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 Table of Contents  
Year : 2017  |  Volume : 4  |  Issue : 1  |  Page : 37-64

Pathologic anatomy of the soft palate, part 1: Embryology, the hard tissue platform, and evolution

Division of Plastic Surgery, Saint Louis University, St. Louis, Missouri, USA; Department of Surgery, Military Teaching Hospital Dr. Alejandro Dávila Bolaños, Managua; Department of Surgery, Teaching Hospital Oscar Danilo Rosales Argüello, National University of Nicaragua – Leon, Nicaragua

Date of Web Publication2-May-2017

Correspondence Address:
Michael H Carstens
160, South Virginia Avenue, Falls Church City, VA 22046

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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jclpca.jclpca_9_17

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The purpose of this communication is to explore in detail the developmental anatomy of the soft palate, its pathologies, and strategies for management. Despite the voluminous literature regarding complete cleft palate in its usual presentation, little attention has been paid to the biology of the isolated soft palate cleft. It exists as a spectrum, ranging in severity from the submucous variant, with nothing notable save a groove and a palpable defect of the posterior spine, all the way to a complete disruption of the soft tissue envelope and the horizontal palatine shelves. All these presentations are but variations of common pathology. Much can be gained from a disciplined examination of these. Our discussion includes two parts. The first part is on the embryologic events that generate the mesenchymal building blocks from which the posterior palate is constructed: palatine bone, oral and nasal mucosa, palatine aponeurosis, and muscle slings. Palate structures develop from neural crest and mesoderm; these tissues originate at specific sites along the axis of the embryo and they can be mapped according to the developmental units of the central nervous system (CNS) from which they are innervated. These units, called neuromeres, are specific zones within the neural tube, the boundaries of which are established by the expression pattern of homeotic genes. The forebrain (prosencephalon) has telencephalon and 3 prosomeres, the midbrain (mesencephalon) has 1-2 mesomeres, and the hindbrain (rhombencephalon) has 12 rhombomeres. Each neuromere has a specific neuroanatomic content and is hardwired to specific tissues outside the brain. We next consider a model of the palate which is analogous to a pinball machine that consists of a platform (bone) and mobile “flippers” or lever arms (the velum). In this study, the osseous platform is discussed in detail with neural crest bones being coded by the sensory innervation of their surrounding soft-tissue envelope. Maxilla, palatine bone, and vomers are all derivatives of hindbrain neural crest arising from rhombomere 2 but distributed according to various neurovascular pedicles of the V2 stapedial system, the anatomy of which will be explained in detail. Next, the evolution of palate will be presented as a series of innovations favoring increased metabolic capacity. A final appendix presents a functional classification of cranial nerves which I have endeavored to make straightforward. This will prove useful when reading the second part of this manuscript having to do with the neuromuscular apparatus of the soft palate.

Keywords: Cleft palate, embryology, evolution, homeotic gene, maxilla, neuromere, palatine bone, rhombomere, vomer

How to cite this article:
Carstens MH. Pathologic anatomy of the soft palate, part 1: Embryology, the hard tissue platform, and evolution. J Cleft Lip Palate Craniofac Anomal 2017;4:37-64

How to cite this URL:
Carstens MH. Pathologic anatomy of the soft palate, part 1: Embryology, the hard tissue platform, and evolution. J Cleft Lip Palate Craniofac Anomal [serial online] 2017 [cited 2019 Jun 19];4:37-64. Available from: http://www.jclpca.org/text.asp?2017/4/1/37/205416

  Introduction Top

Clefts of the soft palate in the presence of an intact hard palate exist in a spectrum of anatomic severity, from the forme fruste submucous variant to a complete separation of both sides extending forward to the horizontal shelves of the palatine bones and finally into the palatal shelves of the maxilla. What are the underlying mechanisms common to all these presentations? Careful examination of the anatomy of the submucous cleft, as compared with that of the normal soft palate, can yield valuable insights into the embryologic defects responsible for this deformity. The developmental field model provides a rationale for surgical approaches to its repair.

The submucous cleft and indeed all other variations of soft palate clefts share three invariable features: (1) deficiency of the posterior border of the horizontal palatine shelf proper, causing universal absence of posterior nasal spine, (2) concomitant deficiency of the palatine aponeurosis causing anterior foreshortening and anterior displacement of soft palate muscle, and (3) anomalous insertion of levator veli palatini (LVP) into horizontal plate of the palatine bone. All three conditions are grossly abnormal [Figure 1].
Figure 1: Submucous cleft palate. Note triangular deficit in palatine shelves and absent non-muscular aponeurosis leading to forward displacement of the levator complex

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Principle 1

The physical position of the normal soft palate with respect to the posterior pharynx is determined by the relative sizes of the bony components to which it is attached. Normal palatine bones have horizontal shelves extending medially to fuse with one another. Here, they form a small posterior nasal spine associated with the insertion of paired uvulus muscles. Furthermore, the physical location of the palatine bones in space is directly related to the anteroposterior length of maxillary palatal shelves. Thus, foreshortening of the maxilla palate and/or the palatine bone will create conditions of velopharyngeal insufficiency even in the presence of a normal soft palate.

Surgical repairs of the soft palate in the presence of an abnormally short bony platform typically involve trying to gain length by rearrangements of existing tissue relationships, such as intervelar veloplasty and Z-plasties. Such procedures do not address anteroposterior spatial deficit. This predisposes to postoperative velopharyngeal insufficiency. An alternative is the interposition of tissue (buccal flaps) between the deficient bony platform and the soft palate musculature, thus gaining length while leaving the soft-tissue relationships between muscle and aponeurosis undisturbed.

Principle 2

The fundamental defect in the soft palate cleft involves the lesser palatine artery (LPA) and its territory of distribution. The palatine bone and anterior 25% of the palatine aponeurosis develop from a common embryologic tissue source: neural crest from the 2nd rhombomere. These structures are supplied by a common neuroangiosome: LPA and its accompanying branch of V2. Deficiency states of these two structures are shared. Thus, a defective palatine shelf is accompanied by tissue reduction or outright loss of the palatine aponeurosis in its nonmuscular anterior zone attached to the posterior margin of the bone. This will bring tensor veli palatini and associated muscles into abnormal close physical contact with the horizontal palatine shelf.

Principle 3

Mesenchymal deficiency in the horizontal of the palatine bone unmasks a muscle-binding site at which LVP forms an opportunistic false insertion. All soft palate muscles insert into the palatine aponeurosis at programmed binding sites. These are located in the middle half of the soft palate. The program arises from interaction between the r2 neural crest aponeurosis and the r2 endothelium. The anterior 25% of aponeurosis has no binding sites uvula muscle lies nasal to levator and arches over it to insert into the posterior nasal spine. These relationships are always normal. The pathologic insertion of levator into the posterior palatine shelf results from: (1) a foreshortened aponeurosis that brings the muscles forward into contact with the bone and (2) an abnormal bony shelf with missing PNS and no uvular insertion.

Principle 4

Normal function of the soft palate cannot take place when the levator sling is falsely inserted into the palatal shelves.

Principle 5

The individual muscles of the soft palate arise from different mesodermal structures in the embryo. The functional status of each muscle must be determined before surgery.

This chapter presents a developmental analysis of the spectrum of isolated soft palate clefts. The discussion will be organized as follows: (1) general statement of the problem, (2) pharyngeal arches 1–3 and their respective contributions to the soft palate, (3) the mesenchymal composition of the pharyngeal arches, i.e., neural crest and paraxial mesoderm (PAM), and where these tissues originate in the primitive embryo, and (4) specific components of the soft palate – bone, muscle, arterial supply, and innervation. With this basic information, a rational approach to cleft formation can be achieved.

  1. Embryologic components of the soft palate

    • Pharyngeal arch development
    • Components of the pharyngeal arches: Neural crest and mesoderm

  2. The bony platform

    • Palatine bone
    • Palatal shelf of the maxilla

  3. Soft-tissue contents

    • Epithelium and fascia
    • Nerve supply
    • First arch muscle
    • Third arch muscle
    • Blood supply
    • Innervation: Motor and sensory

  4. Pathology of the descending palatine neuroangiosome

    • Lesser palatine axis
    • Greater palatine axis
    • Clinical: Developmental field repair of soft palate cleft.

  Embryologic Components of the Soft Palate Top

Introductory remarks

Our analysis will now turn toward the embryology of the normal palate first in terms of embryologic building blocks: neural crest and mesoderm. This requires some vocabulary from developmental biology regarding neuromeres, neural crest, somitomeres, and pharyngeal arches. We shall then review details of the osseous platform, muscle content, blood supply, and innervation. Further description is readily available in excellent standard texts: Gray's Anatomy (editions 39–41), Carlson (available in Spanish, electronic edition through Amazon).[1],[2],[3]

The soft palate develops from the first three pharyngeal arches, each of which contributes distinct components. The first arch is responsible for nasal and oral epithelium, palatine bone, maxillary palatal shelf, and tensor veli palatini. The second arch contributes to taste buds. The third arch contributes to oral epithelium and all remaining soft palate muscles. This well-known model, unfortunately, has little practical value. It is much more useful to focus our attention on the mesenchyme from which the pharyngeal arches are assembled – neural crest and mesoderm – tissues that will ultimately form the recognizable structures of the hard and soft palate.

All craniofacial structures in the mature organism can be readily mapped backward to their embryonic site of origin during early development. Furthermore, all vertebrate embryos make use of a segmentation system based on homeotic genes that define the axis of the organism based on distinct developmental units of the CNS call neuromeres. By familiarizing ourselves with the neuromeric system, we can understand how the palate is constructed and can recognize how specific tissue deficiencies in this can result in cleft formation [Figure 2] and [Figure 3].
Figure 2: Homeotic genes are read out in 3' to 5' corresponding to the anterior-posterior body axis. They are also responsible for specifying what tissues will be produced at each level of the body shown here is the directional similarity between drosophila and human

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Figure 3: Carnegie staging system

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Anatomy of the pharyngeal arches

Organization of mesenchyme in the embryo

Embryonic development is a process in which simple tissues are progressively assembled into progressively more complex forms of organization. In this model, the five pharyngeal arches represent an intermediate step between simple tissue components and recognizable anatomic structures. Each arch is made of three basic components: (1) epithelium, (2) neural crest, and (3) PAM. The pharyngeal arches are like epithelial saddlebags hanging off the side of the future face. Each bag is quickly filled with neural crest cells arising from the neural folds of the hindbrain. Virtually all the mesenchymal structures of the arches (dermis, fat, fascia, cartilage, and bone) are derivatives of rhombencephalic neural crest (RNC). The bags also receive a contribution of mesoderm from physically adjacent structures called somitomeres. Their role is quite limited. They give rise to striated muscles and blood vessels only. At this point, to keep organized, a timetable of pharyngeal arch formation is useful.

