arytenoid and lateral cricoarytenoid, and terminates in thyroarytenoid, The result is a mildly hoarse voice with loss of pitch control. Bilateral
which it also supplies (see also Maranillo et al 2005). superior laryngeal nerve lesions result in shortening of both vocal folds,
The recurrent laryngeal nerve forms several anastomoses with the the overhanging of the epiglottis over the folds and reduced tilt between
superior laryngeal nerves (see Fig. 35.12). The posterior branch of the the thyroid and cricoid cartilage. Effects on the voice are correspond-
recurrent laryngeal nerve ascends deep to posterior cricoarytenoid to ingly greater, with reduced loudness and pitch but variable breathiness.
join the descending branch of the internal laryngeal nerve. The ansa Damage to the internal laryngeal nerve causes loss of mechanorecep-
Galeni, lying on the interarytenoid muscles, forms a direct connection tive and proprioceptive sensation from the larynx. Unilateral loss pro-
between the recurrent and internal laryngeal nerves (see Fig. 35.12). duces a feeling that something is stuck in the throat, whereas bilateral
There is also a complex anastomosis within and over the posterior loss will result in aspiration and can cause dysphagia, with a risk of
surface of the interarytenoid muscles, and, less frequently, anastomoses choking.


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nOITCES
Unilateral complete palsy of the recurrent laryngeal nerve is more language, such as speech and writing, and sensory manifestations of
common on the left side, presumably because the nerve is longer on language, including reading and understanding the spoken word.
this side. There is isolated paralysis of all the laryngeal muscles on the Central control of voice production involves two parallel pathways: a
affected side except cricothyroid, which is innervated by the external limbic pathway responsible for the control of innate non-verbal and
laryngeal nerve. The patient may be asymptomatic or have a hoarse, emotional vocalizations, and a larynx-specific motor cortical pathway
breathy voice and there will be diminished ability to manipulate pitch. responsible for regulating the motor control necessary for voluntary
The hoarseness may be permanent or may become less severe with time voice production. For further reading, see Clark et al (2007), Kaplan
as the contralateral cord develops the ability to hyperadduct and appose (1971), Laver (1980), Atkinson and McHanwell (2002), Titze (1994),
the paralysed cord and thus close the glottis during phonation and Zemlin (1998).
coughing, although this is seldom enough to restore full voice quality.
There may be aspiration of food and drink. Bilateral lesions of the
recurrent laryngeal nerve result in both vocal cords being paralysed and OVERVIEW OF SPEECH PRODUCTION
taking up a paramedian position. Phonation can be nearly normal
because the vocal folds lie so close to the midline, but there will be All speech requires an input of energy. For all sounds in Western Euro-
audible stridor and a very compromised airway. pean languages, and most sounds in other languages, this energy takes
Clinically, the position of the vocal cord in the acute phase after the form of a pulmonary expiration. This continuous airflow is con-
section of the recurrent laryngeal nerve is very variable. Though stridor verted into a vibration within the larynx by a mechanism called phon-
is more common after bilateral lesions and sometimes only audible to ation, in which the vocal folds vibrate periodically, interrupting the


the educated ear, the cords may be sufficiently abducted so that there column of air as it leaves the lungs and converting it into a series of
is little problem with airway obstruction at rest, although the voice is discrete puffs of air. Speech sounds that are produced by vocal fold
always weaker in this situation. The cords are slightly more widely sepa- vibration in this way are said to be voiced. Speech sounds that are
rated in chronic lesions, which renders the voice weaker but with a less produced without vocal fold vibration are termed unvoiced sounds.
precarious airway. Atrophy and fibrosis of paraglottic muscles probably The larynx is an inadequate sound source; the laryngeal ‘buzz’ that
affect the position of paralysed vocal cords in chronic lesions to a is produced by phonation is very quiet and cannot be varied sufficiently
greater degree than variations in the strength of the apposing adductor to produce the complex range of sounds that is human speech. Ampli-
and abductor muscle groups. fication and modification of the sound occur in the supralaryngeal vocal
For many years, conventional wisdom held that movements of tract, which may be considered as a 17 cm long tube, narrow at the
abduction were affected to a greater degree than those of adduction larynx and broadening out proximally as it passes through the pharynx,
when the recurrent laryngeal nerve was partially damaged (Semon’s and oral and nasal cavities. This tube acts as a passive amplifier of the
law). This effect was thought to reflect the internal segregation within sound. (The analogy here is of a megaphone; cupping the hands round
the recurrent laryngeal nerve of axons supplying the laryngeal abductor the lips lengthens the vocal tract and increases the volume of speech.)
muscles; the idea was later undermined by the demonstration that The supralaryngeal vocal tract modifies the basic vibration of the larynx
axons destined for particular laryngeal muscles are randomly distrib- by altering its geometry, length and calibre; it provides a series of reso-
uted within the nerve. The weak abductive action of cricothyroid that nators that can dampen or amplify certain sound frequencies and can
is said to occur on lengthening the vocal folds has been proposed as an transiently interrupt the exhaled air flow and modify it to produce


