Phylogeny and embryology of the facial nerve and related structures. Part I: phylogeny.
The study of evolution provides invaluable insights into human structure and function. Much of evolution is recapitulated during human gestation. Understanding the evolutionary' process helps clarify seemingly complex embryology and anatomy, such as that of the facial nerve and related ear structures, as well as the anomalies that occur when human development is interrupted.
It is extremely useful for otolaryngologists who care for patients with congenital malformations of the ear and anatomically related structures to be familiar with the embryology of the facial nerve. A review of phylogenic history helps clarify many of the complex relationships between the facial nerve and the ossicles and other structures in the temporal bone and extratemporally. A complete description of the embryology and anomalies of the facial nerve, their surgical implications, and the syndromes with which they are associated is beyond the scope of this article; this information is available in other publications that illustrate how knowledge of embryology can be used to predict the position of the facial nerve in malformed ears. (1, 2) Such information is invaluable to the otologic surgeon.
Cranial development in the first land animals
Some 400 million years ago, the first lobe-finned fish crept out of the sea and stayed out. The water-to-land transition was accompanied by, among many other evolutionary changes, a process of development that led to locomotion, breathing, chewing, and hearing. For example, modification of the bones of the jaw in fish resulted in the development of auditory ossicles and a newly formed middle ear in what eventually became humans. Understanding this process helps clarify the origin of the facial nerve's convoluted path.
Approximately 460 million years ago, the anterior gill arches of some aquatic vertebrates evolved into jaws and their supporting structures, including the hyomandibular bone. In these jawed vertebrates (gnathostomes), the hyomandibula played a dual role in feeding and gill ventilation. After some gnathostomes emerged from the sea to dwell on land, the gill arches that did not form the jaw developed to form the tongue, the thyroid cartilage, the cricoid cartilage, and the structures of the pharynx and hypopharynx. The gills themselves became lungs, and the hyomandibula was transformed into an auditory ossicle: the stapes. These land vertebrates (tetrapods) were the ancestors of all present-day land animals, including secondarily aquatic forms such as whales, sea turtles, etc.
Both embryologic fossil records and comparative anatomic evidence suggest that the transformation of the hyomandibula into the stapes--along with the development of the eardrum, the middle ear cavity, and an area for the reception of sound in the vestibular apparatus--occurred independently in modern amphibians (e.g., frogs) and reptiles. Mammals differ from their reptilian ancestors in that their middle ear includes two additional bones, the malleus and the incus, which were apparently derived from the bone that formed the articular portions of the lower and upper jaw, respectively (figure 1).
[FIGURE 1 OMITTED]
Development of the brain case
Some form of brain case is a defining feature of vertebrates. What we call the skull in humans was formed from a combination of the primitive brain case (chondrocranium), the sensory capsules and their underlying supports, components of the visceral skeleton (gill arches and their derivatives), and the overlying dermal bones (dermatocranium). Because of the fossil record, we know precisely what happened to the shape of the vertebrate skull and skeleton through time. All causal explanations, however, are speculative to some degree.
Some attention to the structure of the original connection between the brain case and the gill arches is useful in understanding the basic changes in pressure that allowed for the eventual modification of the jaw and ear. The primitive vertebrate brain is tripartite, consisting of the fore-, mid-, and hindbrain. The basal support for the hindbrain is provided by parachordals that are formed from the sclerotome portion of anterior somites. The parachordals lie beside the notochord beneath either side of the hindbrain.
Support for the forebrain in gnathostomes is provided by the paired polar bodies and anterior trabeculae. The polar bodies probably are derived from the sclerotome. The anterior trabeculae are formed from neural crest tissue, and they make up a portion of the visceral skeleton anterior to the mandibular gill arch. (2) In the primitive jawed vertebrate, the remaining gill arches (i.e., the mandibular, hyoid, and fourth and fifth true branchial arches) surround the pharynx in the ventral part of the head. The sensory capsules--that is, the elements of neural crest tissue that surround the sense organs--are arrayed from anterior to posterior along the tripartite brain in this order: nasal capsule, optic capsule, and otic capsule.