The embryonic period of human development consists of 23 anatomic stages.[4],[5] At stages 6 and 7, the embryonic disc undergoes gastrulation, a three-dimensional transformation into trilaminar structure consisting of the embryonic germ layers ectoderm, mesoderm, and endoderm. Creating a blood supply for the embryo is a two-step process. The extraembryonic vascular system is established at stages 6 and 7, while the intraembryonic vascular system forms at stages 7 and 8 [Figure 4] and [Figure 5].
Figure 4: Stage 7-8: gastrulation (germ layer formation) 1stcells to exit: endoderm (yellow) displaces hypoblast/endoblast (green) 2nd cells to exit: mesoderm (red) will form three distinct zones

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Figure 5: Gastrulation and neurulation Gastrulation begins at r0 and procedes cranial-to-caudal, neuromere-by neuromere When cells exit the primitive streak they acquire the Hox code for that level Mesoderm produced at levels r0 to r8 makes incompletely segmented somitomeres, not somites Lateral plate mesoderm from r0 to r11 is a single mass (not split) and makes only blood vessels

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Mediolateral organization of both ectoderm and mesoderm becomes apparent at stages 7 and 8. This process takes place by virtue of different gradients of gene expression in the midline and at the periphery. The default state of ectoderm is neural. Lateral to the midline, genes expressed by mesoderm cause nonneural ectoderm to form skin. On either side of the neural plate, mesoderm is organized into three developmental zones, depending on the distance away from the neural plate. PAM lies in opposition to the neural plate. It will form the axial skeleton and striated muscles. Intermediate mesoderm (IM), a narrow column extending from C1 in the neck down the length of the embryo, gives rise to the genitourinary system. Lateral plate mesoderm (LPM) forms the appendicular skeleton, vascular system, and internal organs. For our purpose, the pharyngeal arches that make up the palate get their muscles from PAM; their arterial supply (the aortic arch arteries) is constructed from LPM. IM has no craniofacial representation.

Just in front of the neural plate and notochord is a small singular zone of prechordal mesendoderm (PCM). When gastrulation takes place, PCM is the very first mesoderm to appear – it is intimately associated with the underlying endoderm. PCM stays in the midline and forms the endoderm of the buccopharyngeal membrane. With brain growth, signals are exchanged between the forebrain and PCM that are involved with midline separation: the forebrain divides into two hemispheres and the PCM divides and moves laterally to form part of the orbital contents. As PCM separates, the intervening space is immediately filled by midbrain neural crest. Failure of this process to take place results in holoprosencephaly and cyclopia (see chapter 5).

Anteroposterior organization of both CNS and body axis is controlled by homeotic (HOX) genes. The neural plate is programmed into developmental units called neuromeres. Note that each neuromere is defined by a distinct expression pattern of homeotic genes, more like the barcode on your credit card [Figure 6].
Figure 6: Neuromeric system: prosomeres 6, mesomeres 2, rhombomeres 12, myelomeres 31 Neuromeric coding of extracranial tissues occurs during gastrulation, neural crest migration r0 and r1: orbit, isthmus and cerebellum r2-r11 paired rhombomeres supply each pharyngeal arch

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The nomenclature of the neuromeres is as follows: the caudal forebrain (diencephalon) has 3 prosomeres, p1–p3. The prosomeres of the rostral forebrain (telencephalon) are as yet undefined. The midbrain (mesencephalon) has one or two mesomeres depending on the model. The hindbrain (rhombencephalon) has 12 rhombomeres, r0–r11. From a functional standpoint, r2–r11 innervate the five pharyngeal arches. The cerebellum arises from r0 and r1. These two rhombomeres behave as intermediaries between midbrain and the pharyngeal arch system. They act in midbrain-fashion to supply tissues to the orbit and upper 1/3 of the face. Neural crest arising from the neural fold above a given neuromere bears the same homeotic “barcode.” All tissues innervated by it share the common homeotic relationship. They are in register with their nerve supply [Figure 6].

In the process of neurulation during stages 7–8, the neural folds proliferate and roll up like a cigar to form the neural tube. Within the neural folds, neural crest cells differentiate and almost immediately begin to migrate. Rapid brain growth during stage 8 causes the tissues lying anterior to the brain to fold 180° beneath the head. The dorsal aortae, united together with a U-shaped loop in front of the brain, are now directed downward and backward to lie beneath the pharynx. The loop now constitutes paired heart tubes which immediately fuse. By stage 9, cardiac activity is present.

At day 18 (stage 9), PAM lying alongside the forebrain, midbrain, and rostral hindbrain undergoes an HOX-driven segmentation into seven incompletely separate developmental units called somitomeres (Sm1–Sm7) within which the muscles of the head and face will develop. Somitomeres involve a hollow sphere of cells surrounding a central fluid-filled cavity, the somitocoele. The fact that somitomeres are incompletely segmented is important because of their mesenchyme in confluent. Thus, blood vessels formed within one somitomere can link up with those of its neighbors [Figure 7].
Figure 7: Somitomeres (see map by Noden) Orbit: 1-3, 5 1st arch (Sm4), 2nd arch (Sm6), 3rd arch (Sm7) Remaining 37 somitomeres become somites (4+8+12+5+5+3)

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Segmentation of PAM follows a cranial-caudal sequence, with 3–4 new somitomeres produced per day until the final number of 44 is reached. The final count is as follows: 7 craniofacial, 4 occipital, 8 cervical, 12 thoracic, 5 lumber, 5 sacral, and 3 coccygeal.

At day 20 (stage 9) beginning with Sm8, and with all subsequent somitomeres, an additional transformation takes place that converts each somitomere into a somite, a solid mass of cells. Each somite has an epithelial cover that keeps it separate from its neighbors. Each somite is innervated by a single neuromere with which it is in genetic register. The appearance of the first three occipital somites just lateral to the caudal hindbrain is the anatomic definition of stage 9. Stage 10 is defined by the appearance of the fourth somite. The first four somites are in register with the rhombomeres of the medulla, r8–r11. All somites beyond S4 are in register with the spinal cord.

Stages 9–14 are characterized by formation of the five (not six) pharyngeal arches (one per stage). At each stage, a new arch forms and previously formed arches undergo morphogenetic changes. At no time are all five arches distinctly visible. Each arch receives neural crest cells from two rhombomeres with which it is in genetic register. Each arch is divided longitudinally by a genetic axis; the cranial zone is populated by even-numbered neural crest and the caudal zone by odd-numbered neural crest. Within the arches, neural crest responds to positional genes such as the distal-less (Dlx) system to organize and compartmentalize the arches into mesenchymal subsets that, when the arches are repositioned into the face, will differentiate to assume distinct fates such as bone, fascia, and blood vessels. The biology of neural crest is recounted in monographs by LeDourain, Hall, and Trainor.[6],[7],[8],[9]

Cranial to the 1st arch are two types of mesenchymal tissue with unique composition and innervation. (1) Mesencephalic neural crest (MNC) constructs the nonneural tissues of the orbit and all frontonasoethmoid structures. These arise from the midbrain proper (mesomeres, m1 and m2), from the isthmus (r0) that connects midbrain with hindbrain, and from r1. Note that, in neuroembryology, rhombomeres r0 and r1 are considered part of the hindbrain but are functionally more closely related to midbrain. (2) Prosencephalic neural crest (PNC) constructs the frontonasal skin. Rostral PNC (prosomeres p6-p5) makes the epidermis; caudal PNC (prosomeres p4-p1) makes the dermis. The neuromeric system is described by Puelles [Figure 8] and [Figure 9].[10],[11],[12]
Figure 8: Craniofacial neural crest populations Forebrain (diencephalon, p1-p3): frontonasal dermis -- epidermis comes from telencephalon Midbrain neural crest (m1-m2, r0-r1): frontonasal mesenchyme Hindbrain neural crest (r2-r11): pharyngeal arches

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Figure 9: Neural crest migration Prototypical agnathan Ambystoma mexicanum has 7 arches – the first two have not been converted into jaws. NC cells are stellate-shaped and are seen arching over the optic cup and the nasal placode to reach the midline, achieving forebrain coverage. Additional NC cells are seen as the top of the fold flowing downward as future primary meninges.

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Somatic sensation (pain, temperature, etc.) for the entire head is supplied by the sensory nucleus of the trigeminal nerve. This nucleus is quite long and is organized somatotopically. It begins in midbrain and runs all the way down to the spinal cord. The mesencephalic nucleus of V extends throughout the midbrain (m1, m2, r0, and r1). It is also somatotopic and receives input regarding proprioception from the structures of the orbit and frontonasal mesenchyme. The rhombencephalic nucleus of V extends the length of hindbrain, from r2 to r11 and down to c2. It receives input from all the pharyngeal arches.

Sensory supply for craniofacial tissues

Nota Bene for the reader: the identity of the neuromeres that produce the midbrain neural crest (MNC) is poorly appreciated. The midbrain contains two mesomeres marked by external structures: M1 has the superior colliculus associated with vision and m2 has the inferior colliculus associated with hearing. Some authors (Puelles, 2009) map the midbrain with a single mesomere. The midbrain longitudinal fasciculus resides in the midbrain coordinates eye movements; therefore, it is not surprising that the mesomeres are physiologically related to the first two rhombomeres, r0 and r1. All four neuromeres contain nuclei for the extraocular muscles. Oculomotor nuclei reside in both m1 and m2, while rostral r0 contains the decussation of trochlear nerve, and r1 the trochlear nucleus itself [Table 1].
Table 1: Sensory innervation by neuromeres

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The anatomic pathway of V1 sensory nerves and their corresponding V1 stapedial arteries provides a map showing the migration routes of MNC into the orbit and face. The StV1 arteries constitute an “add-on” to the primitive ophthalmic artery. They supply all extraocular structures of the orbit, whereas prOA supplied the globe and optic nerve (see chapter on craniofacial arterial development).

  • V1 innervated neural crest has a truly massive distribution. It provides the prechordal mesoderm with specific contributions to the intrinsic muscles of the eye. It forms the bones of the medial wall and roof of the orbit. All nonmuscular extraocular structures such as fat, fascia, conjunctiva, and sclera are derivatives of r1. The extraorbital distribution of r1 neural crest contributes to the entire fronto-orbital nasal skin envelope, itself a derivative of PNC (a subject covered in the chapter on craniofacial skin and meninges). V1 innervated mucosa of the naso-oropharynx is a derivative of V1 neural crest
  • Fronto-nasal mesenchyme develops from neural crest originating above 6 prosomeres of the forebrain. Epidermis is a product of p6-p5. Dermis is produced by p4-p1. Forebarin has no intrinsic sensory innervation. Therefore, just as in the case of the midbrain, V1 provides sensation. It also programs the various arterial branches of the stapedial system that supply frontonasal mesenchyme,[13] the dermis of which is a derivative of prosomeres p4-p1 and the epidermis of which is formed by non-neural epithelium above prosomeres p6-p5.