explanation for the relative sparing of abduction in these lesions but is speech. This process is known as articulation. The range of sounds that
difficult to reconcile with the alternative view that cricothyroid may be the human vocal tract is capable of producing is very wide, although
a slight adductor of the vocal folds (Mu and Sanders 2009, Wadie et al any one human language will employ a subset of these sounds to
2013). It is likely that predicting the effect of partial lesions of the recur- convey meaning.
rent laryngeal nerve is complicated by the variable patterns of anasto-
mosis that occur between the laryngeal nerves. For further reading, see
Aronson and Bless (2009) and Blitzer et al (2009). MUSCULAR CONTROL OF THE AIRSTREAM
Normal vegetative ventilation involves rhythmic movements of the tho-
Autonomic innervation
racic cage that are produced by intercostal muscles and the diaphragm
and by a number of accessory muscles in the neck, arm and abdomen
Parasympathetic secretomotor fibres run with both the superior and the that have one attachment to some part of the thoracic cage. The thorax
recurrent laryngeal nerves to mucous glands throughout the larynx. is capable of responding mechanically to widely varying demands for
Postganglionic sympathetic fibres run to the larynx with its blood oxygen. From a tidal volume at rest of 500 ml and a respiratory rate of
supply; they originate in the superior and middle cervical ganglia. A 12 per minute, ventilation can increase in fit individuals during vigor-
variable number of paraganglia are located on the internal laryngeal ous exercise to tidal volumes of 4.5 litres and respiratory rates of 20–25
and recurrent laryngeal nerves. Histochemical evidence suggests that per minute.
one population of the neurones in these ganglia have a parasympathetic Normal ventilatory patterns are considerably modified during
function whilst a second population may secrete dopamine (Maranillo speech, reflecting the special demands that speech places on ventilation.
et al 2008, Ibanez et al 2010). The main source of energy for the production of speech sounds is
a pulmonary expiration, although other mechanisms are possible. In
order for speech to be produced, sufficient pressure has to be generated
ANATOMY OF SPEECH


beneath the vocal folds. This subglottal pressure (the difference between
the air pressures above and below the vocal folds) has to be sustained
The principal biological function of the larynx is to act as a sphincter above a minimum level throughout an utterance. It sets the vocal folds
controlling the entry of foreign bodies into the airways and to regulate into vibration if the sound is to be voiced or generates airflow for an
airflow during ventilation. Thus, the larynx is opened widely during unvoiced sound. The minimum subglottal pressure needed for speech
ventilation and is closed tightly during swallowing. The larynx can also production is 7 cmHO, and this increases when loud sounds are pro-
2
close tightly during exertion, effort closure, to regulate thoracic and duced or when sounds are stressed.
abdominal pressure during activities such as defecation or parturition, The need to generate sufficient sustained pressure means that speech
or to fix the thorax to increase mechanical advantage when using the ventilation is markedly non-rhythmical. At the onset of an utterance,
arms to lift objects. The importance of the latter activity should not be inspiration is typically 1.5 litres, which is deeper than for normal quiet
underestimated; one of the many problems reported by patients who ventilation, ensuring that sufficient air is taken in to maintain adequate
have undergone a laryngectomy is a loss of power in their arms when subglottal pressure for the duration of the utterance. Inspiration is also
trying to lift heavy objects. quicker, 0.5 seconds rather than 2–3 seconds. Expiration is much
The larynx is much more than a simple valve that opens and closes. longer than normal, perhaps lasting up to 30 seconds, reflecting the fact
In addition to its sphincteric functions, its location means that it is that the vocal tract is more constricted at the larynx to ensure that
perfectly placed to act as a sound source, or voice, that forms the basis pauses for further inspirations are made at suitable points in an utter-
of nearly all sounds in human speech. The musculoskeletal structure of ance. At the end of the first inspiration during running speech, lung
the larynx is under exquisite neuromuscular control, allowing it to volumes do not fully return to resting levels. Conversational speech


modify the expiratory stream to produce highly complex patterns of normally takes place at a higher range of lung capacities than operate
sound of varying loudness, frequency and duration. The ability to in normal quiet ventilation.
execute these complex movements depends largely on specific areas The non-rhythmical pattern during speech requires greater inspira-
of the cerebral hemispheres that are involved in the motor aspects of tory effort, and for most people it involves a greater use of the


Anatomy of speech
601
53
RETPAHC
diaphragm, usually in combination with the abdominal muscles that moves their vocal processes apart, and converts the rima glottidis into
are attached to the lower ribs (they stabilize the costal attachments of a diamond shape in which both intermembranous and intercartilagi-
the diaphragm and increase the effectiveness of its action). The main nous parts are triangular. The greatest width of the rima glottidis is at
differences, however, are seen in expiration. Speech takes place at higher the point of the attachments of the vocal cords to the vocal processes.
lung volumes, which means that greater recoil forces are stored in the During speech, the true vocal folds vibrate to act as a source of sound
elastic tissues of the lungs and the ribcage. The generation of subglottal for subsequent speech. There have been a number of theories to explain
pressure is the product of these elastic recoil forces and the muscular the mechanism that produces this vibration but these are now only of
forces generated by the expiratory muscles. At the onset of an utterance, historic interest. The aerodynamic–myoelastic theory is generally
unrestrained recoil forces would generate excessive subglottal pressures accepted as the mechanism underlying vocal fold vibration, although
that would be wasteful of air, and hence energy, and would affect the it does not account for all aspects of phonation.
loudness of speech. Conversely, towards the end of an utterance, as At the onset of an utterance, during an expiration, the true vocal
recoil forces decline, subglottal pressure would fall without additional folds are adducted: the lateral cricoarytenoids and interarytenoids bring
muscular exertion. Therefore, early in an utterance, inspiratory muscles, together both the intermembranous and intercartilaginous parts of the
particularly the external intercostals and parasternal parts of the internal glottis, actions that either close the glottis completely or reduce the
intercostals, continue to contract, relaxing slowly to counteract the space between the vocal folds to a linear chink. The mucous membrane
effects of excessive passive elastic recoil. As the recoil forces decline covering the interarytenoid muscles, the interarytenoid fold, intrudes


