face, nasal cavities and palate, oral cavity and tongue
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B Fig. 36.10 Development of the face during
A stages 12–18. A, 4 weeks (3.5 mm).
Frontonasal process B, 5 weeks (6.5 mm). C, 51 2 weeks (9 mm).
D, 6 weeks (12 mm). E, 7 weeks (19 mm).
F, 8 weeks (28 mm).
Nasal placode Nasal pit
Buccopharyngeal Stomodeum
membrane
Maxillary process
Mandibular process
Hyoid arch
D
C
Medial nasal process
Lateral nasal process
Nasolacrimal groove
Maxillary process
Mandible
Hyomandibular cleft
F
E
Medial nasal processes fuse
to form philtrum of upper lip
External ear
Ear tubercles around
hyomandibular cleft
Hyoid bone
Laryngeal cartilages
median downgrowth from the primitive palate forms the definitive cavities is now complete. A number of elevations appear on the lateral
nasal septum; it is supported by cartilage. The fusing medial edges of wall of each nasal cavity: the superior, middle and inferior conchae
the elevated palatal shelves also fuse with the free edge of the nasal (Fig. 36.12B,C).
septum, forming separate right and left nasal cavities above the second- Within the nasal septum, on either side of the septal cartilage,
ary palate. The original positions of the choanae are now covered by a pair of small diverticula, the vomeronasal organs, form at stage
the palatal shelves so that the nasal cavities extend from the nostrils to 18 (6 weeks). From 12 to 19 weeks, the vomeronasal organ has an olfac-
the free (caudal) edge of the palate at the nasopharynx. Bone forms by tory epithelium-like appearance, and luteinizing hormone-releasing
both intramembranous ossification within the palatal mesenchyme to hormone (LHRH)-immunoreactive cells are present in nerve fascicles


form the hard palate, except near its caudal border, and by endochon- extending from it to the olfactory bulb (Boehm et al 1994). In many
dral ossification of the cartilaginous nasal septum. At this time, the free species, the vomeronasal organ has a pheromonal communication
edge of the palatal shelves lies directly below the former position of the function; however, although most adult humans have a vomeronasal
attachment of the adenohypophysial (Rathke’s) pouch to the roof of organ, its olfactory-type structure and LHRH immunoreactivity are lost
the oral cavity. Caudal to the hard palate, its free edges grow to form during later fetal life and a pheromonal function in adults has not been
the soft palate and uvula, which extend into the oropharynx. Myogenic established (Ch. 33 e-book only).
mesenchyme from the first (tensor palati only) and third pharyngeal Bilateral dorsal expansions of the first, second and, possibly, third
arches migrates into the soft palate and around the caudal margins of pharyngeal pouches form the tubotympanic recesses, which will become
the pharyngotympanic tube. Separation of the definitive nasal and oral the tympanic cavities and pharyngotympanic tubes. A number of focal


Development of the heaD anD neck
614
4
noItceS
proliferations of nasopharyngeal endoderm become invaded by lym- A
phoid tissue. First (mandibular) Distal (lateral)
pharyngeal arch lingual swelling
ventral part
ORAL CAVITY Median tongue
bud (tuberculum
Second (hyoid) impar)
In the fifth week (stage 12), the oropharyngeal membrane breaks down
pharyngeal arch
so that communication is established between the ectoderm-lined sto- ventral part Site of thyroid
modeum and the endoderm-lined part of the pharynx, creating a con- diverticulum
tinuous cranial foregut cavity. Formation of the hard and soft palates Copula
Third pharyngeal arch
separates the cranial foregut into the nasal cavity and nasopharynx Hypobranchial
above and the definitive oral cavity below. The oral cavity is demarcated eminence
from the oropharynx posteriorly by the oropharyngeal isthmus, formed Fourth pharyngeal arch Furcula (sixth arch)
by the free edge of the soft palate and uvula above, and the palatoglossal
Laryngotracheal
arch laterally.
groove, cranial end
Tongue
B
Anterior part
Because the mandibular arch grows more rapidly than the others, it of tongue
makes the greatest contribution to the pharyngeal floor. By stage 14
(5 weeks), three swellings are apparent: a small median elevation, the Distal (lateral)
lingual swelling
tuberculum impar or median tongue bud; and paired lateral lingual
swellings distally (Fig. 36.13A). These three swellings fuse to form the
Median tongue
anterior two-thirds of the tongue (Fig. 36.13B), and a small median Mandibular arch bud (tuberculum
diverticulum, the foramen caecum (thyroid diverticulum), forms imme- impar)
diately caudal to the median tongue bud (Fig. 36.13B,C; see Fig.
36.18A). A sulcus forms along the ventral and lateral margins of this Foramen caecum


elevation and deepens, internal to the future dental lamina, to form the
Epiglottis
linguogingival sulcus (groove) (see Fig. 36.13C). Caudal to the median Hyoid arch
(early stage)
tongue bud, a small swelling, the copula, forms in the floor of the
second arch. The hypobranchial (hypopharyngeal) eminence forms in Glottis
the floor of the third arch; it grows over the second arch (which does Third arch
not contribute to the tongue) and fuses with the anterior tongue rudi- Arytenoid swellings
ment along a V-shaped line, the sulcus terminalis, at stage 17 (sixth
week). Another transverse groove separates the developing tongue from
C
the caudal (fourth arch) swelling, which forms the epiglottis.
Labiogingival sulcus
Dermatomes supplied by: Line of fusion of
maxillary process
Ophthalmic nerve Dental lamina
and lateral nasal
process Fungiform papilla
Linguogingival sulcus
Maxillary nerve Maxillary process Median sulcus
Palatoglossal fold
Lateral nasal
Great auricular nerve process Vallate papilla
Palatine tonsil
Fused medial Sulcus terminalis
nasal process Lingual tonsil
Mandibular nerve
Foramen caecum
Line of fusion of Median glossoepiglottic fold
maxillary prominence
Epiglottis
Transverse cervical nerve and the fused medial
nasal process Glottis
Fig. 36.11 The parts of the adult face derived from the ophthalmic Fig. 36.13 Development of the pharyngeal floor and tongue. A, Stage 14,
(frontonasal), maxillary and mandibular divisions of the skin of the face, showing median and lateral swellings in the floor of the first arch. B, After
showing the lines of fusion and definitive innervation. fusion of the swellings. C, The tongue and oropharynx at birth.
A B External nostril C
Lateral nasal
Medial nasal process
process Fusion of maxillary
Eye process with premaxilla
Maxillary
Primary palate
process
Primitive palate
Palatal shelf from
maxillary process Uvula
Eye Eye
Primitive palate
Middle concha


Nasal cartilage
Tongue
Tongue
Meckel’s cartilage
Fig. 36.12 Development of the palate. A–C, Developmental progression over weeks 7–8; ventral views (top row) and coronal sections (bottom row).


face, nasal cavities and palate, oral cavity and tongue
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63
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In general, the composite character of the mucous membrane of the from behind forwards, they enclose the elongating duct. The orifice of
tongue is reflected in its sensory innervation. The anterior, oral, part is the submandibular duct is thus located progressively more distally
innervated by the lingual branch of the mandibular nerve, and by the until it is below the tip of the tongue, close to the median plane. The
chorda tympani of the facial nerve. The posterior, pharyngeal, part of sublingual gland arises at stage 20 as a number of small epithelial
the tongue is innervated by the glossopharyngeal nerve, which is the thickenings within and lateral to the linguogingival sulcus. Each
nerve of the third arch; this nerve also invades the tissue immediately thickening canalizes separately, so multiple sublingual ducts open
distal to the sulcus limitans, including innervation of the vallate papil- on the summit of the sublingual fold, while others join the sub-
lae. The vallate papillae appear within the mucous membrane at around mandibular duct.
10 weeks and increase in number until the end of the second trimester. The minor salivary glands, which are distributed throughout the wall
The root of the tongue, near the epiglottis, is innervated by the vagus. of the oral cavity, except for the gingiva and hard palate, form in a
The motor innervation is from the hypoglossal nerves, which extend similar manner to the major glands but undergo very little branching
around and under the pharynx together with myogenic cells migrating and remain within the submucosa.
from the occipital myotomes during stages 14 and 15.
Tongue development is essentially complete by stage 23. At birth, Lymphoid tissues
the tongue is short and broad, and its entire surface lies within the oral
cavity (see Fig. 14.7). The posterior third of the tongue descends as the
Tonsils form at several sites around the oro- and nasopharynx, where
hyoid bone and larynx descend during the first postnatal year, and by


focal proliferations of endoderm become invaded by lymphoid tissue.
the fourth or fifth year, it forms part of the anterior wall of the
The endodermal epithelial lining grows into the surrounding mesen-
oropharynx.
chyme as a number of solid buds, which are excavated by degeneration
Salivary glands and shedding of their central cells, forming tonsillar fossae and crypts.
Lymphoid cells accumulate around the crypts at about the fifth month
and become grouped as lymphoid follicles; T- and B-cell regions can
The salivary glands arise bilaterally as the result of epithelial–
be identified. The palatine tonsils develop from the ventral parts of the
mesenchymal interactions between the ectodermal epithelial lining of
second pharyngeal pouches (see Fig. 36.4C). A slit-like intratonsillar
the oral cavity and the subjacent neural crest-derived mesenchyme. The
cleft extends into the upper part of the tonsil and is possibly a remnant
parotid gland can be recognized at stage 15 (8 mm) as an elongated
of the second pharyngeal pouch. Lymphoid tissue similar to that of the
furrow running dorsally from the angle of the mouth between the
palatine tonsils is found in the first pouch (tubal tonsils), the surface
mandibular and maxillary prominences. The groove, which is converted
of the posterior part of the tongue (lingual tonsils), and in the dorsal
into a tube, loses its connection with the epithelium of the oral cavity,
pharyngeal wall (adenoid or pharyngeal tonsil).
except at its ventral end, and grows dorsally into the soft tissue of the
cheek. The tube persists as the parotid duct. After fusion of the lateral
Teeth and gums
parts of the maxillary and mandibular prominences, the parotid duct
opens on the inside of the cheek at some distance from the angle of
the mouth. As the gland develops, its branches interweave with the Demarcation of the lips begins after fusion of the facial primordia at
branches of the facial nerve. In the neonate, the parotid gland is rounded stage 18, during the period of secondary palatal development. Two