Muscle derivatives of the somitomeres

Muscles are mapped to their somitomere of origin on the basis of their motor nerve supply and the neuromere from which the motor nerve arises [13],[14],[15][Table 2] and [Figure 10].
Table 2: Muscle derivatives of somitomeres and somites

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Figure 10: Avian model of somitomeres similar to humans Noden, D. M. and Trainor, P. A. (2005), Relations and interactions between cranial mesoderm and neural crest populations. Journal of Anatomy, 207: 575–601. doi:10.1111/j.1469-7580.2005.00473.x

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Bone derivatives of somitomeres and somites

Bones are mapped on the basis of sensory nerve supply to periosseous soft tissues [Table 3].
Table 3: Bone derivatives of somitomeres and somites

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Formation of the pharyngeal arches [Figure 11],[Figure 12],[Figure 13]
Figure 11: Pharyngeal arches: cartilage fishes (7), bony fishes (6), tetrapods (5)

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Figure 12: Basal gnathostome Raja erinacea 7 gill arches (branchiomeres) 1st branchiomere converted to jaws, 2nd (hyoid) branchiomere remains respiratory Advanced gnathostomes convert 2nd branchiomere into suspension for jaws

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Figure 13: Aortic arches: cartilage fishes (7), bony fishes (6), tetrapods (5) AAs transient - unite ventral aortic outflow tract with dorsal aortae – extensive remodeling AA5 involutes – its target, PA5 is supplied by AA4 AA6 assigned to pulmonary circulation There is no 6th pharyngeal arch in tetrapods

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At stage 8, neural crest cells migrate into the mesoderm, filling out a series of homeotically defined zones, arranged in 5 concentric arcs stretching outward and forward from the hindbrain to the anterior terminus of the embryo. Head flexion these zones will come to lie beneath the brain; they will reorganize into five pharyngeal arches. Midway between the anterior boundary with amnion and the notochord is found the buccopharyngeal membrane (BPM), a fusion between ectoderm and endoderm. Lying between the BPM and the notochord is a singular zone of prechordal plate mesoderm, which becomes split with forebrain separation to form orbital tissues. The gap in PCM is filled with midbrain neural crest to form the frontonasoethmoid complex. Failure of this separation causes cyclopia.

Note that, the distinct contributions of midbrain neural crest versus r0–r1 have not been definitively mapped out. We refer to this ectomesenchyme collectively as midbrain neural crest (MNC) and r1 for short.

Neural crest from r0 to r1 does not participate in the formation of the first pharyngeal arch. It flows forward into the future orbits and the fronto-naso-ethmoid mesenchyme. The migration pathways of r1 neural crest follow the neural network of V1. This nonpharyngeal arch mesenchyme contributes to upper eyelid skin, tarsal plate, conjunctiva, sclera, the fasciae of the extraocular muscles, and the membranous bones of the orbit. Myoblasts from the prechordal mesoderm form the intraocular muscles. Myoblasts from somitomeres 1–3 and 5 migrate into to this zone and form the extraocular muscles.

Neural crest mesenchyme from r2 to r11 flows into five genetically defined zones, the future pharyngeal arches. The blood supply for each arch comes from an aortic arch artery running longitudinally through its core. At 22 days (stage 8), rapid growth of the brain causes a flexure at the level of the midbrain that positions the precranial tissues downward and backward. The remainder of the embryonic disc simultaneously folds laterally and ventrally. The arches are now arranged like a series of five horseshoes hanging downward from the neuraxis. The 5th pharyngeal arch (r10/r11) thus abuts backward against the future neck.

Blood supply to the pharyngeal arches [Figure 14] and [Figure 15][16],[17]
Figure 14: Pharyngeal arches supplied by aortic arch arteries Stage 9: 1stAA results from folding Stages 10-13: AA form from aortic outflow tract, one AA per stage Note physical positioning of somitomeres immediately lateral to neural tube

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Figure 15: Oral mucosal representation of arches prior to remodeling Ectoderm back to buccopharyngeal membrane > endoderm starts @ PA3 PA2 mucosa disappears – PA1/PA3 abut @ 1stpharyngeal pouch (Eustachian tube) PA6 does not exist – PA 5 abuts with C1 at the esophagus Soft palate mucosa: oral side = ectoderm / nasal side = endoderm

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Key concept: The external carotid system supplies all derivatives of all the pharyngeal arches, except the jaws and structures connecting the jaws with the skull.

  • Pharyngeal arch 1: Lingual, nonstapedial maxillary
  • Pharyngeal arch 2: Facial, transverse facial, superficial temporal, posterior auricular, occipital
  • Pharyngeal arch 3: Ascending pharyngeal
  • Pharyngeal arch 4: Superior thyroid
  • Pharyngeal arch 5: Superior thyroid (borrowed from AA4).

Note that, sequential development, involution, and remodeling of the embryonic aortic arches are beautifully demonstrated with scanning electron microscopic studies by Hiruma.[18],[19],[20] We are indebted DH Padget at the Carnegie Institution for describing the development of craniofacial vessels. Trained in medical art at Vassar and by Max Bròdel at Johns Hopkins never went on to medical school but became a world-class self-taught embryologist. Padget's illustrations based on staged human embryos constitute the groundwork for our understanding of vascular development.[21]

What about blood supply for the arches? In the beginning, as soon as mesoderm is formed, it contains angioblasts and endothelial precursor cells. These are wildly invasive. These cells join together to form first vesicles and then cords which remodel as the embryonic blood vessels. This process is first seen at stages 5–6 in the extraembryonic mesoderm of the yolk sac and gives rise to the placental circulation. With gastrulation, intraembryonic mesoderm follows the same rules setting up the intraembryonic circulation. Because these two zones of mesoderm are in physical continuity at the periphery of the embryo, blood supply reaches the conceptus from the mother.[2]

At stage 8, the primitive central intraembryonic arterial system forms by spontaneous aggregation of LPM into paired dorsal aortae running on either side of the neural axis for the entire length of the embryo. Just anterior to the BPM, the LPM is known as cardiogenic mesoderm. Here, dorsal aortae form a U-shaped loop. Fusion of the most anterior part of the loop produces paired primitive heart tubes. The distal tubes will form the atria and the proximal tubes the ventricles and the truncus arteriosus, leading backward to the embryo proper. Brain growth forces this anterior zone to fold downward in a 180 arc such that the heart tubes are tucked underneath the future face. The atria now point backward and the truncus arteriosus points forward.

It is now time for the pharyngeal arches to make their appearance. Running through the center of each arch is an aortic arch artery the walls of which are formed from LPM and neural crest. The first aortic arch arteries (AA1) do not form de novo. They are part of the original vascular circuit that connects the truncus arteriosus of the heart to the dorsal aortae. With head folding, they are stretched and bent downward. At stage 10, the 1st pharyngeal arch is clearly seen and consists of a vascular core (AA1) ensheathed by neural crest, ectoderm, and endoderm, all in genetic register with and innervated from rhombomeres r2 and r3. AA2 is developing at stage 10.

At each successive stage, a new pair of aortic arch arteries arises from a more proximal site along the truncus arteriosus. Around each arterial axis, a new pharyngeal arch is organized. In humans, AA5 quickly involutes, making the final blood supply to all 5th pharyngeal arch derivatives dependent on AA4 and its subsequent iteration as the inferior thyroid artery. The pharyngeal arch period is thus complete by stages 13–14. AA6 is dedicated to the pulmonary circulation and has no relationship with the pharyngeal arch system.

Pharyngeal arches quickly undergo a process of spatial reorganization. At stage 9, the first pharyngeal arch is fully formed with a functional arterial system. At stage 11, during formation of the third pharyngeal arch, PA2 has fused with PA1. By stage 12, when the fourth pharyngeal arch makes its appearance, PA3 had moved internally to PA2. At the juncture, virtually all the epithelium originally associated with PA2 has disappeared. The second arch muscles are sandwiched between the superficial and deep layers of first arch tissues; they are positioned superficial to the tissues of the third arch. The second arch produces two functional groups of muscles: a limited number of muscles for mastication and an extensive catalog of muscles for facial expression. The first group shares with the first arch muscles a common deep investing fascia. The second group is enclosed in a separate superficial investing fascia (SIF) that encompasses the entire head, face, and anterior neck (where it is in known as the epicranius or galea). This plane of the SIF is of great surgical importance. Paul Tessier recognized it as the superficial musculoaponeurotic system.

Extensive vascular reorganization takes place. Of the original four aortic arches supplying the pharyngeal arches, only AA3 retains its representation. It produces two new systems, external carotid and stapedial. These systems supply all nonneural craniofacial tissues. The distribution of the stapedial system is poorly appreciated. These arteries follow the somatic sensory branches of the cranial nerves to supply the meninges, orbit, fronto-orbital-nasal mesenchyme, and all 1st arch tissues deep to the facial muscles.

The physical positioning of the five pharyngeal arches can be likened to that of a Japanese fan. Each arch is tucked inside its predecessor: PA1 and PA2 are melded together, inside of which are PA3> PA4> PA5 [Figure 16].
Figure 16: Hard palate: r2 neural crest membranous bones Both GPA and LPA foramina within palatine bone Axis of mesenchymal deposition: anterior-to-posterior / medial-to-lateral

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The spatial inter-relationships of the pharyngeal arches are reflected in their sensory representation and muscle distribution. The skin of the 1st arch covers over all the remaining arches such that it abuts against cervical skin and scalp. Thus, the sensory representation of the midface and lower face is provided by V2 and V3 (the upper face is innervated by V1). The oronasal pharyngeal representation of r2 first arch mucosa makes a boundary with r1 frontonasal mucosa in the nasopharynx and with r6 third arch mucosa in the oropharynx. The first arch mucosa from r3 covers the caudal oropharynx and abuts backward against r7 third arch mucosa of the fauces. There is no mucosal representation of the 2nd arch in the oropharynx.

The muscles of the 2nd arch are almost entirely incorporated within the “envelope” of the 1st arch. Posteriorly, the 2nd arch muscles lie external to the skull and deep to cervical skin. The boundary between 2nd arch and 3rd arch is seen between (1) buccinator and superior constrictor, and (2) stylohyoid and posterior belly of digastric. Deep and posterior to third arch, the fourth and fifth arches are stacked together like Russian dolls. Thus, PA5 arytenoids lie internal to PA4 structures of the larynx.

Blood supply to nonpharyngeal arch tissues of the face

Having created a three-dimensional model of how the arches are arranged, it is time to move onward to see how their individual components are assembled into the hard and soft palate. Work by DH Padget constitutes a unique contribution to the staged development of the craniofacial.[21] Studies by Diamond in primates provide the model for stapedial development.[22],[23]

Key concept: The stapedial system supplies all the nonpharyngeal arch tissues of the face, dura, and skull [Figure 33], [Figure 34], [Figure 35], [Figure 36], [Figure 37], [Figure 38], [Figure 39], [Figure 40].
Figure 33: Breakdown of 1stand 2nd aortic arches leaves two remnants: primitive mandibular and hyoid, respectively. Hyoid will give off the stapedial stem – which persists at term as the carotico-tympanics artery

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Figure 34: Stapedial stem passes upward through stapes and ascends into tympanic cavity where it divides and exits

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Figure 35: Stapedial system: stages 14-17 hyoid: salmon, stapedial stem: yellow-green, upper division: blue-green, lower division: magenta, V1: orange, V2: blue, V3: green ventral pharyngeal artery and external carotid system: yellow

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Figure 36: Stapedial development (stage 14-17) hyoid: salmon, stapedial stem: yellow-green, upper division: blue-green, lower division: magenta, V1: orange, V2: blue, V3: green ventral pharyngeal artery and external carotid system: yellow. Upper division follows greater petrosal (VII) to Gasserian (trigeminal) ganglion. Lower division follows chorda tympani (VII) to infratemporal fossa where it meet V3

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Figure 37: Ascension of stV3 into the cranial cavity via iddle meningeal nerve creates the middle meningeal artery. StV1 makes anastomosis with primitive ophthalmic. Proximal segment involutes completely

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Figure 38: StV2 and StV3 now combine to form the middle meningeal system. Proximal intracranial StV2 stem involutes from the ganglion backwards to tympanic cavity

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Figure 39: Final configuration Stapedial stem persists as carotico-tympanic artery Inferior division persists as anterior tympanic artery

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Figure 40: Maxillo-mandibualr artery is a hybrid (orange) of ECA and extracranial stapedial. ECA branches (yellow) supply pharygeal arch 1. Stapedial branches (pink) supply neural crest structures: jaws and bones connecting jaws to the skull

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Sensory nerves of the trigeminal system accompany and program the individual arteries of the stapedial and external carotid systems. The neuroangiosomes that result delineate the migratory pathways of neural crest to the face and dura [Table 4].
Table 4: Developmental milestone of orbital stapedial system

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How the trigeminal nerve innervates the dura and programs the stapedial system

During stage 14, the cranial nerves develop rapidly. They (especially trigeminal and facial) determine the trajectories of the stapedial system. The innervation pattern is all-important for programming the branches of the stapedial system. Of particular importance is the anatomic pathway for trigeminal supply to the dura. After leaving the trigeminal ganglion, V1 and V2 travel forward in the lateral wall of the cavernous sinus while V3 descends directly out of the skull. Note that, the most proximal sensory branch of each part of trigeminal is dedicated to the dura.