below the point where they can maintain the minimum subglottal into the larynx when these muscles adduct the arytenoids, and so aids
pressure needed for phonation, expiratory muscles contract to maintain closure of the intercartilaginous part of the rima glottidis. The vocal
subglottal pressure as lung air volume nears its resting expiratory level. cords are also tensed, an essential prerequisite for vibration. These
The main muscles involved are the costal parts of the internal intercos- actions cause a build-up of subglottal pressure that continues until a
tals and the subcostal and transversus thoracis muscles. Their actions point is reached when the muscular force of adduction is no longer
are aided by contraction of the anterior abdominal muscles to compress sufficient to resist the rising pressure, and the vocal folds are forced
the abdomen. Accessory muscles such as latissimus dorsi may also come open a little, releasing air into the supralaryngeal vocal tract. The sub-
into play, but normally these accessory muscles are only active at the glottal pressure falls when the subglottic and supraglottic cavities
end of a very long or loud utterance, or in patients whose ventilatory become continuous and the vocal folds begin to close. Two mechanisms
function is compromised. bring about closure. If adductive tension is sustained, then the vocal
Though subglottal pressure tends to remain fairly constant during folds will close. In addition, rapid closure is aided by a physical process,
an utterance, it rises when sounds are stressed, and falls during the the Bernoulli effect. The forcing of air from a region of high to low
production of unvoiced sounds when the larynx is less constricted. At pressure through a narrow space causes an increase in the kinetic energy
these times, compensatory mechanisms are required to ensure that of the molecules at the edge of the space. The effect of this is to lower
pressure is maintained; the precise mechanisms have yet to be eluci- pressure in the space between the folds at the level of the folds them-
dated but the internal intercostal muscles have been implicated. The selves, and this negative pressure simply sucks the folds together because
anterior abdominal muscles are also active in singing and shouting, and they are mobile. This causes a rise once more in the subglottal pressure


in attempts to speak without the pause necessary for inspiration. Con- and the cycle is repeated. The effect is to cause the release of a series of
trary to popular belief, the diaphragm plays little part in the regulation puffs of air into the supralaryngeal vocal tract at a frequency of many
of expiratory force. Unlike the intercostal muscles, the diaphragmatic times per second, which is perceived as a sound of a particular fre-
musculature is sparsely supplied with muscle spindles, and therefore quency (Figs 35.13–35.14).
control of the diaphragm is poorly regulated; minute changes can be The source of energy for the vibration does not come from the larynx
effected more successfully using the intercostal and anterior abdominal itself. The vocal folds do not behave like the prongs of a tuning fork;
muscles. their predominant motion is in the horizontal plane at right angles to
Though the expiratory airflow from the lungs is the source of energy the movement of the air column, and there is little vertical movement.
for most speech sounds, other sources of airflow are also used. The The energy is derived from the motion of the air generated by the mus-
larynx can be used to generate airflow. The sound /p/ is produced by cular and recoil forces in the thorax, and the larynx is simply chopping
closing the larynx and then raising it with the lips closed, using the that column into a series of segments.
larynx like a piston. Opening the lips then releases a puff of air. This is The aerodynamic–myoelastic theory does not explain how vocal fold
called an ejective and is an example of egressive glottalic airflow. Ingres- vibration is sustained; nor does it account for the very obvious muco-
sive glottalic airflow is also possible, though less effective; examples are undulatory component of vocal fold vibration that is visible when the
not found in English but do occur in some African and native American larynx is viewed stroboscopically. Without further input of energy, the
languages. A third kind of airflow is velaric, in which the back of the vibration of the vocal folds as described above would not be sustained
tongue is raised against a lowered soft palate and the vocal tract is closed but would be damped and gradually diminish. For vibration to con-


anterior to that point, either at the lips or with the tongue against the tinue there has to be additional energy input. The analogy here is with
hard palate. This produces a click and is rare. A non-linguistic example a child on a swing. For the motion to continue, either the parent has
in English is the sound made in encouraging a horse. Ingressive pulmo- to push the child at an appropriate point in the cycle, or the child has
nary airflow, such as is found in a groan or a gasp, is theoretically pos- to sustain the motion for themselves by swinging their legs at the crucial
sible, but none of the world’s languages employ this as a source of point in the swing cycle. In the case of phonation, the source of this
airflow. additional energy is unclear. It may come from the inertia of the air
After removal of the larynx, e.g. following laryngeal cancer, patients column itself, i.e. once the vocal folds close, the air column will con-
can be taught to swallow air, store it in a segment of the oesophagus tinue moving upwards because inertia creates a negative pressure above
and then use it as the energy source to produce egressive oesophageal
airflow (oesophageal speech). Speech in these circumstances tends to
have a belching quality and may be badly phrased. Laryngectomy
patients always produce phrases that are shorter than normal, and so
prostheses incorporating valves and surgical shunts are often inserted
to provide a larger egressive airstream by diverting air from the respira-
tory tract into the oesophagus.
PHONATION
The default position of the rima glottidis is open, to maintain patency
of the airway during respiration. In quiet respiration, the anterior inter-
membranous part of the rima glottidis is triangular when viewed from
above. Its apex is anterior and its base posterior, and it is represented
by an imaginary line approximately 8 mm long connecting the anterior
ends of the arytenoid vocal processes. The intercartilaginous part
between the medial surfaces of the arytenoids is rectangular, as the two
vocal processes lie parallel to each other. During forced respiration, the Fig. 35.13 A video montage of the normal phonatory cycle, obtained


rima glottidis is widened and the vocal cords are fully abducted to using a rigid fibreoptic endoscope with stroboscopic illumination.
increase the airway. The arytenoid cartilages rotate laterally, and this (Courtesy of Professor Paul Carding.)


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nOITCES
A
B Laryngeal
vestibule
Vestibular fold
Ventricle
Vocal fold
Infraglottic cavity
Opening phase:
subglottic pressure forces folds apart
A
B
Closing phase:
elastic recoil and Bernoulli effect
Fig. 35.14 The position of the vocal folds during a cycle of vocal fold vibration (phonatory cycle). A, Superior view. B, Coronal view.
the folds. Alternatively, the energy could come from the manner in there will be a consequent thinning and change in tension. Although
which the folds open and close. As the subglottal pressure rises, the an analogy is often drawn between the vocal cords and vibrating strings,
lower portion of the fold opens first and the upper edge of the fold is a better analogy is that of a rubber band: if a rubber band is lengthened,
last to open, and when the subglottal pressure falls, the folds close from the tension will increase but the thickness will decrease. The vocal cords
the bottom edge. It has been suggested that this non-uniform closure may be lengthened by up to 50% of their resting length. It is likely that
creates different shapes within the glottis that may result in differing the initial pitch setting is achieved by action of the cricothyroids, and
negative pressures at different phases of the cycle. It also produces a that fine adjustments can then be made using the vocales. Paralysis of
vertical wave-like motion in the folds, termed the muco-undulatory both cricothyroids, which is usually associated with loss of the neurones
component. The analogy here is with a flag blowing in the wind, and that are distributed via the superior laryngeal nerve (as a result of
it reflects the differing stiffnesses of the various layers of the vocal folds damage to the vagal nuclei in brainstem stroke), results in permanent
described above. This vertical component will impart a negligible hoarseness and inability to vary the pitch of the voice. It is important
amount of energy to the air column, but it is likely to impart harmonics to remember that, once the vocal cords are set in motion, they will
to the basic laryngeal vibration. deviate from their original setting as they vibrate. Auditory feedback of


