Skull Base Embryology: a Multidisciplinary Review
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Childs Nerv Syst (2014) 30:991–1000 DOI 10.1007/s00381-014-2411-x REVIEW PAPER Skull base embryology: a multidisciplinary review Antonio Di Ieva & Emiliano Bruner & Thomas Haider & Luigi F. Rodella & John M. Lee & Michael D. Cusimano & Manfred Tschabitscher Received: 11 March 2014 /Accepted: 25 March 2014 /Published online: 17 April 2014 # Springer-Verlag Berlin Heidelberg 2014 Abstract promises to expand our knowledge and enhance our ability to Introduction The skull base represents a central and complex treat associated anomalies. bone structure of the skull and forms the floor of the cranial cavity on which the brain lies. Anatomical knowledge of this Keywords Anatomy . Comparative anatomy . Embryology . particular region is important for understanding several path- Skull base . Encephalocele . Pharyngeal arches . Functional ologic conditions as well as for planning surgical procedures. craniology Embryology of the cranial base is of great interest due to its pronounced impact on the development of adjacent regions including the brain, neck, and craniofacial skeleton. Introduction Materials and methods Information from human and compar- ative anatomy, anthropology, embryology, surgery, and com- The skull base represents a central and complex bone structure puted modelling was integrated to provide a perspective to of the skull and forms the floor of the cranial cavity on which interpret skull base formation and variability within the cranial the brain lies. Nerves and blood vessels cross skull base functional and structural system. foramina while the foramen magnum allows anatomical con- Results and conclusions The skull base undergoes an elabo- tinuation between the spinal cord and the brain. Anatomical rate sequence of development stages and represents a key knowledge of this particular region is important for under- player in skull, face and brain development. Furthering our standing several pathologic conditions as well as for planning holistic understanding of the embryology of the skull base surgical procedures. Embryology of the cranial base is of great interest due to its pronounced impact on the development of : A. Di Ieva (*) M. D. Cusimano adjacent regions including the brain, neck and craniofacial Division of Neurosurgery, Department of Surgery, St. Michael’s skeleton [1–9]. Hospital, University of Toronto, 30 Bond Street, Toronto, ON, Canada M5B 1W8 e-mail: [email protected] Anatomical synopsis of the skull base A. Di Ieva : T. Haider : M. Tschabitscher Centre for Anatomy and Cell Biology, Department of Systematic Figure 1 shows the intracranial and exocranial surfaces of the Anatomy, Medical University of Vienna, Vienna, Austria skull base. The intracranial portion of the skull base can be E. Bruner divided into three parts: the anterior, the middle and the Centro Nacional de Investigación sobre la Evolución Humana, posterior cranial fossa. Two paired frontal bones, the sphenoid Burgos, Spain and ethmoid bone give rise to the anterior cranial fossa bearing L. F. Rodella : M. Tschabitscher the ventral part of the frontal lobe (orbital gyri). The frontal Department of Clinical and Experimental Sciences, University of bone originates from two symmetric bones after fusion of the Brescia, Brescia, Italy metopic suture forming the main portion of this fossa and the roof of both orbits [10]. The cribriform plate of the ethmoid J. M. Lee Department of Otolaryngology-Head and Neck Surgery, St. bone is located between the two frontal bones and Michael’s Hospital, University of Toronto, Toronto, Ontario, Canada allows connection between the olfactory filiae and the nasal 992 Childs Nerv Syst (2014) 30:991–1000 abducens nerve runs upwards to the cavernous sinus. After its extradural course the sixth nerve first enters the sphenopetroclival venous gulf to reach Dorello’s canal located below the ligament of Gruber and finally passes through the cavernous sinus. [14]. The posterior fossa is bounded laterally by the temporal and the occipital bone and behind and above by the parietal bone. It is the largest cranial fossa and contains the cerebellum, pons and medulla oblongata and allows con- nection to the cervical spinal cord through the foramen mag- num [15]. Further important foramina within this fossa are the internal acoustic canal, the vestibular aqueduct and the jugular foramen containing the glossopharyngeal, the vagus and the accessory nerve as well as the internal jugular vein [15, 16]. Fig. 1 Intracranial (left) and exocranial (right) surfaces of the mature The inferior (exocranial) surface of the skull base is not skull base divided in three compartments and needs to be described separately. Besides the largest portion, the palatine process of the