This primitive arrangement of chondrocranium and gill arches forms the basis of the skull in all jawed vertebrates. Further fusion or linkages between these elements also occurs in a stereotypical fashion, and the exits of the cranial nerves from the brain bear a distinct relationship to the various original brain case components. For example, the exit for cranial nerve VII passes anterior to the otic capsule through a space (incisura pro otica) left by the growth upward and backward of the parachordals to form the acrochordal plate contacting the otic capsule.
The two structures of primary importance in the transition from agnathan (jawless) fish to gnathostomes were the mandibular arch (gill arch 2) and the hyoid arch (gill arch 3). (Gill arch 1 is presumed to have formed the anterior trabeculae.)
In gnathostomes, the mandibular arch forms the bones of the primitive jaw itself. (3, 4) The upper sections of the mandibular arch form the upper jaw (palatoquadrate), and the lower sections form Meckel's cartilage, which gives rise to the lower jaw. The hyoid arch forms the jaw supports; the upper portion of the hyoid arch forms the hyomandibula (which eventually becomes the stapes), and the lower segments of the hyoid arch form the hyoid apparatus.
These connections are somewhat complex. The palatoquadrate has three attachments to the chondrocranium. One attachment is located anterior to the chondrocranium at the anterior trabeculae, another attachment is at the polar bodies, and the third is a posterior attachment at the otic capsule (containing the inner ear). Meckel's cartilage attaches at the posterior portion of the palatoquadrate, next to the anterior attachment of the hyomandibula. Posteriorly, the hyomandibula is connected to the otic capsule (the cranioquadrate passage). There is a space between the otic capsule and the ascending process of the palatoquadrate where cranial nerve VII exits the skull posteriorly. This evolutionary arrangement is reflected in human development during gestation.
There are three basic ways in which the jaw is suspended from the brain case. These designs are called amphistylic, hyostolic, and autostylic. (4)
Amphistylic. The amphistylic arrangement is the primitive pattern from which all others were derived, and it is described above. This type of jaw suspension is rare among extant vertebrates.
Hyostylic. Most modern fish (bony fish with fins) have a hyostylic jaw suspension, which is responsible for their unique ability to move their entire jaw apparatus forward independent of the brain case. Their jaws are attached to the brain case mainly by the hyomandibula, and palatoquadrate connections 1 and 3 are replaced by ligaments.
Autostylic. In the autostylic architecture, the palatoquadrate is essentially fused to the chondrocranium. This is the type of jaw suspension seen in most present-day tetrapods (figure 2).
[FIGURE 2 OMITTED]
Developed in the dermis and capable of bearing rooted teeth, dermal bone was laid down over the entire original chondrocranium on the undersurface of the palatoquadrate and the anterior portion of Meckel's cartilage. These are the bones that form the dermatocranium. The parts that we are particularly concerned with are the new dermal bones that blanket the margins of the mouth. The maxilla and premaxilla are the bones over the palatoquadrate, and the dentary is the dermal bone over Meckel's cartilage (these, remember, were once the mandibular gill arch, situated in the second head segment). The developing jaw articulation is still the neural crest bone of the mandibular arch, which remains uncovered by dermal bone posteriorly. These portions of the palatoquadrate and Meckel's cartilage are called the quadrate in the upper jaw and the articular in the lower jaw. The dermal bone that has supplanted the original anterior bones is called the dentary (figure 3).