and lies between masseter and the ear. During infancy and early child- parallel epithelial thickenings, an outer labiogingival lamina and an
hood, the growing gland extends to cover the parotid duct. Its secretions inner dental lamina, form around the interior border of the mouth in
remain entirely serous. both upper and lower jaws (see Figs 36.13C, 36.15). The linguogingival
The submandibular and sublingual glands form as solid diverticula sulcus is formed as an indentation between the dental lamina and the
that undergo branching morphogenesis, the whole tree-like structure tongue. At stage 22, each labiogingival lamina indents the underlying
later acquiring a lumen. The blind ends of the branches form acini, mesenchyme to form a shallow groove that deepens to form the labio-
whose cells differentiate to form serous cells initially, and mucus- gingival sulcus between the lips and gums. The lining of the oral cavity
secreting cells postnatally. The submandibular gland is identifiable at between the vestibular epithelium of the upper and lower jaws forms
stage 18 as an epithelial diverticulum into the mesenchyme from the the inner aspect of the cheeks. The dental lamina gives rise to the epi-
floor of the caudal part of the linguogingival sulcus. It increases rapidly thelial component of the teeth.
in size and branches several times. At first, the connection of the sub- Tooth formation involves a sequence of epithelial–mesenchymal
mandibular gland with the floor of the mouth lies at the side of the interactions along the dental lamina (Fig. 36.14). These interactions
tongue, but as the edges of the linguogingival sulcus come together, are controlled by a large number of genetic factors, and the extracellular
ORAL ECTODERM Dental epithelium Enamel organ Pre-ameloblasts
Epithelial
cell/tissue Ameloblasts
transformations
ENAMEL
Epithelium
Epithelium causes
Mesenchyme mesenchyme
to condense Enamel organ epithelium
induces dental papilla
mesenchyme to become
Odontoblastic mesenchyme
Epithelial/ Dental papilla induces pre-odontoblasts
induces epithelial


mesenchymal epithelium to form an and odontoblasts
pre-ameloblasts to
interactions enamel organ
become ameloblasts
Dental mesenchyme
induces oral
epithelium to become
dental epithelium Forming dental papilla
JAW MESENCHYME Dental mesenchyme Dental papilla Pre-odontoblasts Odontoblasts
Mesenchymal
cell/tissue Predentine
transformations
DENTINE
Fig. 36.14 A summary of the epithelial–mesenchymal interactions during tooth development.


Development of the heaD anD neck
616
4
noItceS
A
Tongue Labiogingival
lamina
Dental lamina
Labiogingival
sulcus
Enamel
Ameloblasts
Linguogingival sulcus
Pulp Odontoblasts
B
Lip
Fig. 36.16 Pierre Robin sequence. (Courtesy of Mr T Goodacre and
Labiogingival Oxford Radcliffe Hospitals NHS Trust.)
sulcus Dental papilla
Enamel organ
Tooth germ of
permanent teeth The oral cavity after birth
Extension of dental
lamina for second and third
permanent molars
In the neonate, the oral cavity is only potential when the mouth is
closed, but three spaces are formed during suckling. The median space
Tooth germ of first permanent molar
between the tongue and hard palate, which is occupied by the nipple,
Fig. 36.15 The lip, gums and teeth after 24 weeks. A, Oral view. B, The bifurcates posteriorly to produce channels on each side of the soft
right half of the lower jaw viewed from below; the midline is upper right. palate and epiglottis. The larynx is elevated so that its opening is
directed into the nasopharynx, i.e. above the level of the channels, and
milk passes on either side of it to the pharynx and oesophagus. This
matrix (particularly of the basement membranes) is of major import- anatomical arrangement enables the infant to breathe while suckling
ance (Thesleff 2000, Fukumoto and Yamada 2005). In 25 mm embryos, (see Figs 34.11, 34.12A). The hard palate is only slightly arched and its
10 localized thickenings of the upper and lower dental laminae initiate mucous membrane is corrugated by five or six irregular transverse folds
formation of the dental epithelial components of the tooth primordia (rugae), which assist with gripping the nipple. Two lateral spaces, the
(see Fig. 36.14). They expand into dental sacs surrounded by vascular lateral arcuate cavities, are formed between the tongue and cheeks; the
mesenchyme. The epithelium proliferates and indents to form an upper and lower gums situated within these spaces do not touch during


enamel organ, which, by 10 weeks, forms a cap over a mesenchymal suckling. Each cheek is supported by a mass of subcutaneous fat, the
condensation, the dental papilla; collectively, this unit constitutes a suctorial pad, which lies between buccinator and masseter.
tooth bud or germ. The enamel organ becomes bell-shaped and dif-
ferentiates into two layers, the internal and external enamel epithelia;
ANOMALIES OF FACIAL DEVELOPMENT
these are separated by a glycosaminoglycan-rich extracellular matrix, the
stellate reticulum. The cells of the internal epithelium differentiate into
Malformations involving the neural crest
ameloblasts, and the underlying layer of mesenchymal cells differenti-
ates into odontoblasts. The odontoblasts produce and secrete dentine,
which influences the ameloblasts to form enamel; this is laid down in Congenital malformations of the face may be initiated early, mainly
successive layers and, after mineralization, is the hardest tissue in the related to abnormal migration, proliferation and/or apoptosis of neural
body. Enamel and dentine production from the bell-shaped tooth germ crest cells, or later, during the morphogenetic phase of facial develop-
both begin at 24 weeks (Fig. 36.15). The dental papilla mesenchyme ment. Craniofrontonasal syndrome is characterized by a broad forehead
below the odontoblast layer forms the pulp, which becomes vascular- and hypertelorism, premature fusion of one or both coronal sutures, a
ized and innervated. Experimental studies in mice (which have only central nasal groove, and sometimes cleft lip and palate; there are also
incisors and molars) have revealed that regional differences in signal- extracranial features. It is caused by deletions of the gene EFNB1, which
ling pathways within the maxillary and mandibular mesenchymes is known to play essential roles in boundary formation between tissues,
govern the type of tooth produced (Tummers and Thesleff 2009). including those between neural crest and adjacent non-crest cells (Twigg
Fibronectin is present in the basement membrane of the internal et al 2004). Mandibulofacial dysostosis (Treacher Collins syndrome) is


enamel epithelium during the bell phase. It assists attachment of the characterized by incomplete orbits, reduced jaws and auditory ossicles
pre-odontoblasts and is essential for their differentiation; it becomes (hence conductive deafness), abnormal external ears and fistulae or
progressively more abundant during the later fetal period. Collagen I is cysts, suggesting involvement of the first and second arch components
the major supportive extracellular scaffold in the maturing dental of the cranial neural crest. It is caused by haploinsufficiency of the gene
papilla and stellate reticulum. TCOF1. Hemifacial microsomia (Goldenhaar’s syndrome) affects only
At birth, each quadrant of the jaws has five deciduous tooth germs one side of the face and comprises a small mandible (sometimes with
and the germs of the first five permanent teeth. Permanent teeth absence of the temporomandibular joint), malformed or absent ears
develop in accessional positions from the lingual aspects of the decidu- with accessory ear tags, and facial clefts. Experimental evidence in
ous tooth germs and, for the 12 permanent molar teeth, from posterior animals suggests that it is due to haemorrhage of the stapedial artery,
extensions of the dental laminae on each side of both jaws. Mineraliza- which may have a genetic basis. Deficient growth of the mandible
tion begins in both deciduous and permanent teeth before birth. The (micrognathia) is usually associated with other defects. In Pierre Robin
deciduous teeth have well-developed crowns by full term, and eruption sequence (Fig. 36.16), the small size of the mandible obstructs descent
through the gingiva (gum) usually begins with the lower incisors of the tongue, resulting in a U-shaped cleft palate; a conotruncal septum
between 3 and 6 months after birth. After eruption, the gingiva remains defect is present in one-quarter of cases, suggesting possible involve-
attached to the neck of each tooth by the upper part of the periodontal ment of the cardiac neural crest. Further details and references for facial
ligament, whose major part attaches the tooth root to the bone of the malformations may be found in Morriss-Kay and Wilkie (2005) and
tooth socket. Hennekam et al (2010).


formation of the neck
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Fig. 36.17 Cleft lip and cleft palate.
A, Incomplete unilateral cleft lip. B, Complete
unilateral cleft lip. C, Incomplete bilateral cleft lip.
D, Complete bilateral cleft lip and cleft palate (the
nasal septum and both inferior nasal conchae can
be seen). E, Cleft palate (the nasal septum and left
inferior nasal concha can be seen). F, Cleft of the
soft palate. (Courtesy of Mr T Goodacre and
Oxford Radcliffe Hospitals NHS Trust.)
A B
C D
E F
Clefts of the face and palate with hypertelorism in various frontonasal dysplasias, suggesting a
developmentally early broadening of the median region of the face.
Cleft lip occurs when one or both medial nasal processes fail to fuse
with the corresponding maxillary process(es). The severity of clefting
FORMATION OF THE NECK
varies from a small notch in the upper lip to a double cleft extending
into both nostrils (Fig. 36.17). In a unilateral cleft lip, the nasal septum
deviates to the non-cleft side. This is because the muscles on the medial By the time the facial swellings have merged to form a recognizably
side of the cleft (transverse muscles of the nose and orbicularis oris) are human face (stage 20, 7 weeks), Meckel’s cartilage has grown sufficiently
not inserted into either the muscles of the contralateral side or the to project outwards as a potential chin but the face is still orientated
tissues around the nasal septum (Fig. 36.17B). The three functional towards, and close to, the cardiac prominence (see Fig. 36.5). Forma-
groups of superficial facial muscles – nasolabial (transverse nasalis, tion of the posterior part of the neck is, by this time, well advanced,
levator labii superioris and levator labii superioris alaeque nasi), bila- with cartilaginous cervical vertebrae, muscles, nerves and blood vessels.
bial (orbicularis oris) and labiomental (depressor anguli oris) – are all The anterior neck forms gradually, as relatively rapid growth of the


displaced inferiorly. A further consequence is the underdevelopment of anterior structures, including the trachea, oesophagus, common carotid
the incisor-bearing part of the maxilla. These abnormalities, in turn, arteries and jugular veins, takes place. As the extending neck lifts the
influence the mucocutaneous tissues, which results in the displacement head to a forward-facing orientation, the angle between the spinal cord
of the skin of the nostril to the upper part of the lip, retraction of the and brainstem increases. Other contributory changes include growth of
labial skin and abnormalities of the soft tissues on either side of the the first pharyngeal arch at a more rapid rate than the others, so that
mucocutaneous junction. Meckel’s cartilage and the developing membrane bone of the mandible
A narrow or incomplete cleft of the hard palate is likely to be due project further forwards, while the hyoid bone primordium remains
to a growth defect in the palatal shelves and/or a delay in shelf eleva- small, defining the future angle between the anterior neck and lower
tion, and/or to failure of fusion of the apposed palatal shelves. Broader jaw. Myoblasts derived from paraxial mesenchyme invade the second
clefts (Fig. 36.17D,E), in which the tongue lies between the still-vertical pharyngeal arch as it forms and by this stage are present in the super-
shelves, are caused by a greater developmental delay that may be associ- ficial connective tissue beneath the anterior neck skin; these spread out
ated with abnormality of other structures in the face and elsewhere in from the underside of the chin to the upper thorax and differentiate to
the body. In the mildest forms of cleft palate, only the soft palate, and form the platysma (this is the main human remnant of the panniculus
sometimes just the uvula, is cleft (Fig. 36.17F). A submucous cleft, carnosus, the muscle that is present throughout the skin of many
which may be detected as a median V-shaped notch of the soft palate, mammals).
can cause speech difficulties. Very rarely, muscle hypoplasia, particularly The interface between cranial nerve-innervated pharyngeal arch