The following facts about trigeminal are relevant to understand how these nerves conduct the blood supply to the orbit:

  1. V1, upon exiting the cavernous sinus and just before entering the orbit, gives rise to the anterior meningeal nerve supplying the dura of the anterior cranial fossa. It then enters the superior orbital fissure. Once in the orbit, V1 again supplies the dura through a separate dural branch of anterior ethmoid nerve that re-enters the cranial cavity via the cribriform fossa
  2. V2, before exiting the skull through foramen rotundum gives off the middle meningeal nerve to the postorbital dura of anterolateral frontal lobe behind alisphenoid
  3. V3, after exiting the skull through foramen ovale, gives off the recurrent meningeal nerve supplying the temporo-parietal-occipital lobes. This requires that it tracks upward with middle meningeal artery through foramen spinosum.

The stapedial stem divides inside tympanic cavity

The stem of stapedial is the remnant of the primitive hyoid artery to the 2nd pharyngeal arch. When the second aortic arch to PA2 disintegrates at stage 12, it leaves behind a dorsal remnant, the hyoid artery, dangling from the dorsal aorta. With growth of the embryo, the hyoid is repositioned backward toward the otic capsule where it eventually is identified as the sole extracranial branch of ICA.

At stage 14, the definitive circulation of the internal carotid is established. The hyoid artery remains extracranial but it gives off the stapedial stem which immediately tracks upward into the tympanic cavity where stapes forms around it (henceforth the name). Directly beyond stapes, the artery bifurcates. The upper division runs directly forward to the trigeminal ganglion where it picks up V1 and V2 just as the nerves exit the cavernous sinus. The lower division follows chorda tympani out from the tympanic cavity into the face via the pterotympanic fissure. It then picks up V3 sensory nerve just below foramen ovale. All subsequent branches of the stapedial system follow the trajectories of V1, V2 or V3.

Upper division stapedial: Forward to the orbit and upward to V1 dura and V2 dura

The stem artery follows greater petrosal nerve forward to the trigeminal ganglion. Here, it picks up cranial nerves V1 and V2 as they run forward in the lateral wall of cavernous sinus. Immediately upon leaving the sinus both V1 and V2 give off dural branches before exiting the skull. Upper division stapedial artery bifurcates to vascular support for all branches of V1 and V2. These arteries supply: (1) the respective areas of dura and (2) the orbit.

StV1 becomes identifiable at stage 18, enters the orbit during stage 19, and forms an anastomosis with the primitive ophthalmic at stage 20. The “annexation” of stapedial takes place due to the involution of the stapedial stem. Thus, the final product, “ophthalmic artery,” is a hybrid system. Primitive ophthalmic, being derived from ICA, supplies CNS tissue exclusively, i.e., the optic nerve and globe. All remaining tissues of the orbit innervated by V1 are supplied by branches from the derivatives of the original stapedial system.

V2 stapedial artery follows a similar time course. After first giving up a dural branch, it extend forward and by stage 19 it enters the lateral orbit via a separate meningo-orbital foramen in the greater wing of sphenoid. Sometimes this foramen is merely a lateral extension of the superior orbital fissure. StV2 is directed to lateral-most zone of the orbit (Tessier zone 9). At stage 20, the bifurcation of upper division stapedial into StV1 and StV2 becomes a target for a 3rd artery arising from outside the skull and programmed by V3. Extracranial stapedial passes up from below through the foramen spinosum as the middle meningeal nerve and artery. When this anastomosis takes place, the segment that previously connected StV2 with the stapedial stem involutes. StV2 now is converted into the anterior branch of the middle meningeal artery. StV3 subsequently defines the posterior branch of middle meningeal artery.

Lower division stapedial: Forward to the jaws and upward to the V3 dura

As soon as chorda tympani departs from the tympanic cavity, it makes a beeline for the sensory root of V3, where it seeks out lingual nerve by which to convey itself to the tongue. Lower division stapedial tracks along with the nerve. At the same time, the poorly named maxillary branch from external carotid tracks forward toward V3. At stages 18–19, an anastomosis between lower division stapedial and external carotid artery (ECA) creates the hybrid maxillomandibular artery (MMA).

MMA has two functions and three distinct zones. Branches associated with the external carotid supply all original structures of the 1st arch, such as the muscles of mastication, fat, and glands. Branches associated with the stapedial system supply those structures reassigned from the 1st arch: Jaws, the suspensory bones of the maxilla and the dura. The zones of MMA are as follows. Zone 1 – The proximal (mandibular) zone gives off stapedial derivatives that re-enter the skull to supply the tympanic cavity and the dura of the middle and posterior cranial fossa. It also sends StV3 inferior alveolar downward to supply the mandible. The sole ECA branch of the proximal zone supplies mylohyoid. Zone 2 – The branches of the middle (infratemporal) zone are distributed exclusively to muscles of mastication. Zone 3 – The distal (pterygopalatine) zone gives off StV2 branches in the pterygopalatine fossa that are subsequently distributed to the maxilla and its suspensory bones.

Key concept: Anastomoses to the stapedial system result in local changes in blood flow that are responsible for its dissolution.

Reunification and disappearance of the stapedial system

Toward the end of the embryonic period, the anatomy of the stapedial system is drastically altered, making it virtually unrecognizable. Three anastomoses are responsible for these changes.

  1. At stage 20, within the orbit, StV1 is annexed by internal carotid ophthalmic. Its proximal segment dies back to the bifurcation with StV2
  2. Also at stage 18–19, inferior division stapedial joins external carotid just lateral to the sensory root of V3 immediately below its exit from the skull. This anastomosis creates the hybrid MMA
  3. From MMA, middle meningeal artery follows sensory V3 middle meningeal nerve upward to supply the dura. At stage 20, middle meningeal annexes StV2. It does not annex StV1 proximal to the orbit because this segment has already undergone involution. Thus, intracranial middle meningeal becomes a hybrid system: its anterior branch arises from StV2 and its posterior branch arises from StV3.

The common denominator of these anastomoses is the exposure of the distal vessel to higher flow; the proximal segment therefore involutes. StV1 dies backward from the superior orbital fissure to the bifurcation of the superior division. StV2 dies backward from its intersection with StV3. Superior division of stapedial is eliminated completely back to stapes. Inferior division of stapedial distal to stapes persists as the anterior tympanic artery. Proximal to stapes, the stapedial stem persists as the caroticotympanic artery.

Fate of the stapedial system

The intracranial division of stapedial consists of a branch programmed by V1 and a branch programmed by V2. V1 stapedial first gives off a branch to the dura of the anterior cranial fossa. Then, having traversed the superior orbital fissure, it gives off three branches, each which supplies structures both within the orbit and outside of the orbit. Supratrochlear (frontal, nasociliary) and its branches supply zones 13-12 composed of the ethmoid complex, nasal envelope, and medial forehead between the eyebrows. Supraorbital supplies zones 11-10 consisting of the orbital roof, upper eyelid, and lateral forehead defined by the eyebrows. Lacrimal supplies zone 9 which includes alisphenoid, lacrimal gland, and then lateral corner of the upper eyelid.

Like fashion to V1, V2 stapedial also gives off an initial branch to the dura of the middle and anterior cranial fossa. It then gives off StV2 anterior branch of middle meningeal which accesses the lacrimal artery within the orbit via an aperture in the alisphenoid (greater wing), the cranio-orbital foramen. This connection is referred to by various names, the most common being the recurrent meningeal artery. In many cases, the connection disintegrates, leaving lacrimal based on StV1 but the implications for the lacrimal gland are several. Its innervation is complex but its parasympathetic supply from VII relate to a genetic origin of the stapedial system from the 2nd arch.

The extracranial division of stapedial, MMA, gives off branches to the maxillary complex and palate all of which are V2-induced. Thus, the arteries supplying the two fields of zygoma, jugal, and postorbital arise in the pterygopalatine fossa. Zygomaticofacial and zygomaticotemporal supply Tessier zones 7 and 8. Greater sphenoid wing originally arose as the epipterygoid bone, part of the ancient palatoquadrate cartilage from which maxilla evolved. Epipterygoid is an r2 neural crest bone that functioned as part of the support system between palate and maxilla. As such, it is logical that the blood supply for AS should come from the extracranial stapedial system. Additional support for alisphenoid comes from temporalis muscle through anterior deep temporal branch of the external carotid component of MMA. In summary, Tessier zone 9 is complex, supplied by the confluence of three distinct systems.

To complete our picture, V3 stapedial supplies two functionally related zones. Inferior alveolar supplies the dental units and the ramus whereas anterior tympanic refers backward to supply the eardrum, malleus and incus. In so doing, these reflect the complex paleohistory of the mandibular bone complex in which its proximal components such as articular were brought backward into the skull as structures of hearing.

The structure of the lacrimal gland is complex and has provocative implications. Its epithelial components, the ductules, represent invaginations of r1 ectoderm associated with the development of the upper eyelids. General sensory afferents from the gland are carried by V1. Zone 9 of the orbit, which is inhabited by lacrimal gland, is constructed with r2 neural crest. V2 ascending from the pterygopalatine fossa as zygomatic nerve transports parasympathetic motor efferent fibers from the facial nucleus. Thus, the parenchyma of the lacrimal gland arises from r2 neural crest as well. If so, this gives rise to a single unifying hypothesis regarding the origin of salivary glands, all of which arise from either r2 or r3 neural crest. The penetration of each gland by ductal epithelium occurs by physical proximity. Common affectation of lacrimal and salivary glands as is seen Sjögren's syndrome therefore has a common embryological basis.

  Hard Tissues of the Palate: the Platform Top

The position of the soft palate in space is determined by the bony platform to which it is attached: (1) directly by a horizontal plate of the palatine bone (PlH) or (2) indirectly by the palatal shelf of the maxilla (MxP). PlH is supplied/programmed by a single neurovascular axis, the lesser palatine; hence, it is unilaminar. In contrast, MxP is a bilaminar structure. It has a nasal program of a bony lamina in continuity with the inferior turbinate and inferolateral nasal wall. The oral lamina of MxP is an extension of the lingual wall of the maxillary alveolus. Normally, the two laminae are fused, but on occasion, a sinus can be found and ectopic teeth may be present. We shall have more on this fascinating subject anon.