[FIGURE 3 OMITTED]
The relevance of these anatomic details to our discussion of the facial nerve is that the muscles associated with the branchial arches and jaws are innervated by a special set of visceral motor components of the cranial nerves. The relationship between the gill arches and the cranial nerves is complex. Briefly, the mandibular arch musculature was originally innervated by the post-trematic branch of the trigeminal nerve (cranial nerve V, the mandibular nerve). The hyoid arch musculature was originally innervated by the post-trematic branch of the facial nerve (cranial nerve VII, the hyomandibular nerve). When the mandibular and hyoid arches were incorporated into the jaw, cranial nerves V and VII remained with them.
Anatomic changes in the early tetrapods
When fish came onto land, the role of the hyoid arch and the facial nerve changed. The hyomandibula, which in bony fish helped move the operculum (the external gill flap) to aid in gill ventilation, was no longer necessary because the presence of lungs in early tetrapods allowed for independence from the gills. Tetrapods lost the operculum the transition from water to land. (5) Lungs are seen today in a variety of forms of bony fish, and they may be a primitive feature of this entire group, including those ancestral to tetrapods. In most living fish, however, lungs have transformed into swim bladders.(6)
In addition to the loss of the operculum, the first tetrapods were endowed with numerous structural differences from their aquatic relatives. These newborn land dwellers were odd creatures. They had the reproductive biology of modern amphibians, but based on fossil evidence, they can be best characterized as caiman- to crocodile-sized, overweight salamanders. They were slow and clumsy, they had large flat heads, their legs protruded out to the side like those of a lizard, and their skin was moist. Two of the first such creatures were called Ichthyostega and Acanthostega.
When animals began inhabiting the land, they had to contend with a number of structural problems. As fish, their skeletons only had to serve as an anchor for the musculature of movement. As tetrapods, gravity became an enormous factor, and keeping one's body off the ground was a major chore. In response, evolution eventually resulted in a reorganization of primitive skeletal components. No fish--including the rhipidistians, (7) who first braved solid ground had any bony articulation between the skull and the vertebral column. The notochord penetrated the brain case to the level of the pituitary gland, and a series of extrascapular dermal shoulder girdle bones were attached to the dermal head shield. The pelvic girdle was not even attached to the vertebral column. Ribs were insignificant, and the vertebrae had no regional specialization or interlaced neural arches.
In the first tetrapods, there was specialization of the anterior cervical vertebrae into a primitive atlas-axis complex, as well as a distinct split into a cervical trunk, sacral and caudal vertebrae, and interlocking vertebral centra with upright neural arches. The pelvic girdle was firmly attached to the vertebral column, and the pectoral girdle had smaller extrascapular dermal bone components (with the exception of the clavicle, which was larger). The ribs, once fine and flexible, became heavy and imbricating so that they could support the thick trunk. Moreover, the primary vibratory sensory apparatus of the fish, the lateral line, was no longer functional on land. The lateral line consists of a series of pits that contain hair cells that conduct low-frequency vibrations. There is no fluid-to-fluid system on land that transduces sound in this manner. In present-day mammals, high-frequency pressure waves are transmitted to the fluid-based system of the inner ear. No such arrangement existed in early tetrapods, however.
Ventilation and locomotion
The two factors that most significantly affected the arrangement of the bones in the jaw are ventilation and locomotion.