maxilla, the zygomatic process of the maxilla and the cavity. Anteriorly, the ethmoid bone also comprises the crista palatine bone represent the anterior external part. The middle galli, an anchor for the falx cerebri. While the lesser wing of part of the cranial base comprises the body of the sphenoid, the sphenoid bone marks the dorsal boundary of the anterior the petrous part of temporal bones and the basiocciput and cranial fossa, the body and greater wing represent the ventral extends to a virtual transverse line dividing the foramen mag- and lateral part of the middle cranial fossa. Also the squamous num. The bones of the posterior part of the external skull base part of the temporal bone and the parietal bone form the lateral correspond with the intracranial posterior cranial fossa with its border of the middle fossa. In the middle of this fossa, a prominent occipital bone. Most prominent structures are the prominent concave structure is arranged, the sella turcica, foramen magnum and the occipital condyles connecting the containing the hypophysis and building the roof of the sphe- skull to the cervical spine [15]. Variants of occipital condyles noidal sinus. The cavernous sinus is located to both sides of have been described, such as appearance of a third condyle the sella, comprising important structures. The internal carotid with occasional articulation with the dens axis, and a rare artery passes through the cavernous sinus in an S-shaped variant of duplicated occipital condyles [2, 17–19]. manner forming the so-called carotid siphon. Branches from this part of the internal carotid artery supply the hypophysis, part of the dura mater, the optic chiasm, the sixth nerve and the Embryologic aspect of the skull base trigeminal ganglion [11]. Also the abducens nerve proceeds straight through the cavernous sinus, while the maxillary, Pharyngeal arches ophthalmic, trochlear and oculomotor nerves run within the lateral wall [12]. The maxillary nerve originates from the Development of the vertebrate head require the formation of trigeminal ganglion (ganglion Gasseri) where the nerve breaks the neural crest, which represents the origin for connective and down into its three branches, the ophthalmic, the maxillary skeletal tissue of the neck, face and skull [8]. In contrast to and the mandibular nerve located within a duplication of dura trunk neural crest cells, cranial neural crest cells migrate called trigeminal or Meckel’s cave. Foramina in the middle before neural folds fuse to form the neural tube, which is not cranial fossa allow passage towards the viscerocranium, the case for the cranial crest in non-mammalian vertebrates [8, namely the superior orbital fissure for the ophthalmic nerve, 20]. The rostral population of neural crest cells is the major the foramen rotundum for the maxillary nerve and the foramen contributor to skull formation being the origin of the whole ovale for the mandibular nerve. A variant “oval canal” has viscerocranium and the rostral part of the neurocranium [8, 9]. been described, where an osseous lamina continuous with the In adolescents, the coronal suture between the frontal and the pterygoid plate canopies the foramen ovale [13]. The temporal parietal bones marks the boundary between neural crest and lobe is located within the middle cranial fossa supporting its cranial mesoderm origin [10, 20]. Gradual migration of neural distinct shape. The posterior aspect of the sella turcica, the crest cells around the embryonic pharynx leads to formation of dorsum sellae, the posterior part of the sphenoid bone and the five pairs of embryonic arches, each containing epithelial basilar part of the occipital bone represent the anterior border covered ecto- and endoderm as well as mesenchyme originat- of the posterior cranial fossa. Both also contribute to the ing mainly from the neural crest. Neural crest cells of the first formation of the clivus, a sloped bone structure on which the two arches contribute to cranial skeletal elements with Childs Nerv Syst (2014) 30:991–1000 993 associated connective tissue. Condensation of neural crest- base foramina before bones are formed [8]. Defective devel- derived mesenchyme leads to sub-sequential chondrification. opment of the cranial base has been described to be associated After completion of chondrogenesis, dorsal extension con- with anencephaly underlining its importance in development tinues until it reaches the cranial base located laterally to the of the whole skull and brain [4]. The rostral tip of the noto- hindbrain. Arch cartilage undergoes endochondral ossifica- chord (chorda dorsalis) reaches a location caudal to the hy- tion, ligamentous ossification, and a combination of both or pophysis and represents the start of the development of the remains cartilage [8]. Most parts of the skull