The sound that results from the process of phonation has three the sounds produced is used to make minute compensatory adjust-
characteristics: a frequency that is perceived as pitch, an intensity that ments to length, tension and thickness in order to maintain a constant
is perceived as loudness, and a timbre perceived as voice quality. pitch.
The fundamental frequency of the human voice is determined by Any lengthening of the vocal cords tends to thin them. The thickness
the resting length of the vocal cords and varies with age and sex. The can be increased by the vocalis part of thyroarytenoid: as vocalis short-
frequency range of human speech is from 60 to 500 Hz, with an average ens, it will relax the vocal cords and at the same time increase their
of approximately 120 Hz in males, 200 Hz in females and 270 Hz in thickness. Changes in the tension of the vocal cords are produced by
children. The mechanism of frequency alteration is not entirely clear. the same muscles that change their length, namely: cricothyroid, pos-
An increase in subglottal pressure will cause the frequency of phonation terior cricoarytenoid and vocalis, probably acting isometrically.
to rise. During an utterance, however, subglottal pressure appears to The mechanism by which loudness is increased is the subject of less
remain fairly constant, which suggests that the mechanism of frequency debate. Loud sounds are produced by increasing subglottal pressure.
alteration resides in intrinsic changes within the vocal folds. Variations This is achieved, in turn, by changing the opening quotient of the glottis
in frequency (pitch changes) during an utterance are determined by the (the ratio of the time spent in the open phase of the cycle to the total
complex interrelationships between length, tension and thickness of the cycle time). In normal speech, this ratio is usually around 0.5, but in
vocal cords; one of these variables cannot be altered without affecting very loud speech it can fall to 0.3.
the other two parameters to some extent. Gross changes to the vocal Timbre or voice quality refers to the harsh or mellow quality of the
cords demonstrate the effects of these variables. Inflamed and swollen voice. At high volume, the voice tends to be harsher, especially in


vocal cords are much thicker than normal and result in a hoarse voice. untrained voices; higher-frequency components predominate because
At puberty, growth of the thyroid cartilage in males lengthens the vocal higher subglottal pressures are needed to sustain the increased volume.
cords and lowers the fundamental frequency, and the voice ‘breaks’ as This can be overcome to an extent by increasing the airflow rather than
a result. During panic, the vocal cords may be tensed, which means that the pressure.
the cry for help is a high-pitched squeak. A fundamental distinction in speech needs to be made between
Pitch is increased by lengthening the vocal folds, as may be con- voiced and unvoiced sounds; nearly all languages make this distinction.
firmed during direct endoscopic examination of the larynx. At first sight Voicing has been described above. In unvoiced sounds, the vocal folds
this may seem counterintuitive but, as the vocal cords are lengthened, are not vibrating and will usually be opened under the action of


Anatomy of speech
603
53
RETPAHC
posterior cricoarytenoid. The energy from the airstream is then used by PRODUCTION OF VOWELS
other parts of the vocal tract to generate sound, normally by constricting
or stopping the airflow. Phonation is not an all-or-nothing process, All vowel sounds require phonation by vibration of the vocal cords.
however, but is subject to considerable modification and adjustment. Each vowel sound has its own characteristic higher harmonics (fre-
In modal voice, i.e. speaking using habitual pitch, forces acting on the quency spectrum) that exhibit peaks of energy at certain frequencies.
vocal folds are moderate, pressures are sustained, and air is conserved. These energy peaks are always higher multiples of the fundamental
However, phonation can occur when the vocal folds are more open than frequencies and are called formants. Formants are the result of the
usual, resulting in breathy phonation with more air escaping per phon- combined effects of phonation, selective resonance of the vocal tract,
atory cycle than usual. Some languages in South Asia exploit the differ- and the properties of the head as a radiator of sound. The sounds of
ence between breathy and non-breathy sounds, whereas in spoken the different vowels are determined by the shape and size of the mouth,
English, a breathy voice is simply recognized as a feature of some speak- and the positions of the tongue and lips are the most important vari-
ers. At the other end of the spectrum is vocal creak, in which the vocal ables. The tongue may be placed high or low (close and open vowels),
folds are more closed than normal. Different speakers will habitually or further forwards or back (front and back vowels), and the lips may
employ different laryngeal settings that contribute to their particular be rounded or spread.
voiced quality. In whispering, the intramembranous part of the glottis
is closed but the intercartilaginous part remains open, which produces
a characteristic Y-shaped glottis and a greater loss of air at each phona- PRODUCTION OF CONSONANTS
tory cycle.
The main function of the larynx is to act as a sound source, but it can The production of consonants always involves some degree of constric-