All pharyngeal arch bones are neural crest derivatives. The sensory innervation to the maxillary complex is V2, the nucleus of which resides in the second rhombomere, r2. V2 sends branches to all the developmental fields of the maxillary complex. These are accompanied by vascular pedicles that arising from the pterygopalatine fossa – the sensory nerves program the arteries. Defects within this r2 neural crest population – in terms of total cell volume, cellular function, or blood supply – can result in bones that are misshapen, small or even absent.

Key concept: Each bone field is supplied by a specific neurovascular pedicle. Deficiency states of a bone field occur in a distal-to-proximal gradient backward along the neurovascular axis.

The best model is one in which membranous bone develops in response to a predetermined epithelial program which determines its size and shape. Bone development takes place along its neurovascular axis according to a strict spatial-temporal sequence. Failure of the axis results in a gradient of deficiency that runs from distal-to-proximal. In the premaxilla, for example, the medial incisor field develops before the lateral incisor field or, later, the frontal process field making up the internal piriform fossa. Thus, a defect of the medial nasopalatine axis will leave a smaller or absent frontal process, with all the developmental consequences for the production of the cleft lip nasal deformity. We now turn our attention to the embryology of the palatine bone.

Posterior hard palate: Palatine bone

The palatine bone (Pl) develops in membrane from r2 neural crest. The epithelial “program” determining the size and shape of the bone is provided by the r2 nasal and r2 oral mucosa. Descending palatine artery provides its blood supply. This unusual bone plays a key role in connecting the nasal wall, maxilla, and palate with the orbit. It forms the floor of the orbit, inferolateral wall of the nasal cavity, and posterior 1/4 of the hard palate. Its characteristic L-shape results from the intersection of two plates, horizontal and perpendicular, at a slightly acute 80–85° angle. As we can see, this geometry will have surgical implications for cleft palate repair. It also bears three significant processes.

Components of the palatine bone [Figure 17] and [Figure 18]
Figure 17: Palatine bone Horizontal plate develops medial-lateral and anterior-posterior: PNS is final field Attachments: aponeurosis, (all) uvulus (medial), palatopharyngeus (lateral)

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Figure 18: Hard palate is bilaminar: 2 neuroangiosomes Nasal lamina = lateral sphenopalatine Oral lamina = greater palatine Marrow space, potentially tooth-bearing

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Perpendicular plate

Perpendicular plate is a thin lamina with medial and lateral sides plus four borders. The medial side is scooped-out, forming the posterior part of inferior meatus. Just above that, a transverse ridge, the conchal crest, articulated with the palatine process of inferior turbinate higher up, a second transverse ridge, the ethmoid crest, provides and articulation for middle turbinate. Tucked between the two crests is the middle meatus. Still higher up, above ethmoid crest, is a third depression, for superior meatus. The lateral side is rough and irregular; it articulates with maxilla. Along its posterior aspect, a well-chiseled vertical greater palatine groove marks where the maxilla and perpendicular plate enclose the neurovascular bundle. The anterior border is punctuated by a forward projection, the maxillary process, at the same level as the conchal crest. The maxillary process forms the posterior wall of the medial maxillary sinus; it articulates with Inferior turbinate. The rough posterior border articulates with the r1 medial pterygoid plate. This expands into the pyramidal process into which medial pterygoid is inserted. Superior border contains a forward-facing orbital process and a backward-directed sphenoidal process. Separating the two processes is the sphenoid notch that, by articulating with sphenoid, forms the sphenopalatine foramen, an all-important landmark because it communicates between the pterygopalatine fossa and the posterior nasal cavity. It transmits the sphenopalatine neurovascular pedicle and the posterior superior nasal nerves into the nasal cavity.

Horizontal plate

The position of the horizontal plate is space is determined by that of the horizontal plate of the maxilla (MxP). If MxP is reduced in length (its AP dimensions), the horizontal plate of an otherwise normal palatine will likewise be dragged anteriorly. The nasal surface is smooth and concave. The oral surface is rough. It bears near the midline a transverse elevation, the palatine crest, which serves as an attachment for the aponeurosis of tensor veli palatini. The anterior border is irregular, forming a rough articulation with the accessory palatine bone. The posterior border provides attachment for the palatine aponeurosis. The lateral border forms an acute angle (80–85°) with the perpendicular plate. Two bony prominences project from the fused medial borders. Musculus uvulae inserts into posterior nasal spine. The nasal crest articulates with vomer.

LPA is the principle blood supply to horizontal plate. The mesenchyme to form the horizontal plate is deposited from lateral to medial and from anterior to posterior to form a rectangle. If mesenchymal deficiency occurs, it will reduce the horizontal plate in the opposite directions, creating a triangle based laterally and anteriorly.

The pyramidal process projects backward from the intersection between horizontal and perpendicular plates. Its posterior surface insinuates itself into a crevice between the medial and lateral pterygoid plates. An important landmark is the lateral surface is a roughened zone along its anterior aspect. This will abut against the tuberosity of the alveolus. The lesser palatine foramen is located at the intersection between pyramidal process and horizontal plate. The greater palatine canal is formed by the bilaminar confluence of pyramidal process (lateral) against the perpendicular plate (medial). It transmits the descending palatine artery.

The orbital process contains an air cell. It has two nonarticulatory and three articulatory surfaces. Superior surface form the posterior orbital floor. Lateral surface contributes to inferior orbital fissure. Anterior surface articulates with maxilla. Posterior surface contains the opening of the air sinus, which can communicate with the sphenoid sinus. Medial surface articulates with ethmoid labyrinth. Sometimes, this can serves as alternative escape route for the palatine air sinus, which communicates with the posterior ethmoid cells.

The sphenoidal process has three surfaces and three borders. Superior surface connects with medial pterygoid plate and abuts against the sphenoid concha. Medial surface pokes its tiny nose into the nasal cavity. Lateral surface connects with lateral pterygoid plate. Anterior border forms the posterior margin of the sphenopalatine foramen. The medial border of sphenoid process, by virtue of its proximity to the sphenoid bulla, can reach as far as the ipsilateral ala of the vomer where it receives the sphenoid rostrum. Not to be left out, medial pterygoid plate has a vaginal process that articulates with posterior border.

Development of the palatine bone

Ossification is observed immediately after the embryonic period at the 8th week of fetal life (stage 23, 20 weeks). The epicenter is between the horizontal plate and the perpendicular plate. It spreads out in three directions: (1) medially directed horizontal plate and (2) posteriorly directed pyramidal process develop first, followed 2 weeks later by (3) superiorly directed perpendicular plate. All three of these axes are independent.

At birth, the horizontal and perpendicular plates are equal in size. Over time, increasing depth of the nasal chamber increases the relative size of perpendicular plate. As the perpendicular plate extends upward, it encounters the preexisting sphenopalatine neurovascular axis. The osseous mesenchyme splits around the pedicle. The anterior orbital and posterior sphenoid processes results. In point of fact, the complexity of the various processes of palatine bone stems from its relatively insertion into previously established bone fields such as sphenoid, ethmoid, and maxilla. The palatine mesenchyme just has to fit in where it can.

As the horizontal plate develops, new mesenchyme is deposited in a medial-to-lateral and anterior-to-posterior direction. Thus, the newest, most vulnerable zone of the horizontal shelf is medial and posterior, i.e., the posterior nasal spine.

Clinical correlations

The mesenchymal masses of perpendicular plate and horizontal plate are developmentally independent. This reflected in robust blood supply to perpendicular plate from descending palatine artery. Two or three foramina in the perpendicular plate allow for exit of small neurovascular pedicles to supply the mucosa posterior it. These anastomose with the blood supply to the tonsil. As descending palatine artery (DPA) nears its junction with the horizontal plate, it splits into two branches. Lesser palatine artery (LPA) is given off as multiple branches before DPA exits as the greater palatine artery (GPA) to the maxillary hard palate. LPA supplies the oral structures of the soft palate and it perforates through two small foramina to supply the nasal surface as well. Thus, deficiency of the vascular axis to horizontal plate can occur independent of the more proximal supply to perpendicular plate or to its other distal terminus, the greater palatine field.

Developmental wipeout of the entire descending palatine axis is structurally incompatible with life. Mesenchymal deficiency can occur in the distal horizontal plate of palatine, in the distal maxillary hard palate, or in both zones. Both neuroangiosomes demonstrate the pattern of tissue loss, according to their developmental gradients. Lesser palatine insufficiency occurs first at its most distal and posterior territory, the posterior nasal spine. Progressive LPA deficiency works its way laterally and anteriorly. Greater palatine insufficiency occurs first at its most distal and posterior territory. The newest branches of GPA, those supplying the medial edge of the posterior palatal shelf, are the most vulnerable. Thus, if failure of bone mesenchyme occurs, it follows a gradient of severity, from medial-to-lateral and from posterior-to-anterior, all the way forward to the incisive foramen. This explains the clefting pattern of the secondary hard palate.

Anterior hard palate: Maxilla [Figure 19],[Figure 20],[Figure 21],[Figure 22]
Figure 19: Mandible: bilaminar support for dental lamina Eusthenopteron and Paleoherpeton: multiple dermal bone fields that are absorbed but retain programming for differentiation of dentition

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Figure 20: Maxilla development Medial wall: lateral sphenopalatine, greater palatine Lateral wall: superior alveolar - anterior and posterior

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Figure 21: Maxilla and mandible are bilaminar support expansion Mucosa enters maxillary cavity: (1) prevents fusion, (2) permits expansion Maxilla has low-stress muscle environment Medial and posterior walls fixed to cranial base > expansion is lateral and anterior under orbit Mandible surrounded by high-stress muscle environment – no expansion – marrow space

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Figure 22: Vetebrate cladogram jawless jawed with anterior mouth - chondrichthyes / cartilage fishes jawed with ventral mouth - teleostomes (true mouth) - osteoichthyes = bony fishes - tetrapods

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Components of the maxillary complex

The best way to understand the structure of the maxilla is to compare it with that of the mandible. Although they appear very different, their functions are identical, as it is their basic design. Both are bilaminar and consist of multiple bone fields assembled into two functional components: A housing for dental units and a support structure that articulates with the skull. The upper jaw was not always fixed to the cranial base. In early bony fishes, the tooth-bearing palatoquadrate cartilage (the precursor of the maxilla) had a moveable articulation with the chondrocranium. The mandible of choanate fishes and early tetrapods consists of a tooth-bearing dentary bone supported from below by two splenial bones and a more posterior articular bone that constituted the primitive connection to the skull. These structures have all fused (Herring's law) to make a unitary bone, but both sides of the body and mandible are perfused by distinct arteries supplying the attached muscles which bear witness to its more complex past. The potential space between the laminae of the dentary bone contains the dental units while that of the supportive lever arm is filled with marrow.

On the opposite side of the bite plane, the original maxillary bone is analogous to the dentary. Its support structure is fixed, but bilaminar forming a six-sided box, in the center of which is the maxillary sinus. The medial wall of the box (the lateral wall of the nose) is discontinuous. It has a large hole in the center that is partially covered over by the uncinate process of the ethmoid and the inferior turbinate. This is a critical point because the nasal epithelium gains access to the interface between the maxillary laminae and prevents them from fusing. Thus, as growth of the maxillary complex takes place, this potential space expands to form the maxillary sinus. Because the medial lamina of the maxilla is fixed to the cranial base by the ethmoid and palatine bones, expansion of the maxillary sinus must occur laterally, projecting outward beneath the orbit.