of the musculus uvulae, causes palatopharyngeal incompetence. muscles and spinal nerve-innervated trunk muscles occurs at the lower
Cleft lip with or without cleft palate (CL/P) is multigenic or multi- neck and the upper parts of the pectoral girdle. Both the proximal and
factorial in origin, i.e. it has both genetic and environmental compo- distal connections of the trapezius muscle, at the nuchal line of the
nents (Gorlin et al 2001). CL/P has a frequency of 0.5–3.6/1000 live occipital bone and the attachment to the spine of the scapula, are
births, with a 2 : 1 male to female ratio. Isolated cleft palate is genetically formed from post-otic neural crest cells (Matsuoka et al 2005). The
unrelated to CL/P, and has a frequency of 0.4/1000; it is more common neural crest generates areas of endochondral ossification in the cervical
in females. Clefts of the face are rare (1/50,000–1/175,000 births); they vertebral column and scapula associated with trapezius attachment.
are mainly caused by pressure from amniotic bands rather than from This observation has promoted the conception of a ‘muscle scaffold
dysmorphogenesis, although a morphogenetic component cannot be model’ of development to replace the older ‘ossification model’, to
ruled out when the cleft is along a line of fusion, e.g. maxillary– explain the types of ossification seen associated with the accessory
mandibular. Median cleft lip (true hare lip) is also rare, since this is not nerve-innervated trapezius and sternocleidomastoid muscles. It is sug-
a line of morphogenetic fusion. Median grooving of the nose occurs gested that defects in the fate choices of neural crest cells could explain


Development of the heaD anD neck
618
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noItceS
a number of syndromes that have pharyngeal, laryngeal, occipital, cervi- is able to concentrate iodine and synthesize thyroxine. Stage 2
cal and shoulder dysmorphologies and co-occurrence of swallowing (19–29 weeks) is quiescent, with little change in the epithelium/colloid
problems; related syndromes include Klippel–Feil, Sprengel’s deformity ratio and follicular size. Stage 3 (after 29 weeks) is characterized by a
and cleidocranial dysplasia (Matsuoka et al 2005) (see p. 794). gradual increase in the epithelium/colloid ratio and a decrease in fol-
licular size (Bocian-Sobkowska et al 1997). The parafollicular or C cells
of the thyroid gland are derived from the ultimobranchial body, a small
GLANDS OF THE NECK diverticulum of the fourth pharyngeal pouch. The thyroid gland is rela-
tively large in the neonate (see Fig. 14.6A), where it has a long, narrow
Further development of the pharyngeal floor and the second to fourth isthmus connecting lobes that do not yet contact the upper part of the
pharyngeal pouches gives rise to glands that are ultimately disposed in trachea. It usually attains half the adult size by 2 years of age.
the neck and anterior mediastinum, namely: the paired thyroid and Failure of downgrowth of all or part of the thyroid gland from the
parathyroid glands and the thymus. pharyngeal floor results in ectopic thyroid tissue within the tongue
(lingual thyroid), lying between the foramen caecum and the epiglottis.
Thyroid gland Occasionally, parts of the midline thyroglossal duct persist and may
occur in lingual, suprahyoid, retrohyoid or infrahyoid positions; they
may form aberrant masses of thyroid tissue, cysts, fistulae or sinuses,
The thyroid gland is a midline derivative of the pharynx. It is first iden-
usually in the midline. Nodules of glandular tissue may also be found


tifiable in embryos of approximately 20 somites as a median thickening
laterally, posterior to sternocleidomastoid.
of endoderm lying in the floor of the pharynx between the first and
second pharyngeal pouches and immediately dorsal to the aortic sac.
Parathyroid glands
The foramen caecum is the site of a median diverticulum that appears
early in the fifth week in the furrow immediately caudal to the median
tongue bud (see Fig. 36.13B, C; Fig. 36.18). It extends caudally as the The parathyroid glands develop from interactions between the third
thyroglossal duct, passing ventral to the primordium of the hyoid bone. and fourth pharyngeal pouch endoderm and local cranial (vagal) neural
The tip of the duct bifurcates and the tissue mass subsequently divides crest mesenchyme. The third pharyngeal pouch has dorsal and ventral
to form the isthmus and lateral lobes of the thyroid gland. The sites of proliferation (Fig. 36.18B). The epithelium on the dorsal aspect
endoderm-derived epithelial tissue is invested by vagal neural crest of the pouch and in the region of its duct-like connection with the cavity
mesenchyme, which gives rise to the connective tissue capsule and of the pharynx becomes differentiated as the primordium of the inferior
interlobular septa, and perifollicular mesenchyme, which carries the parathyroid glands (parathyroid III). Although the connection between
neurovascular and lymphatic supply to the gland. The gland has three the pouches and the pharynx is soon lost, the connection between the
stages of development. Stage 1 (10–18 weeks) is characterized by active dorsal parathyroids and the ventral thymic rudiments of the third pha-
folliculogenesis and gradual accumulation of colloid; the thyroid tissue ryngeal pouch persists for some time and both move caudally. The
Right thymus Pedicle of left third pharyngeal pouch
Right parathyroid III Left thymus
Left parathyroid III
A B
Endoderm
Buccal cavity
First pharyngeal pouch
Median thyroid diverticulum
Second pharyngeal pouch
Third pharyngeal pouch


Fourth pharyngeal pouch and
caudal pharyngeal complex
Left lateral lobe of thyroid
Tracheo-oesophageal tube
Oesophagus Trachea Thyroid isthmus
Right lateral lobe of thyroid Left fourth pharyngeal pouch
C D
Left parathyroid III
Right parathyroid III Left fourth pharyngeal Left parathyroid III
pouch (ventral portion)
Left parathyroid IV
Right thymus gland Left parathyroid IV
Thyroid gland Right parathyroid III Trachea
Left thymus gland
Right lobe of Right thymus
thyroid gland
Left thymus
Trachea
Oesophagus
Fig. 36.18 A, The ventral aspect of the endoderm of the pharynx, showing the pharyngeal pouches. The areas of contact of the pharyngeal endoderm
with the surface ectoderm are shown as flattened surfaces. Note that the colours of the pharyngeal pouches and the median thyroid diverticulum are
retained in B, C and D. B, Ventral and dorsal diverticuli of the third and fourth pharyngeal pouches and midline thyroid gland at 6 weeks. C, The thymus,
thyroid and parathyroid glands at 7 weeks. D, The thymus, thyroid and parathyroid glands at 71 weeks. (Redrawn with permission from Hamilton WJ,
2
Boyd JD, Mossman HW 1962 Human Embryology: Prenatal Development of Form and Function. Cambridge: W Heffer & Sons.)


formation of the neck
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superior parathyroid glands (parathyroid IV) develop from the dorsal epiglottis. Two linear ridges in the ventral wall of the pharynx extend
recess of the fourth pharyngeal pouches. They make contact with, and ventrally from the sixth arches to the median laryngotracheal groove,
appear to be anchored by, the lateral lobes of the thyroid gland and from which the lower part of the larynx, the trachea, bronchi and lungs
thus remain cranial to the descended parathyroid III glands. Vagal develop (Ch. 52).
neural crest mesenchyme provides the connective tissue elements, and The laryngotracheal groove forms at stage 12 as a ventral endoder-
invading angiogenic mesenchyme gives rise to fenestrated capillaries mal outgrowth from the floor of the caudal part of the pharynx into
and lymphatics. In the neonate, the parathyroid glands are as variable the mesenchyme surrounding the sinus venosus and inflow tract of the
in size and position as they are in the adult. They double in size between heart (see Figs 52.1C, 60.3). This initiates the separation of the respira-
birth and puberty. Parathyroid hormone is produced from the twelfth tory and alimentary tubes. The groove remains at a constant level during
week of development. the embryonic period, and the trachea lengthens distally as its bifurca-
tion point descends. The splanchnopleuric mesenchyme that surrounds
Thymus the developing trachea and oesophagus induces the different histogenic
pathways of the two tubes. By stage 17, the mesenchyme around the
trachea is beginning to condense at regular intervals and undergo chon-
The thymus gland is formed from the ventral part of the third pharyn-
drogenesis to form C-shaped cartilages, whereas that around the
geal pouch on each side (see Fig. 36.18). It cannot be recognized prior
oesophagus has a wide submucosal zone and muscular coats. The res-
to the differentiation of the inferior parathyroid glands at stage 16 but,
piratory diverticulum becomes surrounded by angiogenic mesenchyme


thereafter, it is represented by two elongated diverticula that soon
that connects to the developing sixth aortic arch artery (see above).
become solid cellular masses and grow caudally into the surrounding
For details of early development of the trachea, see page 926; for
vagal neural crest mesenchyme. Ventral to the aortic sac, the two thymic
early development of the oesophagus, see page 1048.
rudiments meet but do not fuse, and they are subsequently united by
In the neonate, the pharynx is one-third of the relative length seen
connective tissue only. The thymus gland becomes located in the an-
in the adult. The nasopharynx is a narrow tube that curves gradually to
terior mediastinum of the thorax once the neck is fully developed and
join the oropharynx without any sharp junctional demarcation. An
the heart has descended. The connection with the third pouch is soon
oblique angle is formed at this junction by 5 years of age, and in the lost, but the stalk may persist for some time as a solid, cellular cord.
adult, the nasopharynx and oropharynx join at almost a right angle.
As the thymus proliferates and descends, the local neural crest-
The oesophagus in the newborn begins and ends one to two vertebrae
derived mesenchyme controls the pattern and development of the
higher than in the adult, extending from between the fourth and sixth
gland. Defective development of the vagal neural crest, which affects
cervical vertebrae to the level of the ninth thoracic vertebra. The nar-
the heart and peripheral neural ganglia, also results in thymic deficien-
rowest constriction is at its junction with the pharynx, where the infe-
cies, as seen in DiGeorge syndrome and Pierre Robin sequence. Neural
rior pharyngeal constrictor functions to constrict the lumen; in this
crest mesenchyme forms connective tissue septa, which produce the
region, it may be traumatized with instruments or catheters.
lobulated architecture of the gland. Angiogenic mesenchyme, including
The neonatal hyoid bone and larynx are relatively high in the neck,
lymphoid stem cells, invades this local mesenchyme, and by 10 weeks,