also function in speech as an airstream generator and as an articulator. tion of the vocal tract. There are many more consonants than vowels,
and, in general, consonants cannot be combined to produce syllables.
The classification of consonants is complex and beyond the remit of
ARTICULATION
this book; what follows is a summary (for fuller details, a textbook of
phonetics should be consulted).
The sound produced by the phonation is not a pure tone because Consonants may be classified on the basis of where the constriction
several harmonics at multiples of the fundamental frequency are also occurs, termed the place of articulation; the degree or extent of con-
generated. Harmonics give a note of a particular frequency its defining striction, termed the manner of articulation; the shape of the constric-
characteristics. An ‘A’ played on an oboe or violin is immediately rec- tion, termed the stricture; and whether or not there is vibration of
ognizable because of the different harmonics generated by the design the vocal folds, when consonants are described as voiced or unvoiced,
of the instrument. The harmonic spectra of individual voices differ and respectively.
will also vary depending upon the mode of phonation adopted. In the Consonants may also be classified as labial, dental, alveolar, velar,
human vocal tract, the fundamental frequency and its harmonics are uvular, pharyngeal or glottic, depending on whether the point of
transmitted to the column of air that extends from the vocal cords to maximum constriction occurs at the level of the lips, teeth, bony ridge
the exterior, mainly through the mouth. Part of the airstream can also behind the teeth, palate, uvula, pharynx or glottis, respectively (Fig.
be diverted through the nasal cavities when the soft palate is depressed 35.15). Different parts of the tongue can be used in combination with
to allow air into the nasopharynx. The supralaryngeal vocal tract acts the above places of articulation. Phoneticians divide the tongue into
as a selective resonator whose length, shape and volume can be varied the tip, anterior edge, the front part of the dorsum, the centre and back
by the actions of the muscles of the pharynx, soft palate, fauces, tongue, parts of the remaining dorsum, and a most posterior part (the root).


cheeks and lips; the relative positions of the upper and lower teeth, These divisions bear no obvious relationship to the anatomical
which are determined by the degree of opening and protrusion or
retraction of the mandible; and alterations in the tension of the walls
of the column, especially in the pharynx. Thus, the fundamental fre-
quency (pitch) and harmonics produced by the passage of air through
the glottis are modified by changes in the supralaryngeal vocal tract. Nasal cavity
Harmonics may be amplified, or dampened. The fundamental fre- Hard palate
quency and its associated harmonics may also be raised or lowered by
Soft palate
appropriate elevation or depression, respectively, of the hyoid bone and
the larynx as a unit by the selective actions of the extrinsic laryngeal
Oral cavity
muscles. Effectively, these movements shorten or lengthen the resonat-
ing column, and to some extent also alter the geometry of the walls
of the air passages. Analysis of the human voice shows that it has a
Nasopharynx
very similar pattern of harmonics for all fundamental frequencies,
determined by the vocal tract acting as a selective filter and resonator. S (vo ef lt u p ma )late 3 4 5 6
This maintains a constant quality of voice without which intelligibility 2 10 7
would be lost (recorded speech played back without its harmonics is
Uvula 8
c suo gm gp esle tete dl y
th
u an
t
i tn ht ee l uli ng ii qb ule e) .
f
reE qa uch
e
nh cu
y
m spa en
c
trv uo mice
o
i fs
e
au cn hiq iu ne d;
i
vi it
d
h ua as
l
vb oe ie cn
e
Oropharynx
Dorsum Front Blade 9
Incisors
could be used for personal identification. 1 Back Tip
During articulation, the egressive airstream is given a rapidly chang-
Tongue
ing specific quality by the articulatory organs, the lips, oral cavity,
Epiglottis
tongue, teeth, palate, pharynx and nasal cavity. The discipline of pho-
netics primarily deals with the way in which speech sounds are pro- Laryngopharynx


duced, and consequently with the analysis of the mode of production
of speech sounds by the vocal apparatus. In order to analyse the way in Mandible
which the articulators are used in different speech sounds, words are
broken down into units called phonemes, which are defined as the
minimal sequential contrastive units used in any language. Hyoid bone
1.Pharyngeal
The human vocal tract can produce many more phonemes than are
2.Uvular
employed in any one language. Not all languages have the same pho- Vocal folds 3.Velar
nemes, and within the same language, the phonemes can vary in dif- 4.Medio-palatal
ferent parts of the same country and in other countries where that Trachea 5.Palatal
language is also spoken. Reproducing phonemes that are not used in 6.Pre-palatal
7.Alveolar
native speech is difficult because such phonemes require unfamiliar
8.Dental
positioning of the speech organs. A native speaker of any language can 9.Labial
quickly recognize the origins of anyone attempting to use their language 10.Retroflex (curled tongue tip)
as a second language. The second-language speaker will usually speak
it with an accent characteristic of their own first language because they Fig. 35.15 A sagittal view of the left side of the head, showing the
are using the familiar configurations of their vocal tract for each supralaryngeal vocal tract, the articulators and places of articulation. The
phoneme instead of the correct positioning. red broken line indicates the tongue position during retroflexion (10).


LARynx
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4
nOITCES
landmarks on the tongue, but they are useful in describing the part of the upper teeth. Neither involves a complete closure but both produce
the dorsum of the tongue that contacts other areas of the mouth. Simi- a significant constriction of the vocal tract with audible turbulence: the
larly, the manner of articulation can vary from a complete closure to a /f/ is unvoiced, while the /v/ is voiced. The sh sound (/∫/) in ship is
slight narrowing. An actual closure of the vocal tract is called a stop. A also a fricative involving a grooving of the tongue and is associated with
narrowing that is sufficient to produce turbulence of the air in the vocal significant audible turbulence; it may be contrasted with the lateral
tract, and which is perceived as a rustling sound, is termed a fricative. approximant /l/ in law, in which the sides of the tongue are lowered.
Approximants involve a degree of closure insufficient to produce tur- In this case, it is the nature of the stricture that is different and the
bulence but with closure greater than that for a vowel. Nasals involve degree of closure, e.g. in the case of the approximant /l/, closure is
a stoppage in the oral cavity with the soft palate lowered to allow airflow insufficient to produce turbulence. The sh sound in ship can be com-
through the nose, and, unlike stops, they can be sustained. Stricture pared to the /k/ in keen, where the position of the tongue is different:
describes the shape of the constriction, e.g. a lateral consonant involves in /k/ the tongue blade contacts the soft palate, while in sh the tongue
depression of the sides of the tongue, while a grooved consonant is tip or the blade contact the postalveolar region. The most dramatic
produced by grooving the dorsum of the tongue. Consonants can be example of the difference between voiced and unvoiced sounds may be
produced with the vocal folds vibrating, when they are termed voiced, appreciated if the /s/ sound in sip is compared with the /z/ in zip. If
or without vocal fold vibration, in which case they are termed unvoiced. the larynx is loosely palpated while making a sustained unvoiced ‘ssssss’