The maxillary hard palate develops in membrane from r2 neural crest. The palatal shelf of the maxilla is an outgrowth from the junction between the internal maxillary lamina and the maxillary alveolus (derivative of the ancient palatoquadrate). Its blood supply reflects these two distinct sources. Lateral nasopalatine artery from the internal lamina supplies the nasal side. Greater palatine artery from the alveolus provides its blood supply on the oral side The interface between these two neurovascular zones, between the lingual alveolar wall below and the inferior turbinate above, is a biologic “signal” that defines the zone from which the palatal shelf will emerge. As we can see, a similar interface zone exists posteriorly that signals the emergence of the soft palate envelope.

Ossification of the maxilla occurs in the same progression with all neuroangiosomes. Documentation exists for anterior superior alveolar and greater palatine. Gradient of bone formation is the same as for the palatine bone: anterior to posterior and medial to lateral.

The palatal process of the maxilla is bilaminar

Alveolar bone in both maxilla and mandible is a bilaminar structure with dental units housed between distinct buccolabial and lingual bones. The buccal wall of the alveolus belongs to the maxilla per se and is supplied by the medial and lateral branches of the infraorbital artery, better named the anterior superior alveolar artery (ASA), and by the posterior superior alveolar artery. The lingual wall of the alveolus and the palatal shelf is a single functional unit supplied by greater palatine branch of the descending palatine artery. These structures appear to be a single unit although, based on comparative anatomy, the shelf of the hard palate may be the evolutionary descendent of a separate prepalatine bone.

Earlier in the evolution, the palate consisted of multiple tooth-bearing bones. Over the course of time, the number of bones is reduced and simplified, a phenomenon known as Herring's law. Like many calvarial bones, the maxillary shelf (prepalatine) is bilaminar because it has two sources of programming. The distinct color difference between the oral mucoperiosteum and the nasal periosteum showed that its two neurovascular axes are biologically different.

For many readers, the concept of the hard palate shelf as a bilaminar structure may come as a shock, but comparison of the maxillary alveolus with the mandibular alveolus is most reassuring. Both structures develop within the first pharyngeal arch in direct opposition to each other (thereby explaining occlusion). Both structures are tooth bearing – recall that teeth are always housed in biliaminar bones. Both structures, in the evolutionary record, are composed of distinct bone fields. Both structures have distinct arterial supplies to their labiobuccal versus lingual walls, and both have distinct arterial supply to the dental units. The posterior superior alveolar artery is the primary supply to the teeth. It is the analog of the inferior alveolar artery of the mandible. Thus, the functional design of the maxilla is virtually the same as that of the mandible. The structures have a different shape and different names, but the functional significance remains the same.

There are four lines of evidence for the bilaminar nature of the palatal shelf. First, like other membranous bones such as frontal bone, it has a dual blood supply (and a dual source of programming). Second, the palatal shelf contains marrow (characteristic of flat bones of the skull). Third, formation of a sinus within the palatal shelf has been documented in primates. Fourth, this bone can be tooth bearing. This is not surprising. Primitive vertebrates had multiple rows of teeth (Bemis, Benton).

The hard palate makes its first appearance in crocodiles. It is unclear whether it represents an evolutionary innovation that buds off from the medial wall of alveolus or whether it is the manifestation of the genetic reappearance of a previous ancient palatal bone, i.e., the prepalatine that has become fused with the maxilla.

Development of the maxillary hard palate

Ossification of the maxillary hard palate starts at the incisive foramen and progressively sweeps backward as more mesenchyme to be added on from proximal to distal (anterior to posterior) and from medial to lateral. The additional mesenchyme demands that new arterioles sprout off from the main axis. For this reason, clefts of the secondary hard palate begin posteriorly and medially. As the mesenchymal deficiency worsens, the cleft extends forward until it terminates at the incisive foramen. In exactly the same way, the neurovascular axis to the lingual lamina of the premaxilla adds mesenchyme from mesial to distal, that is, from proximal to distal. On the buccolabial side, the same pattern is seen. The medial branch of anterior superior alveolar ossifies and sustains eruption before the lateral branch of ASAA.

Clinical correlations

Maxillary palate defects versus palatine bone defects - Which comes first?

Under almost all circumstances, clefts of the maxillary hard palate occur in the present of a defect in palatine bone synthesis. This posterior-to-anterior gradient is based on the developmental sequence of the descending palatine artery. DPA supplies the perpendicular plate of the palatine bone. Having reviewed the various process of the palatine bone, it is clear that a knockout of DPA would affect multiple bone fields of the maxillary complex and the development of the orbit itself. Such a situation would be incompatible with life. However, having synthesized the perpendicular plate, the DPA produces two terminal branches, lesser palatine to the horizontal plate (Plh) and greater palatine to the maxillary hard palate (Mxp). Although these neurovascular axes are developmentally independent, we know from the ossification sequence that horizontal plate is constructed on the prior template of the maxillary hard palate. Thus, clefts of MxP result in clefts of Plh, but isolated clefts of Plh do not affect MxP.

Isolated defective synthesis of the horizontal plate (maxilla normal) is always accompanied by abnormal soft palate anatomy because LPA supplies both the bone and the tensor aponeurosis.

In the submucous cleft, a palpable notch may extend forward into the posterior maxillary shelf. The presence or absence of soft tissue clefting depends strictly on how closely the bone fields approximate one another in the midline. If the critical contact distance is not exceeded, soft tissue closure will take place.

What about the situation of a normal palatine field constructed on an intact, but foreshortened maxilla? In this case, the soft palate is completely normal but displaced forward. Such a situation can produce non-cleft velopharyngeal incompetence (VPI) simply by virtue of an expanded retropalatine space which the soft palate cannot adequately close.

Dental eruption sequence

Dental eruption can be rationalized based on a vascular model in which two distinct axes supply neural crest ectomesenchyme with a subsequent remodeling into the final adult configuration. As a clarification, the infraorbital artery and Anterior superior alveolar artery (ASAA) are one and the same. In early development, the medial branch of ASA supplies a potential lateral incisor and the canine, whereas lateral branch of ASA supplies the primary molars. Dental development spreads out from mesial to distal from the ASA. Thus, medial branch of ASA contributes to an ectopic lateral incisor (9–13 mo); it then supplies the primary canine (16–22 mo). Lateral branch of ASA supplies successively the first primary molar (13–19 mo) and subsequently the second primary molar (25–33 mo).

The adult eruption sequence is analogous: lateral incisor - aberrant (8–9 years) followed by canine (11–12 years)/1st premolar (10–11 years) and 2nd premolar (10–12 years). Posterior superior alveolar artery makes its debut at age 6 by with the first permanent molar. As bone is added on posteriorly to the alveolus, the remaining adult molars develop, each with its assigned branch of Posterior superior alveolar artery (PSAA). The 2nd and 3rd permanent molars appear, respectively, at 11–13 years and 17–21 years. In summary, one can easily rationalize the sequence of dental eruption by knowing two principles: (1) Maturation sequence of the three vascular branches – medial/lateral ASAA, PSAA) is mesial to distal and (2) medial ASAA can potentially form an “ectopic” incisor at the same time as the premaxilla forms its own version of the lateral incisor.

The final configuration of the arterial supply to the teeth can be quite different. Within the dental space of the alveolus, the arterial components of ASAA can unite to form a single vascular arcade with PSA. If the vertical contributions of ASAA to the dental units become attenuated, the final anatomy appears as if all the teeth were originally supplied by PSAA. In point of fact, this is just an artifact of vascular remodeling.

Anterior hard palate: Vomer [24],[25],[26],[27]

The vomer is quadrilateral bone that develops in membrane from r-2 neural crest>. It represents the fusion of paired embryonic vomerine processes. Its shape is programmed from r2 oral ectoderm. Vomer maintains a total of ten articulations with five pairs of bones. Sphenoid and ethmoid are derivatives of r1 midbrain neural crest. Palatine, maxilla, and premaxilla all derivatives of r2 hindbrain neural crest.

Posteriorly it has a deep groove which receives the (paired and fused) vaginal processes of the r1 sphenoid. Paired alar processes flare outward, forming the letter “T.” These articulate posteriorly with the medial pterygoid plates and anteriorly with the sphenoid processes of the r2 palatine bones.

The superior border of vomer receives the fused perpendicular plates of the ethmoid complex. The bones are demarcated by a deep nasopalatine groove which transports the neurovascular axis of the same name. The inferior border of septum, also of r1 midbrain neural crest derivation, is in direct contact with the anterior most upper border of the vomer.

The anterior border of vomer articulates with premaxilla and with septum. A collagenous band, the premaxillary-vomer ligament, has been considered by some to be an “engine of growth.” In reality, it is just a means to share force vectors as each of the membranous structures grows autonomously.

The inferior border of vomer articulates with the shelves of the maxilla and palatine bones. They form a U-shaped nasal crest into which the vomer is situated.

The vomer contains two ossification centers one for each lamina. Although they fuse to what is apparently a single bone, proof of previous bilaterality is seen in the bilateral grooves for nasopalatine nerves, the upper midline groove receiving the ethmoid and vomer, and the presence of flared alar processes. Ossification follows a pattern which traces the trajectory of the nasopalatine axis. Bone is deposited beginning with the penetration of the NP axis through the foramen incisivum. Much like spilling a bucket of paint, mesenchyme for the medial nasopalatine axis “fills out” the premaxilla in three vectors: forward, outward, and downward for the teeth and hence upward for the frontal process. In like fashion, the vomer is synthesized backward and downward. In shape, the vomer can be likened to a scimitar, with a narrow handle hinged at the incisive foramen and a broad blade projecting backward. As the vomer grows, the inferior edge of the scimitar descends, knife-like, into the nasal cavity.

Clinical correlations

Isolated secondary cleft palate due to vomer field defect

Closure of the hard palate depends on the fusion of the shelves of the palatine and maxillary bones with the vomer. This, in turn, requires that the vomer be physically descended into the palatal plane. The critical contact distance between the two bone fields must be achieved. For this to happen, the vomer must descend into the palatal planed. If the vomer field is insufficient, loss of mesenchyme will be seen at its posterior and inferior border, it will be out of the palatal plane, the critical contact distance will be exceeded, fusion to the shelves will be impossible, and a cleft will appear.

The fusion process itself (Zhang) proceeds through epithelial dissolution. Sonic hedgehog in the epithelium (which maintains its integrity) is inhibited by soluble bone morphogenetic protein (BMP)-4 (a by-product of membranous bone synthesis). Reduction of mesenchymal bone mass means a quantitative reduction in the production of BMP-4. The intact epithelial surface will not disintegrate, no fusion is possible, and a “cleft” occurs.[28],[29]

  Role of the Septovomerine Articulation in Septoplasty Top

Correction of septal deviation is a common surgical procedure requiring elevation of the mucoperichondrium surrounding the septum. This maneuver presents a technical problem. As one proceeds from above, inferiorly and posteriorly, tears in the mucoperiosteum can occur along the septovomerine junction. This is due to the confluence of periosteum of the two vomerine lamellae, forming a U-shaped “cradle” that receives the septum. Within this bony trough, a fusion takes place between the mucoperichondrium surrounding the septum and the periosteum of the bone. This confluence of tissue, if not dissected properly, can result in a tear.

