar
  18. 18.
    Bruner E, Manzi G, Arsuaga JL (2003) Encephalization and allometric trajectories in the genus Homo: evidence from the Neandertal and modern lineages. Proc Natl Acad Sci USA 100:15335–15340PubMedCrossRefGoogle Scholar
  19. 19.
    Bruner E, Saracino B, Passarello P, Ricci F, Tafuri M, Manzi G (2004) Midsagittal cranial shape variation in the genus Homo by geometric morphometrics. Coll Antropol 28:99–112PubMedGoogle Scholar
  20. 20.
    Bruner E, Mantini S, Perna A, Maffei C, Manzi G (2005) Fractal dimension of the middle meningeal vessels: variation and evolution in Homo erectus, Neanderthals, and modern humans. Eur J Morphol 42:217–224PubMedCrossRefGoogle Scholar
  21. 21.
    Bruner E, Manzi G, Holloway R (2006) Krapina and Saccopastore: endocranial morphology in the pre-Würmian Europeans. Period Biolog 108:433–441Google Scholar
  22. 22.
    Chernoff B, Magwene PM (1999) Morphological integration: forty years later. In: Olson EC, Miller RL (eds) Morphological integration. The University of Chicago Press, Chicago and London, pp 319–353Google Scholar
  23. 23.
    Cheverud JM (1996) Developmental integration and the evolutino of pleiotropy. Amer Zool 36:44–50Google Scholar
  24. 24.
    Curnow J (1874) Two instances of irregular ophthalmic and middle meningeal arteries. J Anat Physiol 8:155–156Google Scholar
  25. 25.
    Dean D, Hublin JJ, Holloway R, Ziegler R (1998) On the phylogenetic position of the pre-Neandertal specimen from Reilingen, Germany. J Hum Evol 34:485–508PubMedCrossRefGoogle Scholar
  26. 26.
    Diamond MK (1991) Homologies of the meningeal-orbital arteries of humans: a reappraisal. J Anat 17:223–241Google Scholar
  27. 27.
    Dilenge D, Ascherl GF (1980) Variation of the ophthalmic and middle meningeal arteries: relation to the embryonic stapedial artery. Am J Neur Rad 1:45–53Google Scholar
  28. 28.
    Eichmann A, Le Noble F, Autiero M, Carmeliet P (2005) Guidance of vascular and neural network formation. Curr Opin Neurobiol 15:108–15PubMedCrossRefGoogle Scholar
  29. 29.
    Enlow DH (1990) Facial Growth. WB Saunders Company, PhiladelphiaGoogle Scholar
  30. 30.
    Falk D (1987) Hominid paleoneurology. Ann Rev Anthropol 16:13–30CrossRefGoogle Scholar
  31. 31.
    Falk D (1990) Brain evolution in Homo: the “radiator” theory. Behav Brain Sci 13:333–381Google Scholar
  32. 32.
    Falk D (1993) Meningeal arterial pattern in great apes: implication for hominoid vascular evolution. Am J Phys Anthropol 92:81–97PubMedCrossRefGoogle Scholar
  33. 33.
    Falk D, Nicholls P (1992) Meningeal arteries in Rhesus macacques Macaca mulatta: implication for vascular evolution in anthropoids. Am J Phys Anthropol 98:299–308CrossRefGoogle Scholar
  34. 34.
    Frayer DW, Jelinek J, Oliva M, Wolpoff MH (2007) Aurignacian male crania, jaws and teeth from the Mladec caves, Moravia, Czech Republic. In: Teschler-Nicola M (ed) Early modern humans at the Moravian Gate: the Mladec Caves and their remains. Springer, pp 185–272Google Scholar
  35. 35.
    Gentry LR (1994) Imaging of closed head injury. Radiology 191:1–17PubMedGoogle Scholar
  36. 36.
    Giuffrida-Ruggeri V (1904) Proposta di uno studio delle ramificazinoi dell’arteria meningea media nei degenerati. Comunicazioni al XII Congresso della Società Freniatica ItalianaGoogle Scholar
  37. 37.
    Grimaud-Hervé D (1994) Evolution of the Javanese fossil hominid brain. Cour Forsch Inst Senckenberg 171:61–68Google Scholar
  38. 38.
    Grimaud-Hervé D (1997) L’évolution de l’enchéphale chez Homo erectus et Homo sapiens. CNRS Editions, ParisGoogle Scholar
  39. 39.
    Grimaud-Hervé D (1998) Le moulage endocranien de l’hominidé Arago 21 et 47. L’Anthropologie (Paris) 102:21–34Google Scholar
  40. 40.
    Grimaud-Hervé D (2005) Apports de quelques caractères morphologiques endocraniens dans la determination taxinomique des hominidés de Jebel Ihroud (Maroc). Anthropologie XLIII:101–112Google Scholar
  41. 41.
    Grimaud-Hervé D, Saban R (1996) Les empreintes vasculaires observees sur les moulages endocraniens d’hominides fossiles et actuels. Anthropologie XXXIV:27–34Google Scholar
  42. 42.
    Henderson JH, Longaker MT, Carter DR (2004) Sutural bone deposition rate and strain magnitude during cranial development. Bone 34:271–80PubMedCrossRefGoogle Scholar
  43. 43.
    Holloway RL (1978) The relevance of endocasts for studying primate brain evolution. In: Noback CR (ed) Sensory systems of primates. Plenum, New York, pp 181–200Google Scholar
  44. 44.
    Holloway RL, Broadfield DC, Yuan MS (2004) Brain endocasts: the paleoneurological evidence. The Human fossil record, Vol III. Wiley-Liss, Hoboken, New JerseyGoogle Scholar
  45. 45.