The best way to illustrate these classificatory systems in operation is sound, no vibration is felt, but if the ‘ssssss’ is commuted into a pro-
by contrasting the production of different consonant pairs in which longed voiced ‘zzzzzz’, then vibration in the larynx should be readily
only one or two parameters have been changed. The /p/ of peat, the /b/ detectable. The position of the tongue and other articulators is exactly
of beat and the /m/ of meat are all bilabial stops, meaning that they the same for both /s/ and /z/; the difference between them is the pres-
are produced by bringing together the lips. The /b/ and the /m/ are ence or absence of phonation.
voiced but the /p/ is not. The contrast between the /b/ and the /p/ is in
the differing way in which the airstreams are produced. The /b/ is pro-
duced with an egressive pulmonary airflow, while the /p/ is produced
with the glottis closed – hence is unvoiced – and the glottis is then
Bonus e-book image raised using the larynx as a piston to compress the air in the supra-
laryngeal vocal tract prior to the stop being released. The /m/ differs
from the other two stops in being a nasal in which the soft palate is
lowered to allow air to escape through the nasal cavity; unlike the other Fig. 35.9 A contrast-enhanced axial computed tomogram of the
two stops, it can be sustained as in a sound of approval. Bilabial stops neck of a 42-year-old male showing the paraglottic and pre-
can be contrasted with the labiodental fricatives /f/ of feet and the /v/ epiglottic spaces.
of veal, both of which are produced by retracting the lower lip beneath
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CHAPTER
36
Development of the head and neck
Head development is distinct from that of the trunk, utilizing region- the trigeminal ganglion. The non-neuronal cells migrate extensively to
specific genes, signalling mechanisms and morphogenetic processes. surround the telencephalon and part of the diencephalon, forming the
This chapter will provide a description of head and neck development frontonasal mesenchymal populations; they also migrate lateral to the
based primarily on data from studies on human embryos. Since this rhombencephalon to form the mesenchyme of the maxillary and man-
information is necessarily purely descriptive, it will be supplemented dibular regions of the first arch (see Fig. 36.2C–D). The second (hyoid)
by observations from lineage and genetic studies in mouse embryos, population gives rise to the otic ganglion and then migrates from
where the results are likely to be valid for all mammals, including prorhombomere B (which forms rhombomeres 3 and 4), into the
humans. The description of human development is derived from the second pharyngeal arch. The third (vagal) population has a more
following sources, which incorporate primary data by the authors, as extensive origin, from the neural folds caudal to the otocyst, i.e.
well as references to older primary source material: Patten (1968), prorhombomere C. These cells will contribute to the ganglia of the
Hamilton et al (1962), O’Rahilly and Müller (1987, 2001), Hinrichsen glossopharyngeal and vagal nerves, with the non-neuronal vagal crest
(1990), Steding (2009). References to experimental studies in the cells migrating into pharyngeal arches 3, 4 and 6, some of them con-
mouse are provided in the text. tinuing into the heart to contribute to the division of the cardiac
Evolution of the vertebrate head was made possible by the origin of outflow tract (Jiang et al 2000). The neural crest also gives rise to the
a novel cell population, the neural crest. Neural crest cells have the parasympathetic ganglia and parasympathetic postganglionic nerves in


potential to form connective and skeletal tissues in the head, and they the head and neck. For a full account of the neuronal contribution of
make major contributions to the skull. In mammalian embryos, cranial neural crest cells, see Chapter 17. In human embryos, histological
neural crest cells emigrate from the edges of the still-open cranial neural methods have revealed equivalent cranial neural crest cell origins
folds, unlike trunk neural crest cells and the cranial crest of other ver- and migration routes to those of the mouse (O’Rahilly and Müller
tebrates, which begin migration only after neural tube closure. Figure 2007).
36.1 shows stylized views of human embryos at an early stage of neural Caudal to the segmented region of the cranial neural tube, neural
crest migration (Fig. 36.1A) and at the end of the crest migration (Fig. crest cells from the occipital region (prorhombomere D/rhombomere
36.1B). It is important to note that these views do not show the neural 8) migrate with occipital myoblasts to form the hypoglossal cord, even-
crest cells themselves; they can be seen at the same developmental tually differentiating to form the connective tissue (neural crest) and
stages in mouse embryos in Figure 36.2. musculature (myoblasts) of the tongue. No sensory ganglia are formed
In the mouse, a lineage marker has enabled neural crest cells to be from the occipital neural crest in human embryos. The origin of the
traced from the stage at which they leave the neural epithelium through rhombomeres and brain regions in human embryos is shown in Figures
to their final locations in mature tissues. These studies show three sepa- 17.2 and 17.12.
rate populations of neural crest cells migrating from the cranial neural Ectodermal placodes appear as patches of columnar or pseudostrati-
folds; all these give rise to both neuronal and non-neuronal progeny fied epithelium within the otherwise squamous epithelium of the
(Jiang et al 2002; see Fig. 36.2). The first of these populations (trigem- surface ectoderm. Three pairs of placodes contribute to sense organs,