and the trachea is relatively small in relation to the larynx (see Fig.
over 95% of the cells in the gland belong to the T-cell lineage, with a
14.6B); both descend during infancy. The walls of the trachea are rela-
few erythroblasts and B lymphocytes. Hassall’s corpuscles are also
tively thick and the tracheal cartilages are relatively closer together than
present. By 12 weeks, the mesenchymal septa, blood vessels and nerves
in the adult. The trachea commences at the upper border of the sixth
have reached the newly differentiating medulla, which allows the entry
cervical vertebra, a relationship that is conserved with growth, and it
of macrophage lineage precursors. Macrophages and interdigitating
bifurcates at the level of the third or fourth thoracic vertebra.
cells are first seen at 14 weeks. Granulopoiesis occurs in the perivascular
spaces. By 17 weeks, the thymus appears fully differentiated, and after
this time, it produces the main type of thymocyte that is present BLOOD VESSELS IN THE NECK
throughout life (designated TdT+).
With elongation of the neck and the appearance of the major conduct-
Caudal pharyngeal complex
ing vessels from the aortic arch arteries, longitudinal anastomoses in
the cervical region link intersegmental arteries and their branches, and
The most caudal endodermal evaginations of the pharynx are the fourth direct blood flow to the developing brain in the vertebral arteries in
pharyngeal pouch and the ultimobranchial body, a small diverticulum parallel with the internal carotid arteries (see Figs 36.8–36.9).
medial to the main pouch. Collectively, these diverticula are termed the The primary blood vessels of the head and neck consist of a close-
caudal pharyngeal complex (see Fig. 36.18), and they are connected to meshed capillary plexus drained on each side by the precardinal vein,
the pharynx via the pharyngobranchial duct. They are surrounded by which is, at first, continuous cranially with a transitory primordial


vagal neural crest and by the tissues of the developing thyroid gland. hindbrain channel that lies on the neural tube medial to the cranial
The cells of the ultimobranchial body become incorporated into the nerve roots (see Figs 13.1–13.2). This is soon replaced by the primary
lateral thyroid lobes, and give rise to the calcitonin-secreting ‘C’ or head vein, which runs caudally from the medial side of the trigeminal
parafollicular cells of the thyroid gland. ganglion, lateral to the facial and vestibulocochlear nerves and the
otocyst, then medial to the vagus nerve, to become continuous with the
precardinal vein. A lateral anastomosis subsequently brings it lateral to
PHARYNX, LARYNX, OESOPHAGUS AND TRACHEA the vagus nerve.
The ventral pharyngeal vein drains the mandibular and hyoid arches
The larynx forms at the cranial end of the laryngotracheal groove, into the common cardinal vein (see Fig. 17.36A). As the neck elongates,
caudal to the epiglottis (see Figs 36.5–36.6, 36.13). The thyroid carti- its termination is transferred to the cranial part of the precardinal vein,
lage develops from the ventral ends of the cartilages of the fourth, or which later becomes the internal jugular vein (see Fig. 17.36B). The
fourth and sixth, pharyngeal arches. The cartilage appears as two lateral ventral pharyngeal vein receives tributaries from the face and tongue,
plates, each chondrified from two centres and united in the mid-ventral and becomes the linguofacial vein. As the face develops, the primitive
line by a fibrous membrane, within which an additional centre of maxillary vein extends its drainage into the territories of supply of the
chondrification develops. The cricoid cartilage arises from two cartilagi- ophthalmic and mandibular divisions of the trigeminal nerve, includ-
nous centres, which soon unite ventrally, gradually extend, and ulti- ing the pterygoid and temporal muscles, and it anastomoses with the


mately fuse on the dorsal surface of the tube as the cricoid lamina. It linguofacial vein over the lower jaw. This anastomosis becomes
has the appearance of a modified tracheal cartilage. Paired arytenoid the facial vein; it receives blood from the retromandibular vein from
swellings appear within the ventral tissue of the sixth arches from stage the temporal region, and drains through the linguofacial vein into the
14, one on each side of the cranial end of the laryngotracheal groove. internal jugular. The stem of the linguofacial vein is now the lower part
As they enlarge, they approximate to each other and to the caudal part of the facial vein, whilst the dwindling connection of the facial with
of the hypobranchial eminence, where the epiglottis develops. The the primitive maxillary becomes the deep facial vein. The external
opening into the larynx, at first a simple slit, is converted into a jugular vein develops from a tributary of the cephalic vein from the
T-shaped cleft by the enlargement of the arytenoid swellings. The verti- tissues of the neck; it anastomoses secondarily with the anterior facial
cal limb of the T lies between the two swellings, and its horizontal limb vein. At this stage, the cephalic vein forms a venous ring around the
lies between them and the epiglottis. The arytenoid swellings differenti- clavicle, by which it is connected with the caudal part of the precardinal
ate into the arytenoid and corniculate cartilages (Fig. 36.6), and the vein. The deep segment of the venous ring forms the subclavian vein
ridges that join them to the epiglottis become the definitive aryepiglot- and receives the definitive external jugular vein. The superficial segment
tic folds, within which the cuneiform cartilages differentiate from the of the venous ring dwindles, but may persist in adult life. The deep


Development of the heaD anD neck
620
4
noItceS
aspects of the maxillomandibular facial prominences, the retrogingival the bones are formed. The adenohypophysial (Rathke’s) pouch is
oral cavity, the pharyngeal walls and their lymphoid and endocrine still connected to the roof of the oral cavity as the skull base cartilage
derivatives, and the cervicothoracic oesophagus thus all have drainage forms (dashed lines in Fig. 36.20A; see also Fig. 17.14), but already lies
channels that connect with the precardinal complex. Laryngeal and adjacent to the diencephalon-derived neurohypophysis to form the
tracheobronchial veins also drain to the precardinal complex, whilst the downwardly projecting pituitary gland (hypophysis) at the base of the
capillary plexuses, developed in the (splanchnopleuric) walls of the fine caudal diencephalon.
terminal respiratory passages and alveoli, converge on pulmonary veins The notochordal sheath is rich in sulphated glycosaminoglycans,
of increasing calibre, finally making secondary connections with the left which play a role in inducing condensation and chondrification of the
atrium of the heart, and may be grouped with the vitelline systems. occipital sclerotome-derived mesenchyme around it.
The structures referred to in the following account are illustrated in
Figure 36.20B, which shows the cartilaginous skull base of a 40 mm
SKULL
(9-week) embryo. The central regions of all four occipital sclerotomes
contribute to the parachordal cartilage, which surrounds the notochord
The skull has two major functional and anatomical components: the and extends as a flat plate on either side of it by the end of the seventh
neurocranium and the viscerocranium. The neurocranium is composed week, forming the basioccipital component of the occipital bone (see
of the calvaria and basicranium; it surrounds and protects the brain and Fig. 44.13). Laterally, the exoccipital components (derived from scle-


the special sense organs of olfaction, vision, hearing and balance. The rotomes 3 and 4) chondrify soon afterwards; they extend around the
viscerocranium, which includes the squamous part of the temporal hindbrain to form the occipital arch, which is developmentally equiva-
bone, forms the skeleton of the face, palate and pharynx, and mediates lent to the neural arch components of vertebrae. Roots of the hypoglos-
the functions of feeding, breathing and facial expression; it also protects sal nerve run between the parachordal and exoccipital cartilages, so that
the tongue and forms the middle ear and the bony external acoustic when the exoccipital and parachordal components fuse, they leave
meatus. The most rostral neural crest cell population makes a major foramina for these nerve roots (see Fig. 44.12). The supraoccipital part
contribution to the skull, forming the whole viscerocranium and the of the occipital cartilage extends dorsally from the exoccipital cartilage
rostral part of the neurocranium (Fig. 36.19). The boundary between to complete the foramen magnum. After formation of the exoccipital
neural crest and cranial mesoderm lies between the frontal and parietal cartilages, differentiation also extends further rostrally in the medial
bones (coronal suture) of the calvaria; the skull base is formed by neural part of the skull base, with formation of the hypophysial polar cartilages
crest rostral to the tip of the notochord, and is sclerotome-derived (i.e. on either side of the hypophysial stalk; they unite in the median plane
from paraxial mesenchyme) in the notochordal region (McBratney- to form the primordium of the postsphenoid, cradling the hypophysis
Owen et al 2008). The tip of the notochord lies immediately caudal to and retaining a perforation for the hypophysial stalk until the third
the hypophysial fossa (Fig. 36.20A). Broadly speaking, the bones of the month. This part of the basisphenoid cartilage will form the sella turcica


skull base are formed by endochondral ossification (chondrocranium), with its hypophysial fossa. The presphenoid cartilages, rostral to it, form
whereas those of the calvaria and face ossify directly from mesenchymal the jugum of the sphenoid body. This is the last part of the medial part
condensations, i.e. by intramembranous ossification. Several bones are of the skull base to differentiate as cartilage, bridging the gap between
of compound structure with respect to their tissue origins and/or type the postsphenoid and the cartilaginous nasal capsule.
of ossification: the occipital, temporal and sphenoid bones, and the At stage 17, mesenchyme begins to condense and later to chondrify
mandible. The following account is based largely on descriptive studies around the nasal pits, forming the outer part of the nasal capsule and
on human embryos and fetuses (O’Rahilly and Müller 1987, 2001, the nasal septum; the roof of each nasal capsule is completed slightly
2007), with some details of cell lineage based on investigations in the later, when cartilage differentiates around the olfactory nerve bundles
mouse. to form the cribriform plates of the ethmoid bone. During the third
month, cartilaginous conchae form. The whole nasal capsule is well
developed by the end of the third month, and consists of a common
CHONDROCRANIUM median septal part, sometimes initially termed the interorbitonasal
septum or mesethmoid, and the outer ectethmoid. The conchae ossify
The first cranial skeletal structures to differentiate are the cartilages of during the fifth month; the superior and middle conchae form part of
the skull base, sensory capsules, viscerocranium and occiput (see Figs the ethmoid bone, and the inferior pair become separate elements. Each
36.5, 36.20B). Development of the pharyngeal arch-related cartilages lateral part of the nasal capsule becomes ossified as the orbital plate
of the viscerocranium and ear ossicles has been described in the section and ethmoidal labyrinth, whose spaces (‘cells’) communicate with the


on the pharynx. Before any mesenchyme condenses to initiate the for- nasal cavity and become filled with air after birth (see p. 566). Part of
mation of cranial cartilage, the major cranial nerves and blood vessels the capsule remains cartilaginous as the septal and alar cartilages of the
are already in place; hence, the foramina of the skull are specified before nose, and part is replaced by the intramembranous vomer and nasal
bones.
Orbital cartilages surround the eye but do not undergo ossification
Anterior fontanelle Sagittal suture
in their entirety. The most rostral of them becomes continuous with the
Frontal bone
presphenoid cartilage by differentiation of a cartilaginous bridge that
forms the caudal boundary of the optic foramen, enclosing the optic
Parietal nerve; this later ossifies to form the lesser wing of the sphenoid bone
Coronal bone (orbitosphenoid). The greater wing of the sphenoid (alisphenoid) has
suture both intramembranous and endochondral components; the endochon-
Posterior
dral part initially differentiates as a cartilage surrounding the mandibu-
Greater fontanelle
lar branch of the trigeminal nerve, forming the foramen ovale. This
wing of
sphenoid Lambdoid condensation extends medially to join the rostral edge of the hypophy-
suture sial (polar) cartilage on each side. It also extends rostrally to surround
Nasal the maxillary branch of the trigeminal nerve, forming the foramen
bone rotundum. Lastly, it extends laterally to join the intramembranous part
of the bone, which replaces the caudal part of the orbital cartilage. The
Zygoma greater and lesser wings of the sphenoid are separated by the oculomo-
(malar) tor, trochlear and abducens nerves and by the first (ophthalmic) divi-
Interparietal
Occipital sion of the trigeminal nerve.
Maxilla S Eu xop cra co ipc itc aip lital bone The otic capsule differentiates from a mesenchymal condensation
around the otocyst, after its morphogenesis to form the cochlea and
Mandible