    House HP, Patterson ME (1964) Persistent stapedial artery: report of two cases. Trans Am Acad Ophthalmol Otolaryngol 68:644–6PubMedGoogle Scholar
  46. 46.
    Hyrtl J (1836) Neue beobachtungen aus dem gebiete der menschlichen und vergleichenden anatomie. Med Jahrb d Oesterreich Staates 10:457–466Google Scholar
  47. 47.
    Klingenberg CP (1998) Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev Camb Philos Soc 73:79–123PubMedCrossRefGoogle Scholar
  48. 48.
    Klingenberg CP (2002) Morphometrics and the role of the phenotype in studies of the evolution of developmental mechanisms. Gene 287:3–10PubMedCrossRefGoogle Scholar
  49. 49.
    Leonard WR, Robertson ML (1992) Nutritional requirements and human evolution: a bioenergetics model. Am J Hum Biol 4:179–195CrossRefGoogle Scholar
  50. 50.
    Leonard WR, Robertson ML (1994) Evolutionary perspective on human nutrition: the influence of brain and body size on diet and metabolism. Am J Hum Biol 6:77–88CrossRefGoogle Scholar
  51. 51.
    Leonard WR, Robertson ML (1997) Comparative primate energetics and hominid evolution. Am J Phys Anthropol 102:265–281PubMedCrossRefGoogle Scholar
  52. 52.
    Maiuri F, Donzelli R, de Divitiis O, Fusco M, Briganti F (1998) Anomalous meningeal branches of the ophthalmic artery feeding meningiomas of the brain convexity. Surg Radiol Anat 20:279–84PubMedCrossRefGoogle Scholar
  53. 53.
    Marcozzi V (1942) L’arteria meningea media negli uomini recenti, nel Sinantropo e nelle rcimmie. Riv Antropol 34:407–436Google Scholar
  54. 54.
    McLennan JE, Rosenbaum AE, Haughton VM (1974) Internal carotid origins of the middle meningeal artery-the ophthalmic-middle meningeal and stapedial-middle meningeal arteries. Neuroradiology 7:265–275PubMedCrossRefGoogle Scholar
  55. 55.
    Moss ML, Young RW (1960) A functional approach to craniology. Am J Phys Anthropol 18:281–292PubMedCrossRefGoogle Scholar
  56. 56.
    Muller F (1977) The development of the anterior falcate and lacrimal arteries in the human. Anat Embryol 150:207–227PubMedCrossRefGoogle Scholar
  57. 57.
    O’Laughlin V (1996) Comparative endocranial vascular changes due to craniosynostosis and artificial cranial deformation. Am J Phys Anthropol 101:369–385CrossRefGoogle Scholar
  58. 58.
    Rak Y, Kimbel WH, Johanson DC (1996) The crescent of foramina in Australopithecus afarensis and other early hominids. Am J Phys Anthropol 101:93–99PubMedCrossRefGoogle Scholar
  59. 59.
    Richtsmeier JT, Aldridge K, de Leon VB, Panchal J, Kane AA, Marsh JL, Yan P, Cole TM (2006) Phenotypic integration of neurocranium and brain. J Exp Zool (Mol Dev Evol) 306B:360–378CrossRefGoogle Scholar
  60. 60.
    Saban R (1979) Le systeme veineux méningé de l’homme fossile de Biache-Saint-Vaast Pas de Calais, d’apres le moulange endocranien. CR Acad Sci Paris D 289:1129–1132Google Scholar
  61. 61.
    Saban R (1982) Le systéme des veines méningées moyennes chez les hommes fossiles de Tchécoslovaquie, d’aprés le moulage endocranien. Anthropos 21:281–295Google Scholar
  62. 62.
    Saban R (1995) Image of the human fossil brain: endocranial casts and meningeal vessels in young and adult subjects. In: Changeaux P, Chavaillon J (eds) Origins of the human brain. Oxford, Clarendon Press, pp 11–38Google Scholar
  63. 63.
    Schoenemann PT, Gee J, Avants B, Holloway RL, Monge J, Lewis J (2007) Validation of plaster endocast morphology through 3D CT image analysis. Am J Phys Anthropol 132:183–92PubMedCrossRefGoogle Scholar
  64. 64.
    Steffen TN (1968) Vascular anomalites of the middle ear. Laryngoscope 78:171–97PubMedCrossRefGoogle Scholar
  65. 65.
    Stringer C (2002) Modern human origins: progress and prospects. Phil Trans R Soc London B 357:563–579CrossRefGoogle Scholar
  66. 66.
    Tobias PV (1995) The brain of the first hominids. In: Changeaux JP, Chavaillon J (eds) Origins of the human brain. Clarendon, Oxford, pp 61–83Google Scholar
  67. 67.
    Wood B, Collard M (1999) The human genus. Science 284:65–71PubMedCrossRefGoogle Scholar
  68. 68.
    Wood B, Richmond BG (2000) Human evolution: taxonomy and paleobiology. J Anat 197:19–60PubMedCrossRefGoogle Scholar
  69. 69.
    Wu X, Schepartz LA, Falk D, Liu W (2006) Endocranial cast of Hexian Homo erectus from South China. Am J Phys Anthropol 130:445–54PubMedCrossRefGoogle Scholar
  70. 70.
    Zasler ND, Katz DI, Zafonte RD (2006) Brain injury medicine: principles and practice, Demos Medical PublishingGoogle Scholar
  71. 71.
    Zuckerkandl E (1876) Zur Anatomie der Orbitalarterien. Med Jahrb (Wien) 1876:343–350Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Centro Nacional de Investigación sobre la Evolución Humana (CENIEH)BurgosSpain
  2. 2.Department of NeurosurgerySan Filippo Neri HospitalRomeItaly

Personalised recommendations