Ventilation. Mammals use a combination of diaphragmatic contraction and intercostal effort to compress and expand their lungs. Primitive tetrapods had not yet experienced these muscle adaptations. Their ribs were rather immobile and structurally locked into the effort to support the body, and they were not available to be modified for respiration. The first tetrapods probably forced air in and out of their lungs by a process called buccal pumping. (8) Buccal pumping is the mode of ventilation in modern amphibians, and it is closely akin to the mode by which fish ventilate their gills. It is conceivable that the hyomandibula played a role in buccal pumping in the earliest tetrapods. (3) However, in all tetrapods, the hyomandibula's role in feeding and ventilation became obsolete. It appears that the hyomandibula then served as a bony link connecting the brain case and the cheeks, a partial retention of its original function in fishy
During buccal pumping, an animal opens its nostril and lowers the floor of its mouth while elevating the palate and keeping the glottis closed; this creates a vacuum in the oral cavity, into which air is drawn. Then the animal occludes the nostril, opens the glottis, raises the floor of the mouth, and depresses the palate; this forces the air from the oral cavity into the lungs, which expand to accommodate it. Then the lungs contract by elastic recovery, and the glottis and nostril open to allow the air out. This process is sufficient for drawing in oxygen, but the release of carbon dioxide is still primarily achieved in the water through moist skin, as it was in primitive tetrapods. (10)
Locomotion. As these clumsy tetrapods slowly became more mobile and terrestrially comfortable, their efforts to move more efficiently became an evolutionary force. At first, amphibians were not using their legs so much for propulsion, but for holding fast to the ground so that their trunk muscles could lilt their bodies over their legs. (11) This type of ambulation was very inefficient, both in terms of energy expenditure and the occupation of axial muscles and bone for the purpose of movement. The legs of the early amphibians were splayed out to their sides, and their elbows and knees pointed up. The femur and humerus were more or less horizontal and at right angles to the lower limb bones. As these amphibians became more adept at using their limbs for propulsion, their legs became positioned further beneath the body and their elbows and knees pointed back rather than up. This inward turning of the limbs was responsible for the characteristic twisting of the radius and ulna that is seen in the forearms of many modern tetrapods, including humans.
In addition to the locomotive advantages conferred by the repositioning of the legs under the body, this change also meant that the legs were now closer to the animal's center of gravity. The repositioning alleviated the tremendous support problems that were to that point being solved, or at least managed, by the enormous, imbricating ribs, which helped assure that the body would not be crushed when it lay on the ground. Once the legs could keep their bodies off of the ground, these tetrapods developed coordinated movement of the muscles via antagonistic pairs and improved proprioception. As a result, the axial skeleton and musculature were relieved of design constraints whose function was to maintain the shape of the body when it rested on the earth.
Profound changes in morphology and physiology
With greater speed and range of movement, tetrapods could breathe more easily and eat a greater variety of substances. These two changes accounted for subsequent alterations in ventilation and head shape. It was at this point that great changes began to occur in the morphology and physiology of tetrapods and in their way of life. This point marked the transition of some species from amphibians to reptiles.
The physiology of land animals underwent significant evolution in terms of circulation, reproduction, osmoregulation, sensation, digestion, and excretion. The changes in locomotion and support that relieved the ribs of their weight-bearing role allowed the ribcage and rib musculature to adapt to a new function: expanding and compressing (by elastic recovery) the lungs. It is very likely that the development of an adequate means of expelling all the carbon dioxide through the lungs (rather than by resorption through the skin) spelled the end of moist skin for those tetrapods that became fully terrestrial. It is probable that this better means of expelling carbon dioxide allowed these creatures to become fully independent from the water and contributed to the development of the amniote egg, which was integral to the transition from amphibian to reptile. (8)Regardless of whether this is true, the use of costal ventilation made buccal pumping obsolete. Now that the jaw was no longer locked into a structure that facilitated buccal pumping, it began to change in response to other selective pressures. One should consider that the processes of costal ventilation, limb modification, and jaw reorganization likely occurred somewhat simultaneously rather than sequentially. Evolutionary systems tend to coevolve as minute advances in one system's design are made possible only by subtle alterations in another.