Tympanic ring semicircular canals. Differentiation of cartilage begins laterally, at the
Auditory ossicles same time as the hypophysial cartilages are first detectable; it is com-
Squamous part of temporal bone Styloid process plete by stage 20. Chondrogenesis around the point of exit of the ves-
tibulocochlear nerve creates the internal acoustic meatus. Chondrogenesis
of mesenchyme around the carotid arteries joins each hypophysial
Neural crest Sclerotome Cranial paraxial mesenchyme
cartilage to the otic capsule, forming the carotid canals. A gap occupied
Fig. 36.19 The newborn skull, showing the tissue origins of the bones by the jugular vein and the glossopharyngeal, vagus and accessory
(based on combined mouse and human data). The darker green nerves remains between each otic capsule and the parachordal cartilage;
represents the sites of fontanelles. this is the jugular foramen. Chondrogenesis of the mesenchyme


Skull
621
63
Retpahc
A B C
Hypophysial fossa 40 mm
A Branches
1 of I/cribiform
plate
Mesenchyme B
covering Parachordal C II
cartilaginous cartilage/ Branches
cranial base basioccipital D of III, IV,
I Vi, VI
Notochord 3 Vii
C aa rr to et rid
y
Viii
VII
J
Anterior arch of atlas Jugular VIII
Notochord vein IX
Body of axis F X
G XI
Third cervical vertebra H XII
4
D Key to chondral elements
A Nasal capsule
B Orbitosphenoid
C Presphenoid
80 mm D Postsphenoid
E Basioccipital
F Otic capsule
G Exoccipital
H Supraoccipital
I Alisphenoid
J Meckel’s mandibular cartilage
K Cartilage of malleus
L Styloid cartilage
M Hyoid cartilage
N Thyroid cartilage
O Cricoid cartilage
1 P Arytenoid cartilage
B
Key to dermal (membrane) elements
I
5 1 Frontal bone
11 2 Nasal bone
4 3 Squama of temporal bone
10
4 Squama of occipital bone (interparietal)
9 D 5 Parietal bone
8 H 6 Maxilla
7 Lacrimal bone
2 C 8 Zygomatic bone
A F 9 Palatine bone
10 Vomer
7
E 11 Medial pterygoid plate
6 L 12 Tympanic ring
13 Mandible
3
G
K
M
13
N
J
O
12
P
Fig. 36.20 Representative stages in the development of the cranium. In all the diagrams, the chondrocranium and cartilaginous stages of vertebrae are
shown in blue, except where ossification is occurring; here, the colour is green. The membrane bones are shown in cream. Cranial nerves are indicated
by the appropriate Roman numeral. A, A sagittal section through the cranial end of the developing axial skeleton in an early human embryo of


approximately 10 mm (5 weeks), showing the extent of the notochord. B, The superior aspect of the cranium of a human embryo at 40 mm (9 weeks). The
remnant of the hypophysial stalk is indicated by a black dot in the hypophysial fossa. C, The lateral aspect of B. D, The lateral aspect of the cranium of
a human embryo at 80 mm.
between the separate cartilages completes formation of the cartilagi- most of the cartilage until only the major synchondroses remain; these
nous skull base and sensory capsules, which together form a continuous enable the endochondral skull base and sensory capsules to continue
framework around the pre-existing blood vessels and cranial nerves by growing until they reach their final size at puberty or earlier. At birth,
9 weeks (40 mm) (see Fig. 36.20B,C). unossified chondrocranium persists in the alae, lateral nasal cartilage
The process of endochondral ossification in the skull is essentially and septum of the nose, the sphenoethmoidal junction, the spheno-
the same as that of the long bones, except that each ossification centre occipital and sphenopetrous junctions, the apex of the petrous tempo-
is equivalent to a primary centre, and follows a specific programme of ral bone (foramen lacerum), and between ossification centres of the
growth and patterning. Growth takes place within the cartilage between sphenoid and occipital bones. As indicated above, parts of the chon-
adjacent ossification centres; these joints are termed synchondroses. The drocranium do not ossify, but are replaced by adjacent intramembra-
first ossification centres to appear are those of the lesser and greater nous bone, e.g. the greater wing of the sphenoid (alisphenoid). In
wings of the sphenoid, at 8 and 9 weeks, respectively. A single basisphe- general, endochondral ossification centres form later than intramem-
noid ossification centre appears at 11 weeks; three presphenoid and four branous ossification sites, which first appear during the seventh and
postsphenoid ossification centres appear at 16 weeks. Bone replaces eighth weeks.


Development of the heaD anD neck
622
4
noItceS
CALVARIA two bones appear to be separated by a wide gap at the coronal suture;
in fact, this gap only shows the separation of the mineralized parts of
The bones of the calvaria (roof and lateral walls of the neurocranium) the bone – the unmineralized edge of the parietal bone actually over-
are formed entirely by intramembranous ossification. They are also laps the caudal edge of the frontal bone. After the upgrowth phase,
described as dermal bones, since they are considered to be the evolu- mineralization takes place centrifugally from the central points of the
tionary descendants of dermal plates formed as a protective cover for frontal and parietal bones, which, by this time, form convex plates over
the brain in fishes. In humans, as in all mammals, the major part of the curvature of the underlying brain (see Fig. 36.20D).
the calvaria is formed by paired frontal and parietal bones and the During vaginal birth, the overlap of the frontal and parietal bones
unpaired interparietal (membranous part of the occipital bone). The enables them to slide over each other. During the neonatal period,
squamous part of the temporal bones and the alisphenoids contribute when the baby cries and intracranial pressure rises, the overlapping
to the lateral walls. Lineage data from mouse studies indicate that the bones slide apart, increasing the fronto-occipital diameter of the skull.
frontal and squamous temporal bones are of neural crest origin and the Growth at the coronal suture provides the major increase in the fronto-
parietals are of mesodermal origin; the interparietal is mixed (Jiang occipital plane of the calvaria. Premature synostosis of the coronal
et al 2002). The coronal suture thus forms at the neural crest–mesoderm sutures restricts growth in this plane, causing brachycephaly; unilateral
interface, as does the sagittal suture, due to a small tongue of neural coronal synostosis leads to plagiocephaly, in which one side of the skull


crest tissue lying between the two developing bones. These tissue inter- fails to grow in the fronto-occipital plane. Uni- and bilateral coronal
faces are significant for initiating the molecular signalling system that synostosis comprises 20–25% of all forms of craniosynostosis.
governs growth of the calvaria. Growth at the borders of adjacent bone, The metopic and sagittal sutures are formed when the upwardly
i.e. in the sutures, is the major mechanism of calvarial growth. A extending frontal and parietal bones (respectively) reach the vertex of
sequence of events that maintains a balance between cell proliferation the skull and abut in the median plane. Growth in these sutures
and osteogenic differentiation is mediated by an intercellular signalling increases the breadth of the skull. Premature fusion results in the forma-
system that includes the transcription factor TWIST and ligand–receptor tion of a narrow, elongated skull. Sagittal synostosis is the most common
interactions between fibroblast growth factors (FGFs) and their recep- form of craniosynostosis (40–55%).
tors (FGFRs). Mutations in the genes encoding these proteins cause The interparietal bone (supranuchal squamous portion of the occip-
premature fusion of the cranial sutures (craniosynostosis), which ital bone) forms from two ossification centres that appear in the eighth
results in deficient growth in the plane perpendicular to the suture (Fig. week. These are considered to be homologous with the paired post-
36.21; Morriss-Kay and Wilkie 2005, Johnson and Wilkie 2011). In parietal bones of reptiles. The fact that they unite to form a single bone
addition to the expansion-related growth that takes place in the sutures, in mammals may be due to the interpolation of a small area of neural
appositional growth, in which bone is laid down on, and resorbed crest that migrates from the hindbrain after neural tube closure (Jiang
from, the bone surfaces, plays an important role in remodelling the et al 2002). Two further ossification centres develop laterally at 12 weeks.
calvarial bones to maintain a degree of curvature that matches the There is, at first, a wide gap occupied by cartilage between the inter-


curved surface of the growing brain. Appositional growth can also parietal and parietal bones, which disappears as the membrane bones
provide some compensatory expansion of the skull in craniosynostosis grow towards each other, forming the lambdoid suture when they abut.
(see Fig. 36.21). The lambdoid suture contributes growth to the caudal border of the
The frontal and parietal bones are initiated as basolateral mesenchy- parietal bones and to the upper part of the occipital bone. Synostosis
mal primordial, which extend upwards between the dermal connective of this suture is relatively rare (fewer than 5% of craniosynostosis cases)
tissue and the mesenchymal dura mater. They do not, as previously and has a less severe effect on overall skull growth than coronal and
thought, differentiate within the mesenchyme of an ‘ectomeninx’ that median fusions. Between the interparietal bone and the foramen
surrounds the brain. As the frontal and then the parietal primordia magnum, the calvaria is completed by endochondral ossification of the
extend upwards, the differentiating osteoblasts secrete osteoid, which supraoccipital component of the occipital bone.
then undergoes mineralization. Only the mineralized parts of the bones In addition to the sutures that are formed where two membrane
are detected in alizarin-stained specimens and X-rays. Clear frontal bones abut, fontanelles are formed where three or four bones meet.
bone primordia are detectable in the superciliary arch region of alizarin- In the median plane, these are the anterior fontanelle, at the junction
stained human embryos by the eighth week. As they become mineral- of the metopic and sagittal sutures, and the posterior fontanelle, at
ized above this level, the parietal bone primordia can also be seen. The the junction of the sagittal and lambdoid sutures. The anterolateral
A B
C D
E F
G H
Fig. 36.21 Craniosynostosis. A–B, Line drawings of frontal and lateral views of sagittal synostosis. C–D, Three-dimensional computed tomography


(3D-CT) scans. Premature fusion of the sagittal suture has restricted growth in breadth of the skull but there is compensatory growth in the fronto-
occipital plane. E–F, Line drawings of frontal and lateral views of bicoronal synostosis. G–H, 3D-CT scans. Premature fusion of both coronal sutures has
restricted growth in the fronto-occipital plane but there is compensatory growth in breadth. The pairs of CT scans are not from the same patients as
those indicated in the line drawings; the endotracheal tube has been digitally removed from D. (CT scans courtesy of P Anslow.)