On the other hand, when a vomer flap is elevated from below, as in a unilateral cleft lip and palate, an incision is made at the boundary between vomer and maxillary shelf. The resultant mucoperiosteal plane and submucoperichondrial plane are confluent. Exposure of the septum from below is fast, easy, and atraumatic. Why the discrepancy? In this scenario, at site of confluence, the “lip” of vomer ipsilateral on the cleft side is missing. The U-shaped cup of vomer bones that receives the septum is disrupted on the cleft side. Entry into the subperichondrial plane is uncomplicated.

  Appendix: Evolution of the Palate Top

Recommended reading: Bemis, Benton, Kardong [30],[31],[32]

The emergence of the hard palate: A timeline [Figure 23]
Figure 23: Choanate fish – proximal to tetrapod: Eustheopteron Palatoquadrate cartilage: (1) anterior part covered by dermal bone – maxilla (2) posterior part ossifies to palatal series (metapterygoid/epipterygoid) and quadrate Meckel's cartilage (mandible) covered by dermal bones

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Elements of the facial skeleton first appeared about 500 million years ago with jawless fishes having seven or more gill arches. Chondrichthyan fishes had the first cartilaginous skull and remodeled the first two gill arches into upper and lower jaws. Shortly thereafter bony fishes, the osteichthyes developed neural crest dermal bones which were used to ensheath the jaw cartilages and the brain. They then diverged into two lines, based on the support system for their fins. Actinopterygians, the ray-finned fishes, having bony struts controlled by muscles inside the body cavity, became wildly successful. The mammalian line traces back to fossil sarcopterygian fishes, named for their fleshy fins with muscles outside the body cavity. These gave rise to the rhipidistians, or lungfishes, a specialization of which, the choanata, developed a mechanism to breathe air into the oral cavity via the nose. From the choanate fishes, tetrapods emerged on land with critical innovations. Having inherited choanae and lungs from the rhipidistians, tetrapods were air-breathers. The pectoral girdle was completely free from the skull, permitting the evolution of a neck and mobile head of great advantage for capturing prey. The spinal column was strengthened by weight-bearing articulations, zygapophyses. Digit-bearing limbs appeared, with a baseline of six to eight. The next great subdivision arose with the invention of amniotic membranes that permitted birth to take place on land, avoiding the aquatic phase of development. Primitive tetrapods developed into reptiliomorphs that bifurcated into anamniota (amphibians) and amniota (reptiliomorphs – the future reptiles, birds, and mammals). In the latter clade, the digital formula stabilized at five. Changes in predation associated with specialized chewing muscles are manifested to flanges of the sphenoid bone, the modern day pterygoid plates.

Reptiliomorphs again bifurcated into the line producing true reptiles and birds and the pelycosaurs leading to therapsids and then mammals. The descendent of reptiliomorphs are classified by the fenestration pattern of the temporal fossa. These represent attachments for chewing muscles and give information about control of the mandible. The diapsids have both an upper and a lower fenestra behind the postorbital and squamosal bones and are represented by reptiles and birds. All mammals are synapsids, having a single temporal fenestra low on the skull and bounded by a bony bar (the future zygomatic arch) running postorbital (the precursor of the upper half of zygoma) and the squamosal bones. Further classification is based on changes in dentition, mastication, and locomotion.

The skull of the basal synapsid dimetrodon shows many changes related to a carnivorous lifestyle with powerful jaw muscles. Many bones changed names. The limbs remained sprawled out, with the femurs being horizontal. Members of the next transition, Therapsida developed large canines. Their limbs were now directly below the body, making them agile runners and effective predators. A subsequent subgroup of therapsids, the cynodonts, is proximal to mammals. The dermal bones that ensheath the cynodont mandible meld together for the first time to form a “single” unitary dentary bone. Former bone fields were either suppressed (remaining as genetic entities) or displaced into the temporal region to form the ear bones. Cynodonts developed postcanine teeth with cusps for grinding. Part of temporalis gave rise to temporalis attached to the arch. The presence of a well-developed palate leads one to the conclusion that the cynodonts were endothermic.

  Bone of the Oral Cavity a Portrait in Broad Brushstrokes Top

The skull of earliest craniates (jawless fishes) consisted of a hypaxial splanchnocranium, referring to the support structures of the gill arches (up to 9 in all) and an epaxial chondrocranium at the brain. Some species were able to ossify their endoskeleton including the skull base. They also produced an exoskeleton in the form of a head shield consisting of dermal bones, the dermatocranium. The original function of splanchnocranium was strictly respiratory, but, with advent of the chondrichthyans, it became an essential tool for feeding as the first two arches morphed into a dorsal palatoquadrate cartilage and a ventral mandibular cartilage. Bone-forming capability was secondarily lost in the cartilaginous fishes but was regained in the osteichthyes.

In the bony fishes, ossification returned with the changes in the skull. The posterior part of both palatoquadrate and mandibular cartilages ossified into two opposing bones, quadrate and articular. These form the jaw joints in all vertebrates except mammals (which have a temporomandibular joint). At the same time, these fishes regained the ability to form a dermatocranium. Multiple dermal bones make up the roof of the skull and ensheath the jaws. At the time of the choanate fishes such as Eusthenopteron, very close to the emergence of tetrapods, these dermal bones cause the face to be elongated for better feeding. Multiple bones cover the mandible – although these “disappear” in mammals, the genetic “ideas” that programmed them may explain regional differences in differentiation of teeth. Premaxilla and maxilla are now present.

A palatal series of bones is present with metapterygoid visible laterally in the area anterior to the jaw joint. On intraoral view, the pretetrapod palate consists of an external arch of premaxilla and maxilla within which are palatine and ectopterygoid (both tooth bearing), pterygoid, and parasphenoid. Paired vomers are in contact with the palatine and pterygoid bones. A vertical intracranial joint at the center of the chondrocranium permitted the mobility of the upper jaw and front of the skull [Figure 23] and [Figure 24].
Figure 24: Choanate fish: Eusthenopteron Hard palate: palatine / ectopterygoid / pterygoid 1. Epipterygoid dorsal to pterygoid 2. Epipterygoid suspended from the skull Vomer, palatine, and ectopterygoid are tooth-bearing, premaxilla and maxilla are just dermal Parasphenoid is short, covers presphenoid only

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We now turn our attention to tetrapods beginning with the basal paleoherpeton. Choanae appear in the mouth on either side of premaxillae. These are likely preserved today as the nasopalatine canals. Just behind the premaxillae, the vomers no longer have teeth. Lying above the pterygoids (but not attached), epipterygoids represent a persistent mobile articulation with the brain case. The interpterygoid vacuities between pterygoids and chondrocranium represent the plane movement. This kinetic skull was not as well adapted to predation [Figure 25] and [Figure 26].
Figure 25: Basal tetrapod (parasagittal view): Paleoherpeton Epipterygoid (future alisphenoid) - internalized by postorbital / jugal and squamosal - basal articulation with pterygoid

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Figure 26: Palatal bones in contact with skull base but mobile Interpterygoid vacuity: potential space between palate and skull base Choanae open into anterior mouth – no separate nasal passage Vomer no longer tooth-bearing, premaxilla becomes tooth bearing

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The lineage of mammals began with the synapsid skull and passed through the sailed reptiles. Dimetrodon demonstrates anterior choanae. The primary palate lies dorsal, just beneath the skull base. There are no nasal cavities. Therapsids became more mammal-like with changes in limb positioning and in the cranial skeleton. The advanced therapsid line, the cynodontids (just proximal to true mammals), represented by Probainognathus, are the immediate precursors of mammals. They had powerful chewing muscles, requiring a fixed, akinetic skull. It became anchored to the skull, allowing for greater force generation. The epipterygoid (future alisphenoid) unites medially with the remainder of the sphenoid and inferiorly to pterygoid. The latter bone shrinks down to wing-like pterygoid processes projecting downward from sphenoid. Of greatest importance is the development nasal cavities. These come about from two processes. The choanae shift posteriorly and the rostral primary hard palate shrinks backward (and will ultimately be eliminated). Parasphenoid becomes incorporated upward into basisphenoid. In its place, the vomers move to the midline and receive the midline septum, which makes its debut at this time. The floor of the cranial cavity becomes the roof of the nasal cavity. The maxillae and palatine bones develop now develop medial shelves to form the floor of the nasal cavity. The shelves fuse to the vomer. The nasal choanae are now retro-positioned at the margin of the hard palate. Fossil evidence for a soft palate appears at this time, with its attachment sites on the pterygoid processes. The palatine bone ceases to be toth-bearing [Figure 26], [Figure 27], [Figure 28], [Figure 29], [Figure 30].
Figure 27: Transition of hard palate – pre-mammal Horizontal shelves not yet produced by maxillae and palatine bones Epipterygoid articulates with pterygoid Post orbital moves forward and temporal fenestra opens Zygomatic arch defined Parasphenoid (NC) fuses forward of basisphenoid (PAM) into presphenoid (NC)

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Figure 28: Bone fates of mammalian palate Parasphenoid absorbed into presphenoid Epipterygoid = alsiphenoid Ectopterygoid = lateral pterygoid plate of sphenoid Pterygoid = medial pterygoid plate of sphenoid

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Figure 29: Primary vs. secondary hard palate

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Figure 30: Transition of modern palate: cynodonts to mammals Incorporation of ear bones pathognomonic for mammalia

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  Appendix: Functional Anatomy of Cranial Nerves to the Soft Palate Top

Many biology texts refer to r8 as the terminal rhombomere, lumping together a wide variety of neuroanatomic relationships. Extensive work by puelles breaks up r8 into 4 pseudorhombomeres because of individual relationships between the medullary nuclei and extraneural structures.[12] For purposes of simplification, and because Puelles' work gives a more accurate description, we use his terminology in this text.

Apart from the oculomotor nerves (III, IV, and VI) and the hypoglossal nerve to the tongue (XII) all cranial nerves are mixed, that is they contain two or more functional components. In the rhombencephalon, the various nuclei contributing to each cranial nerve are classified into six longitudinal columns, each one with a specific function. The motor columns (efferent output from the CNS) are in the basal (medial) hindbrain. Sensory columns (afferent into the CNS) are lateral. The columns are organized in mirror-image manner according to their function. For those readers wishing a quick review (or for those with nothing better to do with their time), the anatomy of the columns from medial to lateral is as follows.

Motor columns of the brainstem (basal plate)

The somatic efferent column (general somatic efferent [GSE]) is the most medial. It contains the nuclei serving the oculomotor muscles and tongue. The derivatives are as follows: From Sm1 (inferior rectus, inferior oblique, and medial rectus), Sm2 (superior rectus, superior oblique), and Sm5 (lateral rectus - some species have a 2nd component from Sm6). The tongue arises from occipital somites (S2–S4); these also give rise to sternocleidomastoid and trapezius. This column extends cranially into the midbrain/mesencephalon where we find cranial nerve nuclei III and IV.

The visceral efferent column (general visceral efferent [GVE]) is located lateral to GSE. GVE is a misnomer. It is not strictly visceral because it is motor for the glands of the eye and mouth. These nuclei belong to the parasympathetic autonomic nervous system. They supply highly localized ganglia (relay stations) with preganglionic parasympathetic nervous system (PANS) motor fibers for a wide variety of functions, such as pupillary control, salivation, bronchoconstriction, cardioinhibition, and of peristaltic activity of the intestine. The midbrain component of this column contains Edinger-Westphal nucleus of III. Superior salivatory nucleus of VII in register with r4–r5 supplies the lacrimal gland and salivary glands. Inferior salivatory nucleus of IX in register with r6–r7 supplies the parotid gland. The caudal continuation of GVE is the dorsal nucleus of X in register with r8–r11. It supplies all organs of the thorax and abdomen. Thus, the motor component of cranial nerve X does not supply striated muscle.