So, between the time of the appearance of early amphibians approximately 380 million years ago and the appearance of reptiles approximately 310 million years ago, the jaw changed from being basically a one-point snapping structure to a structure that had some level of refined movement. Amphibians use the opening-and-shutting technique that characterizes inertial feeding, while reptiles can execute both inertial feeding and static feeding; the latter is accomplished by applying pressure while the mouth is closed. (12) This advance in feeding was made possible by distinct changes in the jaw musculature. The primitive adductor muscle for the mandible had split into two parts: the pterygoideus, which originated in the pterygoid flange, and the muscle that in mammals is called the temporalis, which originated in the dermal skull roof behind the eyes; both of these muscles are innervated by the Vth cranial nerve. Different points of insertion on the jaw and skull allowed for more flexible jaw dynamics. The leverage of the pterygoideus was best when the jaw was open, an arrangement that powered the snapping motion; the leverage of the temporalis was best when the jaw was closed, which provided static pressure. These developments were accompanied by the doming of the reptilian skull, which became distinct from the flat amphibian skull. The temporalis runs in an inferosuperior direction from the jaw to the skull roof. Because muscles can stretch only about one-third the distance of their resting length, the temporalis needed a high insertion point on a domed skull in order to achieve enough length to permit the stretch required for the jaw to open.
At this point in the evolutionary process, the palatoquadrate was completely fused with the chondrocranium to form a true autostylic jaw suspension, and it was covered almost entirely by dermal bone. The remainder of the palatoquadrate and Meckel's cartilage divided into smaller bones. Several smaller, posteriorly located bones remained uncovered, including the epiptery goid, the pterygoid, and the quadrate. The lower jaw was almost completely made up of dentary bone; other minor components included the angular, surangular, and articular bones. The jaw joint was made up of the two most posterior bones, the quadrate on top and the articular on the bottom.
When a group of reptiles called the synapsids branched off from the main reptile line to become the precursors of mammals, the jaw again underwent changes. Mainly, it developed a complexity of musculature that allowed the quadrate, articular, and hyomandibular bones to migrate to the middle ear. The process of development can be traced by following the evolution of pelycosaurs (animals with spiked sails on their backs that resembled large Komodo dragons) to cynodonts, whose jaws and related muscular features were much closer to those of mammals. The changes ill the anatomy of the jaws that took place as mammal-like reptiles evolved into mammals were characterized by an increase in the size of the temporalis muscle and the dentary bone and a reduction in the size of the postdentary bones (i.e., what was left of the mandibular arch) (figure 4). The postdentary bones in synapsids are the functional jaw elements; the quadrate and articular are both large, and the stapes is relatively massive, and it contacts the quadrate distally.
[FIGURE 4 OMITTED]
The modern jaw
This tremendous change in jaw musculature can be understood macrocausally in terms of food requirements. Mammals are endothermic, and they typically need 10 times more food and oxygen per unit of body mass than do reptiles, which are exothermic. Thus, there was a general trend in mammalian evolution toward an increase in the volume of jaw musculature and in tooth complexity. The primary advancement occurred in the masseter muscle. Mammals needed to achieve a faster means of processing food, which they accomplished by breaking down food into smaller particles, which increased the amount of food surface area that could be digested at once. In other words, they began to chew their food.
The ability to efficiently masticate was enhanced by an increase in the size of the temporalis muscle. Unless the size of the pterygoideus muscle also increased correspondingly, the location of the bite point would have had to change. However, such an enlargement of the pterygoideus, which is located medial to the jaw, would have blocked the throat passage. Therefore, the bite point did change. Also, the evolution of the masseter provided the extra force--as well as the capacity for lateral movement--that allowed for more efficient grinding of food. Accompanying adaptations included the bowing of the zygomatic arch to accommodate the larger masseter and the increased complexity of the post-canine teeth for mastication.
No definitive premise has been proposed to explain why the jaw joint changed from the quadrate/articular junction to a dentary condyle, while the old jaw joint structures moved to develop into ear structures. One very good explanation, however, is based on the hypothesis that the quadrate/articular jaw joint was already a part of the auditory apparatus. (13) Vibrations of a tympanum (recent evidence suggests that the tympanum was supported by the reflected lamina of the angular bone) were conducted through the articular bone in the lower jaw, through the quadrate bone in the upper jaw, through the stapes, and into the uric capsule. The stapes was already resting against the quadrate, where it supported the palatoquadrate. It is possible that the branch of reptiles that became mammals transduced sound in this fashion the entire time, and that competition for the function of these three bones did not occur until the advent of endothermy and the subsequent need for more rapid food processing. The reliance on mastication to maintain a high metabolism might have resulted in a situation in which the animal spent so much time masticating that it lost its ability to hear (have you ever tried to listen to someone talk while you were chewing potato chips?). Many reptiles, on the other hand, eat only once a month, and even the most voracious reptile appetites don't approach the level of mammalian consumption. Furthermore, when reptiles do eat, they grab and gulp rather than chew (because their energy demand is much lower than that of mammals, rapid digestion is not important). Hence, ingestion has had little or no effect on audition in reptiles.