Skull
623
63
Retpahc
fontanelle lies between the frontal, parietal, greater wing of the sphe- the fetal period, the amount of growth is proportionately less than that
noid and squamous temporal bones; its site after closure is called the of the calvaria, reflecting the dominant influence of brain growth in the
pterion. The posterolateral fontanelle lies between the parietal, petrous latter.
temporal, exoccipital and basioccipital bones; after closure, its site is
called the asterion. The size of the fontanelles at birth, and the timing
of their closure, are highly variable. Delayed growth of the skull bones ANTENATAL ULTRASOUND IMAGING OF THE HEAD
causes ossification defects, including cranium bifidum and parietal
AND NECK
foramina, for which several genetic defects have been identified. Cleido-
cranial dysplasia is a defect of ossification affecting the intramembra-
The fetal head appears oval on transthalamic and transventricular
nous part of the clavicle as well as the calvaria; it is caused by
planes, symmetrical and broader posteriorly (see Fig. 14.4). Biparietal
haploinsufficiency of the bone master gene RUNX2.
diameter and head circumference are routinely measured. The size of
the cisterna magna can be estimated to note hypoplasia of the posterior
MEMBRANE BONES OF THE FACE fossa of the skull. Increased thickness of the nuchal tissues at the back
AND VISCEROCRANIUM of the neck, measured from the outer edge of the occipital bone to the
outer skin edge, is part of screening for Down’s syndrome (Nafziger and
Vilensky 2014). Nuchal translucency is increased in a number of triso-
The face and viscerocranium are formed from neural crest-derived
mies and in fetuses with congenital heart defects (Chen 2010). The
membrane bones. The facial skeleton includes, from forehead to chin:
causes of this are complex and include an increase in hyaluronic acid
the frontal bones, the orbital bones (frontal, lacrimal and zygomatic),
in the extracellular matrix in the nuchal skin folds, aberrant jugular


the nasal bones and the vomer, the maxilla and the mandible. The
lymphatic flow and disturbed venous–lymphatic differentiation leading
maxilla and mandible form from first arch mesenchyme, as do the
to local oedema (de Mooij et al 2010).
medial pterygoid plates of the sphenoid bone, the palatine and
Prenatal diagnosis of asymmetrical craniodystosis and of cranio-
the tympanic bones.
facial syndrome has been reported. Facial clefting can be identified,
During migration, the trigeminal neural crest cells divide into a
although demonstration of isolated cleft palate is difficult (Twining
frontonasal population that migrates superior to the eye and comes to
2007). Abnormalities of the fetal neck are uncommon.
surround the telencephalon and part of the diencephalon, a mandibu-
lar population that migrates into the first pharyngeal arch, and a max-
illary population that forms the maxillary swelling (see Fig. 36.2). The
frontal, lacrimal, nasal bones, the vomer and the premaxillary (incisor POSTNATAL GROWTH OF THE SKULL
tooth-bearing) part of the maxilla are derived from the frontonasal
mesenchyme; the maxilla and zygoma are derived from the maxillary Postnatal growth of the skull is characterized by changing proportions
mesenchyme; and the mandible and tympanic bone are derived from of its components. Growth of the brain continues to be extremely
the mandibular mesenchyme. The mandible is the first membrane rapid in the first 2 years. The metopic suture fuses during the first year,
bone to begin ossification; its single ossification centre appears in the by which time the rapid phase of increase in breadth of the forehead
seventh week. The maxilla and premaxilla have primary ossification is complete; further growth and remodelling of the frontal bones is
centres by 7 weeks, and three further ossification centres (orbitonasal, mediated by appositional growth. The sagittal suture continues as an
nasopalatine and zygomatic) form in the maxillary mesenchyme at active growth centre until puberty, when growth of the brain is com-


8 weeks; these components fuse to form a single bone, in contrast plete. In addition to continuing growth of the frontal and parietal
to some mammals, in which the incisor-bearing premaxillary part bones, the squamous temporal bone increases in size so that it con-
remains separate. In the neonatal skull, the suture between the primary tributes a greater proportion of the calvaria in the adult than in the
(premaxilla-derived) and secondary parts of the palate is still patent. neonate (Fig. 36.22). The inner ear and the petrous temporal bone
By 8 weeks, ossification centres for most of the facial and viscero cranial around it grow very little after birth, so the increasing breadth of the
bones are present, except for the tympanic ring, for which four ossifi- skull draws the petrous temporal bone out laterally, creating the bony
cation centres appear at 12 weeks. They fuse to form the sickle-shaped external acoustic meatus. The tympanic ring (with the tympanic mem-
bone that supports the tympanic membrane (see Fig. 36.6). There is as brane) lies at the surface of the meatus in the neonatal skull; it remains
much anteroposterior as vertical growth in the first 5 years of life. After at the proximal end of the deepening canal. Use of sternocleidomas-
the age of 5 years, there is more vertical growth. During the first 5 years toid to lift the head results in formation of the mastoid process of the
of life, there is a steady increase in maxillary volume; maxillary growth temporal bone, which develops air-filled spaces (mastoid air cells) that
rate accelerates during the time that the permanent dentition is devel- are continuous with the middle ear cavity. The paranasal sinuses begin
oping and erupting (Langford et al 2003). to form in late fetal life as diverticula from the nasal cavity that gradu-
The mandible is a developmentally complex bone. Although the ally invade the maxilla, frontal, ethmoid and sphenoid bones. At birth,
body of the bone is formed by intramembranous ossification, the coro- small ethmoidal and maxillary sinuses are present, but the frontal


noid region and condyle are formed by endochondral ossification in sinus is nothing more than an out-pouching from the nasal cavity, and
cartilage that develops after formation of the membrane bone. These there is no pneumatization of the sphenoid bone (p. 566). Thickening
secondary ossification centres form at 10–14 weeks. Distal cartilage of the skull bones is accompanied by increasing size of the sinuses,
forms two further secondary ossification centres, the mental ossicles, at and by a change in form of the sutures, from straight to wavy lines
7 months. This complex system enables the mandible to grow at both and, finally, to the complex interdigitations seen in the adult. After
proximal and distal ends, analogous to a long bone. growth ceases, the skull sutures contain inert connective tissue and
Growth of the face occurs in the sutures between the membrane some cartilage; in old age, some of them are completely replaced by
bones in a similar manner to that of the calvarial sutures but, during bone (natural synostosis).
a a
b b
Fig. 36.22 During postnatal growth of the skull, the viscerocranium increases in size relative to the neurocranium. This diagram shows that, with the
height of the cranial vault expressed as similar in newborn and adult skulls (lines a↔b), the facial skeleton increases particularly rapidly during childhood
and puberty.


Development of the head and neck
623.e1
63
Retpahc
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SUBSECTION: Special senses
CHAPTER
37
External and middle ear
By convention, the ear is subdivided into three parts: the external, root by a squamosal foramen, which transmits the petrosquamous
middle and inner ear. It is largely, but not entirely, contained within sinus. The anterior root juts almost horizontally from the squamous
the temporal bone. The ears not only receive, modulate, conduct, part. Its inferior surface, with an anteroposterior convexity, forms a
amplify and discriminately analyse the complex pressure waves that are short semi-cylindrical articular tubercle and comes into contact with
sound, but also contain the end organs of balance. the articular disc of the temporomandibular joint. The tubercle forms
the anterior limit of the mandibular fossa.
The anterior part of the zygomatic process is thin and flat, and the
TEMPORAL BONE
temporal fascia is attached to its superior border. The inferior border is
short and arched, and gives origin to some fibres of masseter. The lateral
Each temporal bone consists of four components: the squamous, petro- surface is convex. The medial surface is concave and provides further
mastoid and tympanic parts and the styloid process (Fig. 37.1). The attachment for part of masseter. The anterior end is deeply serrated and
squamous part has a shallow mandibular fossa associated with the slopes obliquely posteroinferiorly to articulate with the temporal
temporomandibular joint (Ch. 32). The petromastoid part is relatively process of the zygomatic bone, forming the zygomatic arch. Anterior to
large; its petrous portion houses the auditory apparatus and is formed the articular tubercle, a small triangular area forms part of the roof of
of compact bone. In contrast, the mastoid process is trabecular and the infratemporal fossa; it is continuous behind with the anterior root
variably pneumatized. The tympanic part has the form of a thin and and in front with the infratemporal crest of the greater wing of the
incomplete ring whose ends are fused with the squamous part. The sphenoid.
styloid process gives attachment to the styloid group of muscles. The
Mandibular fossa


temporal bone contains two canals. The external acoustic meatus (exter-
nal auditory canal), visible on the lateral surface, conveys sound waves The mandibular fossa is limited in front by the articular eminence
to the tympanic membrane and the internal acoustic meatus (internal of the zygomatic process. It presents an anterior articular area, formed
auditory canal), evident on the medial surface, through which the facial by the squamous part, and a posterior non-articular area, formed by
and vestibulocochlear nerves pass. the tympanic element. The articular surface is smooth, oval and concave,
and contacts the articular disc of the temporomandibular joint. Unlike
Squamous part most other synovial joints, it is lined by fibrous tissue rather than
hyaline cartilage, reflecting its intramembranous development. The
non-articular area sometimes contains part of the parotid gland. A
The squamous part lies anterosuperiorly, and is thin and partly trans-
small, conical postglenoid tubercle separates the articular surface later-
lucent. Its external temporal surface is smooth, slightly convex, and
ally from the tympanic plate.
forms part of the temporal fossa, to which temporalis muscle is attached.
Posteriorly, the mandibular fossa is separated from the tympanic
Above the external acoustic meatus, it is grooved vertically by the
part by the squamotympanic fissure. Rarely, a postglenoid foramen
middle temporal artery. The supramastoid crest curves backwards and
exists anterior to the external acoustic meatus in the line of fusion of
upwards across its posterior part and gives attachment to the temporal
the squamous and tympanic parts. When present, it replaces the squa-
fascia. The junction between the squamous and mastoid parts is approx-
mosal foramen noted above and transmits the petrosquamous sinus.
imately 1.5 cm below this crest, and traces of the squamomastoid
Medially, a projection from the petrous part of the temporal bone
suture may persist. The suprameatal triangle, a depression marking the
(tegmen tympani) comes to lie within the squamotympanic fissure,
position of the mastoid antrum (which is medial to the triangle at a