Hence, why is vagus cited as the motor nerve of the soft palate?

The pharyngeal arch (“branchial”) efferent column (special visceral efferent [SVE]) is the most lateral motor column. SVE is also a complete misnomer, as it contains nuclei for structures that are neither branchial nor special nor visceral. However, we use SVE anyway. Why the confusion?First off, striated craniofacial muscles originate from either somitomeres or the first 4 occipital somites, not from arches – myoblasts migrate into pharyngeal arches only secondarily. Second, only fishes with gills have branchial arches (branch signifying gills). All the rest of us land-dwelling tetrapods (throw in a few snakes) breathe air; thus, those embryonic structures formerly assigned to form gills now create the pharynx. Hence, the term pharyngeal arches. Third, the concept of “branchial” muscles was somehow assumed, by virtue of their location to relate to visceral functions, such as swallowing. These were considered “ventral” and therefore had to be LPM – this concept is now disproven. We now know that all craniofacial striated muscles originate from PAM. Having cleared up this mess, SVE nuclei supply striated muscles of pharyngeal arches 3–5, down to and including pharynx and larynx. Note that the muscles controlling head-versus-pectoral girdle (sternocleidomastoid and trapezius) are non-arch muscles arising from somites S1-S7. Their nerve, spinal accessory is a peripheral nerve incorporated into the head. Motor components of cranial nerves V, VII, IX, X, and the cranial portion of XI are all SVE. The nucleus ambiguus belongs to the SVE column.

In the upper cervical spinal cord (c1–c4), this situation is much simpler. There are no branchial arch muscles per se and therefore there is but a single somatic motor column.

Sensory columns of the brainstem (alar plate)

The general visceral afferent column receives parasympathetic input.

Special visceral afferent column, known as the nucleus of tractus solitarius, receives taste information via VII (anterior 2/3 tongue), IX (posterior 1/3 tongue), and X palate/pharynx. Taste fibers from the posterior 1/3 of the tongue and the soft palate ascend in the nucleus solitarius and synapse in its gustatory zone. Palate fibers most likely synapse at levels r6 and r7, whereas fibers from the tongue target those neuromeric levels that are in genetic register with the mesoderm and neural crest from which they originated, i.e., from r8-r11.

General somatic afferent column receives general sensory input (pain, temperature from the head. Nerve fibers travel as glossopharyngeal and vagus from the palate and pharynx the pharynx, and larynx to levels r6–r11.

Special somatic afferent column is dedicated balance and hearing. The vestibular nucleus is very extensive running from r5 to r11. The cochlear nucleus is localized lateral in register with r6–r7.

Clarifications regarding motor control of the soft palate

Palate muscles get their motor supply from r6 to r7 in nucleus ambiguus. The sensory distribution to the soft palate is IX are associated with both cranial nerves IX and X. However, recall that dorsal motor vagus is not motor to striated muscle. Nucleus ambiguus “chooses” to send efferent neurons to the palate via the vagal pharyngeal plexus. Thus, although textbooks say the only muscle of the 3rd arch is palatopharyngeus and it is supplied by IX, the reality is that all palate muscles get neurons from the 3rd arch zone of nucleus ambiguus, r6–r7. These simply travel to palate via sensory vagus of the pharyngeal plexus. The gag reflex is sensory to r6–r7 via glossopharyngeal and motor back to palate from r6 to r7 and to pharynx from r8 to r11 via the vagus [Figure 31].
Figure 31: Nucleus ambiguus: 3 motor zones Upper 1/3: r6-r7 to palate, upper and middle constrictor Middle 1/3: r8-r9 to external larynx, inferior constrictor Inferior 1/3: r10-r11 to internal larynx Don't code the soft palate as IX or X, just code it as r6-r7 XI extends from r8-c3: represents the lateral motor column and supplies ancient cucullaris muscle (SCM, trapezius)

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Cranial nerve XI, spinal accessory, runs from r8 down to c3. It is a modified peripheral nerve that innervates the nonbranchiomeric cucullaris muscle, the derivatives of which are sternocleidomastoid and trapezius. In fishes, cucullaris is an epaxial muscle that runs from a dermal bone series attached to the back of the skull (the future pectoral girdle) forward to the dorsal aspects of the branchial arches. In tetrapods, the pectoral girdle is detached from the skull and XI appears for the first time. The mammalian cucullaris arises from somites 1-7, therefore it has motor nuclei extending all the way from c1-c3 that encodes the clavicle forward to r8. For this reason some texts describe the (branchiomeric) soft palate muscles as under the control of XI but this impossible as XI belongs to an outboard, originally epaxial system [Figure 32].
Figure 32: Functional anatomy of cranial nerves YELLOW: eye muscles (Sm1-Sm3, Sm5) are not pharyngeal arch derivatives; tongue muscles come from somites 2-5 BROWN: pharyngeal arch muscles, V, VII, IX, X, XI upper 1/3 nucleus ambiguus = soft palate XI supplies NON-pharyngeal arch muscles (SCM, trapezius) and extends from r8 to c3

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A word about muscles: Epaxial versus hypaxial, visceral versus branchial

Neurons exiting the brainstem and spinal cord are either somatic efferent, somatic afferent, or mixed. They grow in two different directions as determined by gene signals, primarily the presence or absence of BMP-4.

Epaxial nerves supply structures dorsal to the neuraxis. These nerves are quite simple. Epaxial nerves may have contributions from more than one neuromere, but they travel as individual structures. This is because the migration routes of epaxial muscles are simple; they follow a strict spatiotemporal sequence. Muscles build up on one another, with mononeuromeric muscles before multineuromeric muscles (simple before complex) in cranio-caudal, ventro-dorsal, and medio-lateral order. This, in turn, is determined by the fact that such muscles insert into structures that maintain fixed relationships with respect to the body axis.

Hypaxial nerves supply structures ventral to the neuraxis. In the head and neck, these nerves can be quite complex with contributions from multiple functional columns. Hypaxial nerves can form plexuses, complex “switchyards” giving off branches of which have combinations of cell bodies. This is because the migration routes of myoblasts are complex. Although they follow the same spatiotemporal rules, they insert into appendicular structures, such as the upper limb, which, during development, undergo position changes with respect to the body axis. Structures residing in a fixed position within the body wall, such as intercostal muscles and diaphragm, are innervated by individual hypaxial nerves, not via plexuses.

Note for the uninterested: The term “visceral” is a misnomer when applied to cranial nerves; it really should be read as hypaxial. If we define the viscera as internal structures of arising from IM (genitourinary system), ventral LPM (cardiovascular system, gastrointestinal system), and those glands supplying endoderm or ectoderm, then the term viscera is OK. Obviously, the ciliary muscles have nothing to do with the viscera. Moreover, it is difficult to conceive of the larynx as viscera. We just have to keep it in mind that we are using the term viscera rather loosely. All pharyngeal arch structures are hypaxial to the neuraxis as are the cranial nerves that supply them. Pharyngeal arch for tetrapods is equivalent to branchial arch for gill-bearing fishes; both give rise to purely hypaxial structures.

Nerve supply to the soft palate and pharynx

Having defined our terms, let's review cranial nerves IX, X, XI, and XII in terms of their functional components:

Glossopharyngeal nerve (IX)

Somatic motor: None, no striated muscles from somites.

“Branchial” motor: Striated muscles of the 3rd arch arise from PAM of somitomere 7. Glossopharyngeal nerve per se supplies only one muscle from Sm7, palatopharyngeus. Instead, glossopharyngeal receives motor fibers from XI in the cranial nucleus ambiguus,(1). stylopharyngeus nerve and (2) communicating nerve to vagus conveys motor fibers from r6 to r7 to the soft palate very important for us.

Visceral motor: Tympanic nerve innervates the tympanic membrane; it carries PANS fibers from inferior salivatory nucleus to lesser petrosal nerve to the otic ganglion just above foramen ovale where they synapse to travel with V3 auriculotemporal nerve to parotid gland.

Visceral sensory: Carotid sinus nerve carries afferent baroreceptor input.

General sensory: Tonsillar nerve, lingual nerve, and pharyngeal plexus.

Special visceral sensory: Taste fibers from posterior 1/3 of tongue.

Vagus nerve (X)

Somatic motor: None, no striated muscles from somites.

“Branchial” motor: Striated muscles of the 4th and 5th arches arise from the caudal nucleus ambiguus. Pharyngeal nerve to the constrictors contains contributions from r6 to r11. The soft palate, superior, and middle constrictors are supplied by r6–r7. Middle constrictor r8–r11. Superior laryngeal nerve from r8 to r9 supplies the PA4 intrinsic muscles of the larynx. Inferior laryngeal nerve from r10 to r11 supplies the PA5 muscles of the larynx.

Visceral motor: Smooth muscle from the level of c1 downward arises from LPM. All parasympathetic innervation to glands of the pharynx, larynx, neck thorax, and abdomen arise from or are situated in tissues arising from LPM.

Visceral sensory: Lower 2/3 of esophagus, remainder of the gastrointestinal tract and all other viscera.

General sensory: Pharynx from inferior constrictor, larynx and upper esophagus.

Special visceral sensory: Taste fibers from epiglottis.

Accessory nerve (XI)

Somatic motor: None.

“Branchial” motor: Basal form in sharks is the cucullaris muscle. This muscle functions as levator of the branchial arches extending from pectoral girdle forward to base of the skull, i.e., from r10 to r11 to c4/c5. Additional spinal contributions may run as low as c7. Cucullaris becomes sternocleidomastoid and trapezius. In its original form, XI was an exclusively spinal nerve but the backward expansion of the skull brought the first two levels inside the skull.

Visceral motor: none.

Visceral sensory: none.

General sensory: Somatic sensory from sternocleidomastoid and trapezius.

Special visceral sensory: none.

XI has extensive representation in the nucleus ambiguus, running all the way from r6 to r11 and continuing as the spinal nerve down as low as c7. But XI has no direct branches to palate, pharynx or larynx so its motor fibers travel to their destinations via glossopharyngeal and the vagus. XI in the cranial nucleus ambiguus (r6–r8) are distributed via the sensory branches of glossopharyngeal to soft palate, upper and middle constrictors, and superior laryngeal nerve. XI in the caudal nucleus ambiguuus (r9–r11) are distributed by the sensory fibers of vagus to the inferior laryngeal nerve.

The neuroanatomy of the accessory nerve is of great importance for understanding the transition between the head and the neck.[33],[34]

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  References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13], [Figure 14], [Figure 15], [Figure 16], [Figure 17], [Figure 18], [Figure 19], [Figure 20], [Figure 21], [Figure 22], [Figure 23], [Figure 24], [Figure 25], [Figure 26], [Figure 27], [Figure 28], [Figure 29], [Figure 30], [Figure 31], [Figure 32], [Figure 33], [Figure 34], [Figure 35], [Figure 36], [Figure 37], [Figure 38], [Figure 39], [Figure 40]

  [Table 1], [Table 2], [Table 3], [Table 4]

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