inal) originates from the diencephalic region of the forebrain, the mid- forming the olfactory epithelium, the lens and the otocyst, undergoing
brain, and prorhombomere A of the hindbrain, which subsequently morphogenesis to form a pit and then (for the lens and otic pits) a
divides to form the first two rhombomeres (see Figs 36.2A–B; see also closed cyst (vesicle). Epipharyngeal placodes are situated within the
Fig. 17.2). Those neural crest cells with a neuronal fate contribute to dorsal ectoderm of pharyngeal arches 2, 3 and 4; some of their cells
A B
Oropharyngeal membrane Closing otic vesicle
Amnion
Pharyngeal
part of foregut
Somite 4
Preotic sulcus
Optic vesicle
Otic sulcus
Somite 5
Heart
Heart
Closed neural tube
Notochord
Connecting stalk
Yolk sac wall
Brain regions Pharyngeal arches
Telencephalon Arch 1 (mandibular)
Diencephalon Primitive streak Arch 2 (hyoid)
Mesencephalon Arch 3
Rhombencephalon Arch 4
Fig. 36.1 Human embryos during the early stages of head development. The occipital–cervical boundary is indicated by an arrow. A, A sagittal section
of a stage 10 embryo, in which neural tube closure has begun in the future occipito-cervical region. B, A lateral view of a stage 12 embryo; the occipital–
cervical boundary between somites 4 and 5 is indicated by an arrow (see also Fig. 17.2). 605


Development of the heaD anD neck
606
4
noItceS
describes a loose cellular organization with a rich extracellular matrix,
A B in contrast to the sheets of simple epithelial tissue that form the outer
ectodermal and inner endodermal layers of early embryos. Prior to the
migration of neural crest cells from the edges of the cranial neural folds
to their final destinations, the only mesenchyme in the embryonic head
is ‘primary mesenchyme’, i.e. mesenchymal cells formed by epithelial–
mesenchymal transformation in the primitive streak. There is no lateral
plate mesenchyme in the head; all of the cranial mesenchyme is parax-
ial. Cranial mesenchyme derived from placodal, primary mesenchymal
and neural crest sources has specific distributions and specific deriva-
tives, and is not interchangeable.
The first transverse division to form in the early embryonic brain is
the preotic sulcus (see Figs 36.1A, 36.2A), which defines the boundary
between prorhombomeres A and B. This early division is of major func-
tional and organizational significance, since it separates the regions of
origin of the skeletogenic neural crest populations that make a major
contribution to the skull from those that form skeletal structures in
the neck (hyoid bone and larynx). During cranial neurulation, the
prorhombomeres undergo subdivision so that, by the time the brain
region of the neural tube closes, seven rhombomeres can be clearly
C D distinguished; the occipital region (adjacent to the four occipital
somites) remains unsegmented (see Fig. 36.2B). (By analogy with the
segmented rhombencephalon, it is also referred to as prorhombomere
D/rhombomere 8.) The segmental organization of the embryonic head
caudal to prorhombomere A is related to the expression of evolution-
arily conserved HOX genes (written Hox in the mouse) that have their
rostral boundaries at specific rhombomere divisions; they are also
expressed in the corresponding neural crest cells (reviewed by Santagati
and Rijli 2003; see also Fig. 17.16). Genetic experiments in the mouse


and other vertebrates have shown that skeletal patterning of the first
pharyngeal arch depends on the absence of Hox gene expression in the
neural crest cells migrating into it; skeletal patterning of the second arch
depends on the expression of Hoxa2. Investigation of Hox gene expres-
sion in arches 3–6 has not revealed clear skeletal patterning functions.
EMBRYONIC PHARYNX AND
PHARYNGEAL ARCHES
Fig. 36.2 Mouse embryo heads during the period of cranial neural crest The most cranial portion of the foregut, the embryonic pharynx, is the
cell migration. A–B, Scanning electron micrographs (A, dorsal view; scaffolding around which the face, palate and anterior neck structures
B, median section) of embryos near the start (4 somite pairs) and end are built. The development of this region from neural crest, paraxial
(18 somite pairs, interior view) of the period of neural crest cell migration. mesenchyme, surface ectoderm and foregut endoderm involves spatio-
At the 4-somite stage, the neural folds are convex and the hindbrain is
temporal coordination of cell movement, tissue growth and tissue inter-
divided into prorhombomeres A, B and C by the preotic (arrow) and otic
actions. As successive populations of neural crest cells migrate around
(arrowhead) sulci; at the 18-somite stage, the neural tube is closed and
the pharynx at progressively more caudal levels, five pairs of pharyngeal
the hindbrain is divided into seven rhombomeres (numbered) and the
arches are formed (numbered 1, 2, 3, 4 and 6 for comparative anatomy
unsegmented occipital region (oc). Rathke’s pouch is indicated by a small
reasons). This process is complete by stages 14–15 (5 weeks). Pharyn-
arrow on B. C–D, Lateral views of embryos at the 5- and 23-somite stage,
geal clefts (grooves) separate the arches externally; they are matched
respectively, carrying a permanent marker for neural crest cells and the


neural epithelium from which the trigeminal crest cells originate (blue internally by internal depressions, the pharyngeal pouches. Pharyngeal
stain). Trigeminal neural crest cells (nc) migrate as a veil-like mass arches are also known as branchial arches because of their evolutionary
beneath the surface ectoderm, originating as a continuous group from origin supporting the gills in the earliest vertebrates. Many of the
prorhombomere A, the midbrain and the caudal diencephalic region (d) of changes seen during development of the mammalian pharynx reflect
the forebrain, into the frontonasal region (fn) and the first arch (white lines the functional evolutionary origins of this region. Since the term
indicate the level of the migrating edge). After migration, frontonasal ‘branchial’ means ‘of the gills’, the term ‘pharyngeal arch’ will be used
neural crest cells (fn) cover the telencephalon and rostral diencephalon, in the following account of human embryology.
surrounding the eye (e); maxillary (mx) and mandibular (md) neural crest Each pharyngeal arch consists of an epithelial covering, ectoderm
populates the first pharyngeal arch; the trigeminal ganglion primordium (V) externally and endoderm internally, filled with mesenchyme that is
is also present. Hyoid neural crest cells from prorhombomere B have mainly of neural crest origin, with a contribution from primitive streak-
populated the hyoid arch and the primordium of ganglion VII/VIII, rostral derived mesenchyme (paraxial mesenchyme) (Fig. 36.3B; Table 36.1).
to the otocyst (ot); vagal crest cells from prorhombomere C are migrating The neural crest cells of each arch form a skeletal element and associ-
into arches 3 and 4, and starting to form the primordia of the
ated connective tissue; they also give rise to the walls of an aortic arch
glossopharyngeal and vagal ganglia, caudal to the otocyst. Other
blood vessel, which is lined with endothelium derived from angiogenic