further dividing it into petrotympanic and petrosquamous fissures. The
depth of approximately 1.25 cm), lies between the anterior end of the
petrotympanic fissure leads into the tympanic cavity and contains an
supramastoid crest and the posterosuperior quadrant of the external
anterior malleolar ligament and the anterior tympanic branch of the
acoustic meatus. The triangle usually contains a small suprameatal
maxillary artery. The anterior opening of the anterior canaliculus for the
spine anteriorly.
chorda tympani nerve lies at the medial end of the fissure.
The internal cerebral surface of the squamous part is concave and
contains depressions that correspond to convolutions of the temporal
Petromastoid part
lobe of the cerebral hemisphere. This surface is grooved by the middle
meningeal vessels. Its lower border is fused to the anterior region of the
petrous part but traces of a petrosquamosal suture often appear in adult The petromastoid part of the temporal bone, although morphologically
bones. The superior border is thin and bevelled internally; it overlaps one element, is more conveniently described as two parts, namely:
the inferior border of the parietal bone at the squamosal suture. Pos- mastoid and petrous parts.
teriorly, it forms an angle with the mastoid element. The anteroinferior
Mastoid part
border, thin above and thick below, meets the greater wing of the sphen-
oid bone; it is bevelled internally above, and bevelled externally below. The mastoid part is the posterior region of the temporal bone and has
The squamous part has a zygomatic process and a mandibular fossa. an outer surface roughened by the attachments of the occipital belly of
occipitofrontalis and auricularis posterior. A mastoid foramen, of vari-
Zygomatic process able size and position, and traversed by a vein from the sigmoid sinus
The zygomatic process juts forwards from the lower region of the squa- and a small dural branch of the occipital artery, frequently lies near its
mous part. Its triangular posterior aspect has a broad base that is posterior border. The foramen may be in the occipital or occipitotem-


directed laterally, presenting superior and inferior surfaces. The zygo- poral suture; it may sometimes be parasutural or may be absent.
matic process then twists anteromedially, so that its surfaces become The mastoid part projects down as the conical mastoid process and
medial and lateral. is larger in adult males. Sternocleidomastoid, splenius capitis and lon-
The superior surface of the posterior part is concave. The inferior gissimus capitis are all attached to its lateral surface, and the posterior
surface is bounded by anterior and posterior roots, converging into the belly of digastric is attached to a deep mastoid notch on its medial
anterior part of the process. The tubercle of the zygomatic root gives aspect. The occipital artery runs in a shallow occipital groove that lies
attachment to the lateral temporomandibular ligament at the junction medial to the mastoid notch. The internal surface of the mastoid
of the roots. The posterior root is prolonged forwards above the external process bears a deep, curved sigmoid sulcus for the sigmoid venous
acoustic meatus, its upper border continuing into the supramastoid sinus; the sulcus is separated from the underlying innermost mastoid
624 crest. Very rarely, the squamous part is perforated above the posterior air cells by a thin lamina of bone.


625
73
RETPAHC
Temporal bone
A
Groove for middle temporal artery
Parietal margin
Suprameatal triangle
Squamous part, temporal surface
Supramastoid crest
Sphenoidal margin
Parietal notch
Suprameatal spine
Zygomatic process Mastoid foramen
Occipital margin
Articular tubercle
Tympanomastoid fissure
Mandibular fossa, articular surface
Petrotympanic fissure Mastoid notch
Sheath of styloid process
Mastoid process
Styloid process
Tympanic part
External acoustic meatus
Parietal margin
B
Parietal notch
Arcuate eminence
Squamous
Petrous part, part, cerebral
superior border surface
Mastoid foramen
Sphenoidal
Occipital margin margin
Subarcuate fossa
Groove for sigmoid sinus
Opening of vestibular canaliculus Apex of petrous part
Intrajugular process
Internal acoustic meatus
Styloid process
C Sphenoidal margin
Carotid canal
Apex of petrous part
Zygomatic process
Carotid canal
Articular tubercle
Opening of
cochlear canaliculus Mandibular fossa
Petrotympanic fissure
Jugular fossa
External acoustic meatus
Sheath of styloid process
Tympanic part
Styloid process
Stylomastoid foramen
Mastoid process
Occipital margin
Mastoid notch
Occipital groove
Fig. 37.1 The left temporal bone. A, Lateral aspect. B, Medial aspect. C, Inferior aspect. (With permission from Waschke J, Paulsen F (eds), Sobotta
Atlas of Human Anatomy, 15th ed, Elsevier, Urban & Fischer. Copyright 2013.)


ExTERnAl And middlE EAR
626
4
nOiTCES
The superior border of the mastoid part is thick and serrated for The superior border, the longest, is grooved by the superior petrosal
articulation with the mastoid angle of the parietal bone. The posterior sinus. The attached margin of the tentorium cerebelli is fixed to the
border is also serrated and articulates with the inferior border of the edges of the groove except at its medial end, where it is crossed by the
occipital bone between its lateral angle and jugular process. The roots of the trigeminal nerve. The posterior border, intermediate in
mastoid element is fused with the descending process of the squa- length, bears a sulcus medially, which forms, together with the occipital
mous part; below, it appears in the posterior wall of the tympanic bone, a gutter for the inferior petrosal sinus. Behind this, the jugular
cavity. fossa contributes (together with the occipital bone) to the jugular
foramen and is notched by the glossopharyngeal nerve. Bone on either
Petrous part
or both sides of the jugular notch may meet the occipital bone and
The petrous part is a mass of bone that is wedged between the sphenoid divide the jugular foramen into two or three parts. The anterior border
and occipital bones in the cranial base; it contains the labyrinth. It is is joined laterally to the squamous part of the temporal bone at the
inclined superiorly and anteromedially, and has a base, apex, three petrosquamosal suture; medially, it articulates with the greater wing of
surfaces (anterior, posterior and inferior) and three borders (superior, the sphenoid bone.
posterior and anterior). Two canals exist at the junction of the petrous and squamous parts,
The base would correspond to the part that lies on the base of the one above the other, separated by a thin osseous plate and both leading
skull and is separated from the squamous part by a suture. However, to the tympanic cavity; the upper canal contains tensor tympani, while
this suture disappears soon after birth. The subsequent development of the lower canal is the pharyngotympanic tube.


the mastoid processes means that the precise boundaries of the base
are no longer identifiable. Tympanic part
The apex, blunt and irregular, is angled between the posterior border
of the greater wing of the sphenoid and the basilar part of the occipital
The tympanic part of the temporal bone is a curved plate below the
bone. It contains the anterior opening of the carotid canal and limits
squamous part and anterior to the mastoid process. Internally, it fuses
the foramen lacerum posterolaterally.
with the petrous part and appears between this and the squamous part,
The anterior surface contributes to the floor of the middle cranial
where it is inferolateral to the auditory orifice. Behind, it fuses with the
fossa (Ch. 28) and is continuous with the cerebral surface of the squa-
squamous part and mastoid process, and is the anterior limit of the
mous part (although the petrosquamosal suture often persists late in
tympanomastoid fissure. Its concave posterior surface forms the anter-
life). The whole surface is adapted to the inferior temporal gyrus.
ior wall, floor and part of the posterior wall of the external acoustic
Behind the apex is a trigeminal impression for the trigeminal ganglion.
meatus. The tympanic membrane is attached to a narrow tympanic
Bone anterolateral to this impression roofs the anterior part of the
sulcus on its medial surface. The quadrilateral concave anterior surface
carotid canal but is often deficient. A ridge separates the trigeminal
is the posterior wall of the mandibular fossa and may contact the
impression from another hollow behind, which partly roofs the intern-
parotid gland. Its rough lateral border forms most of the margin of the
al acoustic meatus and cochlea. This, in turn, is limited behind by the
osseous part of the external acoustic meatus and is continuous with its
arcuate eminence, which is raised by the superior (anterior) semicircu-
cartilaginous part. Laterally, the upper border is fused with the back of
lar canal but is not necessarily directly over it. Laterally, the anterior
the postglenoid tubercle; medially, it forms the posterior edge of the


surface roofs the vestibule and, partly, the facial canal. Between the
petrotympanic fissure. The inferior border is sharp and splits laterally
squamous part laterally and the arcuate eminence and the hollows just
to form, at its root, the sheath of the styloid process (vaginal process).
described medially, the anterior surface is formed by the tegmen
Centrally, the tympanic part is thin and is often perforated. The stylo-
tympani, a thin plate of bone that forms the roof of the mastoid
mastoid foramen lies between the styloid and mastoid processes; it
antrum, and extends forwards above the tympanic cavity and the canal
represents the external end of the facial canal, contains part of the
for tensor tympani. The lateral margin of the tegmen tympani meets
aponeurosis of the posterior belly of digastric, and transmits the facial
the squamous part at the petrosquamosal suture, turning down in front
nerve and stylomastoid artery.
as the lateral wall of the canal for tensor tympani and the osseous part
of the pharyngotympanic tube; its lower edge is in the squamotympanic
Styloid process
fissure. Anteriorly, the tegmen bears a narrow groove related to the
greater petrosal nerve (which passes posterolaterally to enter the bone
by a hiatus anterior to the arcuate eminence). The groove passes for- The styloid process is slender and pointed, and projects anteroinferiorly
wards to the foramen lacerum. A smaller and similar hiatus and groove from the inferior aspect of the temporal bone. Its length varies, ranging
may be found more laterally; they are related to the lesser petrosal nerve from a few millimetres to an average of 2.5 cm. Often almost straight,
(which runs to the foramen ovale). The posterior slope of the arcuate it can show a curvature, an anteromedial concavity being most common.
eminence overlies the posterior and lateral semicircular canals. Lateral Its proximal part (tympanohyal) is ensheathed by the tympanic plate,