Comparing the needs of more primitive species with those of mammals would only explain why the jaw joint changed, not how it changed. We still have not identified a causal evolutionary set of circumstances that would explain the adaptive mechanisms at each stage during which changes occur. The most plausible explanation seems to be that the small bones at the back of the jaw experienced reactionary stress as the powerful jaw muscles forced the action of the jaw. (14) As noted, the temporalis had become increasingly larger throughout early mammalian development. The angle of the muscle projected farther back on the enlarged temporal fossa to accommodate the increase in muscle size. The combination of the alteration of the bite point and the increase in muscle mass changed the vectors of the stress on the jaw joint. During inertial action, the force tended toward dislocation of the dentary/ postdentary joint, and during static pressure, the force caused the bones to grind against one another. Fibers of the temporalis muscles split off in an anterior orientation to relieve the reactive pressure against the weaker postdentary bones. In the meantime, a piece of bone called the condylar process grew posteriorly to help brace the connection between the dentary and postdentary bones. Eventually, the bone flange reached the squamosal of the skull and became a second jaw joint. The muscle fibers that constituted the deep masseter, which grew off anteriorly to relieve the stress on the jaw joint, were ideally suited for mastication and better jaw control. The formation of a new, stronger jaw joint formed entirely of the dentary bone freed the articular, quadrate, and hyomandibula and allowed them to become encapsulated in a middle ear cavity for the sole purpose of conducting sound (figure 5). These bones, which retained the same basic relationships in mammals as they did in mammal-like reptiles, are the malleus, incus, and stapes.
[FIGURE 5 OMITTED]
The phylogeny of the muscles of facial expression and the facial nerve is somewhat less easily understood than that of other muscles of branchiomeric origin. Nevertheless, recognizing that most muscles have retained the innervation they acquired during the gill-arch stage helps clarify the arrangement in humans. For example, muscles that arise from the mandibular arch (i.e., the temporal, masseter, pterygoid, and mylohyoid muscles and the tensor of the tympanum, tensor of the velum palatinum, and the anterior belly of the digastric muscles) are supplied by the trigeminal nerve, the nerve of the mandibular arch. In lower life-forms up through fish, facial expression is limited to mandibular motion. In humans, the muscles of the mandibular arch have been pre-empted for use in chewing and swallowing, and they are not primarily involved in facial expression. In the faces of fish and lower animals, there is no muscle tissue between the skin and bones, and the muscles used for chewing and swallowing are not used for facial expression. Therefore, the nearest available muscles that could provide for facial expression--those of the hyoid arch--migrated to serve this purpose. The different degrees of complexity in the ascending order of animals (e.g., from fish to amphibians to mammals) correlate with the extent of hyoid arch muscle migration. In amphibians, a superficial layer of muscle in what was once the gill area acts as a primitive constrictor. In mammals, both the deep and superficial layers of the hyoid musculature spread into the face and carry the facial nerve with them, thus creating its intricate course (figure 6).