to the eminence, the posterior part of the tegmen tympani roofs the especially anterolaterally, while muscles and ligaments are attached to
mastoid antrum. its distal part (stylohyal). In vivo, its relationships are important. The
The posterior surface contributes to the anterior part of the posterior styloid process is covered laterally by the parotid gland; the facial nerve
cranial fossa and is continuous with the internal surface of the mastoid crosses its base; the external carotid artery crosses its tip, embedded in
part. The opening of the internal acoustic meatus lies near its centre. A the parotid; and medially, the process is separated from the beginning
small slit leading to the vestibular aqueduct lies behind the opening of of the internal jugular vein by the attachment of stylopharyngeus.
the meatus, almost hidden by a thin plate of bone. This contains the
saccus and ductus endolymphaticus, together with a small artery and External acoustic meatus
vein. The terminal half of the saccus endolymphaticus protrudes
through the slit between the periosteum and dura mater. The subarcuate
The temporal bone contains the bony (osseous) part of the external
fossa lies above these openings.
acoustic meatus.
The irregular inferior surface is part of the exterior of the cranial base.
Near the apex of the petrous part, a quadrilateral area is partly associ-
Ossification
ated with the attachment of levator veli palatini and the cartilaginous
pharyngotympanic tube, and partly connected to the basilar part of the
occipital bone by dense fibrocartilage. Behind this region is the large, The four temporal components ossify independently (Fig. 37.2). The
circular opening of the carotid canal, and behind the opening of the squamous part is ossified in a sheet of condensed mesenchyme from a
canal is the jugular fossa, which is of variable depth and size, and con- single centre near the zygomatic roots, which appears in the seventh or
tains the superior jugular bulb. The inferior ganglion of the glossopha- eighth week in utero. The petromastoid part has several centres that


ryngeal nerve lies in a triangular depression anteromedial to the jugular appear in the cartilaginous otic capsule during the fifth month; as many
fossa (below the internal acoustic meatus). At its apex is a small opening as 14 have been described. These centres vary in order of appearance.
into the cochlear canaliculus, occupied by the perilymphatic duct (a Several are small and inconstant, soon fusing with others. The otic
tube of dura mater) and a vein draining from the cochlea to the internal capsule is almost fully ossified by the end of the sixth month. The
jugular vein. A canaliculus for the tympanic nerve from the glossopha- tympanic part is also ossified in mesenchyme from a centre identifiable
ryngeal nerve lies on the ridge between the carotid canal and the jugular about the third month; at birth, it is an incomplete tympanic ring,
fossa. The mastoid canaliculus for the auricular branch of the vagus deficient above, its concavity grooved by a tympanic sulcus for the
nerve is laterally positioned in the jugular fossa. Behind the jugular tympanic membrane. The malleolar sulcus for the anterior malleolar
fossa, the rough quadrilateral jugular surface is covered by cartilage that process, chorda tympani and anterior tympanic artery inclines obliquely
joins it to the jugular process of the occipital bone. downwards and forwards across the medial aspect of the anterior part


External ear
627
73
RETPAHC
Fig. 37.3 The lateral
1 surface of the left
Petrosquamous fissure auricle. Key: 1, helix;
7 2, crus of helix; 3,
auricular tubercle; 4,
Squamous part 5 antihelix; 5, crura of
6 antihelix; 6, triangular
3 fossa; 7, scaphoid
fossa; 8, concha of
5 auricle; 9, external
acoustic meatus; 10,
tragus; 11, antitragus;
2 4
Petrous part 12, intertragic notch;
13, lobule of auricle.
Tympanic part 10 9 8 (With permission from
Berkovitz BKB,
Moxham BJ 2002 Head
12 11 and Neck Anatomy.
Fig. 37.2 The left temporal bone at birth. (With permission from Waschke London: Martin Dunitz.)
J, Paulsen F (eds), Sobotta Atlas of Human Anatomy, 15th ed, Elsevier,
Urban & Fischer. Copyright 2013.)
13
of the ring. The styloid process develops from two centres at the cranial
end of cartilage in the second visceral or hyoid arch; a proximal centre
for the tympanohyal appears before birth, and another, for the distal
stylohyal, appears after birth. The tympanic ring unites with the squa-
mous part shortly before birth, and the petromastoid fuses with it and
the tympanohyal during the first year. The stylohyal does not unite with middle ear cavity is as large as it is in the adult but the pharyngeal
the rest of the process until after puberty and may never do so. opening in the nasal part of the pharynx is relatively smaller. The course
Once ossified, the tympanic cavity, mastoid antrum and the pos- of the pharyngotympanic tube is horizontal in the newborn, whereas
terior end of the pharyngotympanic tube become surrounded by bone. in the adult it passes from the middle ear downwards, forwards and
The petrous part forms the roof, floor and medial wall of the cavity, medially.


while the squamous and tympanic parts, together with the tympanic
membrane, form its lateral wall. At birth, the middle and inner ears are
adult size, and the tympanic cavity, mastoid antrum, tympanic mem- EXTERNAL EAR
brane and auditory ossicles are all almost adult size. The anterior
process does not join the malleus until 6 months later. The internal The external ear consists of the auricle, or pinna, and the external
acoustic meatus is approximately 6 mm in horizontal diameter, 4 mm acoustic meatus. The auricle projects to a variable and individual degree
in vertical diameter and 7 mm in length at birth, and the adult diam- from the side of the head. It collects sound waves and conducts them
eters are 7.7 mm and 11 mm, respectively. along the external acoustic meatus inwards towards the ear drum, the
After birth and apart from general growth, the tympanic ring extends tympanic membrane. The auricle thus acts as the first element of a series
posterolaterally to become cylindrical, growing into a fibrocartilaginous of stimulus modifiers in the auditory apparatus.
tympanic plate, which forms the adjacent part of the external acoustic
meatus at this stage. This growth is not equal but is rapid in the anterior
and posterior regions, which meet and blend. Thus, for a time, an AURICLE (PINNA)
opening (foramen of Huschke) exists in the floor; it usually closes at
about the fifth year but is sometimes permanent. The external acoustic The lateral surface of the auricle is irregularly concave, faces slightly
meatus is relatively as long in children as it is in adults, but the canal forwards, and displays numerous eminences and depressions (Fig.
is fibrocartilaginous, whereas its medial two-thirds are osseous in 37.3). It has a prominent curved rim, the helix. This usually bears a
adults. Surgical access to the tympanic cavity is via the mastoid antrum, small tubercle posterosuperiorly, Darwin’s tubercle, which is quite pro-
and in children it is necessary to remove only a thin scale of bone in nounced around the sixth month of intrauterine life. The antihelix is a


the suprameatal triangle to reach the antrum. The tympanic plate curved prominence, parallel and anterior to the posterior part of the
ensheathes the styloid process by posterior extension, and extends helix; it divides above into two crura, which flank a depressed triangular
medially over the petrous bone to the carotid canal. fossa. The curved depression between the helix and antihelix is the
Initially, the mandibular fossa is shallow, facing more laterally, but scaphoid fossa. The antihelix encircles the deep, capacious concha of
it then deepens and ultimately faces downwards. Posteroinferiorly, the the auricle, which is incompletely divided by the crus or anterior end
squamous part grows down behind the tympanic ring to form the of the helix. The conchal area above this, the cymba conchae, overlies
lateral wall of the mastoid antrum. The mastoid part is at first flat, so the suprameatal triangle of the temporal bone, which can be felt
that the stylomastoid foramen and rudimentary styloid process are through it, and which overlies the mastoid antrum. The tragus is a small
immediately behind the tympanic ring. The mastoid part becomes curved flap below the crus of the helix and in front of the concha; it
invaded by air cells, especially at puberty. The lateral mastoid region projects posteriorly, partly overlapping the meatal orifice. The antitragus
grows downwards and forwards to form the mastoid process, which is a small tubercle opposite the tragus and is separated from it by the
means that the styloid process and stylomastoid foramen become in- intertragic incisure or notch. Below it is the lobule, composed of fibrous
ferior. Descent of the foramen lengthens the facial canal. The mastoid and adipose tissues. It is soft, unlike the majority of the auricle, which
process is not perceptible until late in the second year; consequently, is supported by elastic cartilage and is firm. The cranial surface of the
the facial nerve is relatively superficial and susceptible to damage during auricle presents elevations that correspond to the depressions on its


surgical exploration during this period. The subarcuate fossa gradually lateral surface and after which they are named (e.g. eminentia conchae,
fills and is almost obliterated. eminentia fossae triangularis).
In the neonate, the petrous and squamous parts of the temporal At birth, most of the linear dimensions of the auricle are approxi-
bone are usually partially separated by the petrosquamous fissure, mately three-quarters of their adult size; the length and height of the
which opens directly into the mastoid antrum of the middle ear. Rarely, tragus are less than half of their adult size. Width dimensions mature
the fissure closes in infants during the first year but it sometimes between the ages of 5 and 11 years; length dimensions mature between
remains unclosed up to the age of 19 years; it is a route for the spread 12 and 16 years (Purkait 2013).
of infection from the middle ear to the meninges. There is a bimodal
Common congenital anomalies
growth pattern in the lateral surface dimensions of the temporal bone
in children; marked increases in dimension occur from birth to the age Developmental anomalies of the branchial arches may produce a
of 4 years but little growth is seen between the ages of 4 and 20 years grossly misshapen or microtic auricle, sometimes with associated
(Simms and Neely 1989). The neonatal internal acoustic meatus is anomalies of the middle ear and significant hearing loss. Deformity of
about half the length of its adult counterpart. Its opening from the the pinna may be the result of hereditary factors, exposure to teratogens


ExTERnAl And middlE EAR
628
4
nOiTCES
or unusual intrauterine positioning. A number of common anomalies is no cartilage in the lobule or between the tragus and the crus of the
have been recognized; they carry descriptive names or eponyms (Porter helix, where the gap is filled by dense fibrous tissue. Anteriorly, where
and Tan 2005) (Table 37.1). the helix curves upwards, there is a small cartilaginous projection: the
spine of the helix. Its other extremity is prolonged inferiorly as the tail
Skin of the helix and it is separated from the antihelix by the fissura anti-
tragohelicina (antitragohelicine fissure). The cranial aspect of the carti-
lage bears the eminentia conchae and eminentia scaphae, which
The skin of the auricle continues into the external acoustic meatus to
correspond to the depressions on the lateral surface. The two eminences
cover the outer surface of the tympanic membrane. It is thin, has no
are separated by a transverse furrow, the sulcus antihelicis transversus,
dermal papillae, and is closely adherent to the cartilaginous and osseous
which corresponds to the inferior crus of the antihelix on the lateral
parts of the canal; inflammation of the canal skin is very painful because
surface. The eminentia conchae is crossed by an oblique ridge, the
of this attachment to the underlying structures. The thick subcutaneous
ponticulus, for the attachment of auricularis posterior. There are two
tissue of the cartilaginous part of the meatus contains numerous ceru-
fissures in the auricular cartilage, one behind the crus of the helix and
minous glands that secrete wax, or cerumen. Their coiled tubular struc-
another in the tragus.
ture resembles that of sweat glands. The secretory cells are columnar
when active but cuboidal when quiescent; they are covered externally
by myoepithelial cells. Ducts open either on to the epithelial surface or Ligaments
into the nearby sebaceous gland of a hair follicle. Cerumen prevents