[FIGURE 6 OMITTED]
According to a paleontologic adage, ontogeny recapitulates phylogeny. In the embryology of present-day mammals, the developmental process in the bones and muscles of the first and second branchial arches involves a re-enactment of the evolutionary process than begot the mammalian middle ear. Meckel's cartilage grows back to meet a primary jaw joint and becomes enveloped by intramembranous bone. The posterior portion ossifies into the articular, while the posterior portion of the upper jaw ossifies into the quadrate. In mammals, the dentary expands to make up the entire mandible, while the condyle grows back to meet the squamosal component of the cranium, forming the second jaw joint. The articular, quadrate, and stapes separate from the other intramembranous bones of the jaw and become isolated as middle ear components--that is, the malleus, incus, and stapes. During the sixth and seventh weeks following fertilization, the frontal, auricular, occipital, and platysma muscles are derived from the primordial superficial muscle sheet. (15) The primordial deep layer of muscle from the hyoid arch gives rise to muscles that control the movements of the nose and lips and around the eyes. Knowledge of the migratory pattern of these muscles and the branches of the facial nerve and external carotid artery that they carry with them is helpful in understanding the complex anatomy of the human adult. It is also helpful in understanding the congenitally abnormal anatomy associated with interrupted migration during development.
(1.) Sataloff RT. Embryology and Anomalies of the Facial Nerve and Their Surgical Implications. New York: Raven Press, 1991.
(2.) Sataloff RT. Embryology of the facial nerve and its clinical applications. Laryngoscope 1990;100:969-84.
(3.) Goodrich ES. Studies on the Structure and Development of Vertebrates. London: Macmillan, 1930.
(4.) DeBeers GR. The Development of the Vertebrate Skull. Oxford: Oxford University Press, 1931.
(5.) Clack JA. The stapes of Acanthostega gunnari and the role of the stapes in early tetrapods. In: Webster DB, Fay RR, Popper AN, eds. The Evolutionary Biology of Hearing. New York: Springer Verlag, 1992:405-20.
(6.) Liem KF. Form and function of lungs: The evolution of air breathing mechanisms. Am Zool 1988;28:739-59.
(7.) Panchen AL, ed. The Terrestrial Environment and the Origin of Land Vertebrates. London: Academic Press, 1980.
(8.) Brainerd EL, Ditelberg JS, Bramble DM. Lung ventilation in salamanders and the evolution of vertebrate air breathing mechanisms. Biol J Linn Soc 1993;49:163-83.
(9.) Carroll RL. The hyomandibular as a supporting element in the skull of primitive tetrapods. In: Panchen AL, ed. The Terrestrial Environment and the Origin of Land Vertebrates. London: Academic Press, 1980:293-317.
(10.) Little C, The Colonisation of Land: Origins and Adaptations of Terrestrial Animals. Cambridge: Cambridge University Press, 1983.
(11.) Carroll RL. Early evolution of reptiles. Ann Rev Ecol Syst 1982; 13:87-109.
(12.) Carroll RL. Problems of the origin of reptiles. Biol Rev 1969; 44:393-432,
(13.) Allin EF. Evolution of the mammalian middle ear. J Morphol 1975; 147:403-38.
(14.) Bramble DM. Bifocal model of jaw function. Paleobiology 1978; 4:271-301.
(15.) Patten BM. Human Embryology. Philadelphia: Blakiston, 1946: 112-13, 306-14, 371-5, 435.
From the Department of Otolaryngology-Head and Neck Surgery, Graduate Hospital, Philadelphia, and the Department of Otolaryngology--Head and Neck Surgery, Thomas Jefferson University, Philadelphia (Dr, Sataloff), and the University of Pennsylvania School of Medicine, Philadelphia (Dr. Selber).
Reprint requests: Robert Thayer Sataloff, MD, Department of Otolaryngology--Head and Neck Surgery, Thomas Jefterson University, 1721 Pine St., Philadelphia, PA 19103. Phone: (215) 7326100; fax: (215) 790-1192; e-mail:email@example.com
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|Title Annotation:||Original Article|
|Author:||Selber, Jesse C.|
|Publication:||Ear, Nose and Throat Journal|
|Date:||Sep 1, 2003|
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