abbreviations: d, diencephalon; hn, Hensen’s node; ht, heart; mb,
mesoderm. Paraxial mesenchyme also forms the muscle associated with
midbrain; p, pharynx; r1, rhombomere 1 of the hindbrain; t, telencephalon.
each pharyngeal arch. In mouse embryos, a cell lineage marker for
(A and B, With permission from Morriss-Kay GM, Wilkie AOMW 2005
mesoderm has shown that, by embryonic day 10.5 (equivalent to
Growth of the normal skull vault and its alteration in craniosynostosis.
human stage 13, or about 32 days), mesoderm-derived mesenchymal
J Anat 207:637–53. C and D, With permission from Jiang X, Iseki S,
cells have contributed both angiogenic and myogenic cells to the pha-
Maxson RE et al 2002 Tissue origins and interactions in the mammalian
skull vault. Dev Biol 241:106–16.) ryngeal arches (Yoshida et al 2008). Motor and sensory innervation
derives from arch-specific cranial nerves. For an overview of the organ-
ization of these tissues in the pharynx, see Figure 12.4; for their fate,
undergo epithelial to mesenchymal transformation, joining the under- see Table 36.1 and Figures 36.5–36.7. Since the organization of the
lying neural crest cell condensations to form sensory neuroblasts in the embryonic pharynx and related structures is similar in all vertebrate
cranial sensory ganglia V, VII, IX and X. Some cells from the otocyst and embryos, this phase has been termed ‘pharyngula’.
an adjacent placode similarly delaminate to contribute to the ganglion The first pharyngeal arch, unlike the other arches, possesses dorsal
of cranial nerve VIII (see Fig. 17.18). and ventral processes, and appears C-shaped in lateral view. It is also
The epithelial to mesenchymal transformation of some cells from termed the ‘mandibular arch’; however, this is not entirely appropriate
ectodermal placodes contributes a third component to the cranial mes- because its proximal (dorsal) end also contributes to maxillofacial


enchyme. It is important to note that the term mesenchyme simply and palatopharyngeal structures and to the middle ear. The second


embryonic pharynx and pharyngeal arches
607
63
Retpahc
A B
Pharyngeal pouch
Mandibular nerve
Meckel’s cartilage
Chorda tympani
Stapedial artery
Facial nerve
Arch 1
Reichert’s cartilage
Arch 2 Tympanic branch of
glossopharyngeal nerve
Arch 3
Glossopharyngeal nerve
Arch 4 Vagus, trunk
Arch 6 Superior laryngeal nerve
Sixth aortic arch artery
Dorsal aorta Recurrent laryngeal nerve
Fig. 36.3 Pharyngeal arch development. A, A scanning electron micrograph of a human embryo (stage 14/15), showing the right lateral aspect of the
pharyngeal arches; auricular hillocks are visible on arch two. B, The pharyngeal region (stage 15) viewed from the dorsal aspect. The whole left side and
part of the right side of the endodermal roof of the pharynx has been removed to show the grooves in its lateral walls and floor, and the nerves, arteries
and cartilages of the arches. The position of the right otocyst is shown as a clear oval. (A, Courtesy of Prof G Steding, Georg-August-University of
Göttingen, Göttingen, Germany.)
Table 36.1 Derivatives of the pharyngeal arches
Arch number Arch name Embryonic cartilage Cartilage derivative Muscle Nerve Artery
1 Mandibular Quadrate Incus Tensor tympani Trigeminal (V) First aortic arch artery
Meckel’s Malleus Muscles of mastication Mandibular division [transitory]
Anterior ligament of malleus Mylohyoid
Spine of sphenoid Anterior belly of digastric
Sphenomandibular ligament Tensor veli palatini
Genial tubercle of mandible
2 Hyoid Reichert’s Stapes Stapedius Facial (VII) Stapedial artery [transitory]
Styloid process of temporal bone Stylohyoid
Stylohyoid ligament Facial muscles, incl.
Lesser horn and upper part of body Buccinator
of hyoid bone Platysma
Posterior belly digastric


3 Third Greater horn and lower part of Stylopharyngeus Glossopharyngeal (IX) Common carotid artery, first
body of hyoid bone part of internal carotid artery
4 Fourth Thyroid cartilage Pharyngeal and extrinsic Vagus (X) Proximal part of subclavian
Corniculate cartilage laryngeal muscles, Pharyngeal branch artery on the right
Cuneiform cartilage levator veli palatini Arch of aorta between origins
of left common carotid and
left subclavian arteries
6 Sixth Arytenoid cartilages Intrinsic laryngeal muscles Vagus (X) Part between the pulmonary
Recurrent laryngeal branch trunk and dorsal aorta
becomes ductus arteriosus
on left, disappears on right
pharyngeal arch is termed the hyoid arch because of its contribution to is complete (first and second arch cartilages), the element extends dor-
the hyoid bone (and to other parts of the hyomandibular apparatus in sally until it comes into contact with the skull base lateral to the hind-
fishes). The third, fourth and sixth arches are not named. brain (Fig. 36.5). An arch cartilage may remain as cartilage, undergo
The mandibular arches, first seen at stage 10, grow ventromedially endochondral ossification or become ligamentous, or a combination
in the floor of the pharynx to meet in the median plane, forming the of these (Fig. 36.6).
ventral border of the early mouth above the cardiac (pericardial) promi- The first arch cartilage, Meckel’s cartilage, forms the embryonic lower
nence. The maxillary processes are not clearly visible as surface struc- jaw skeleton. After the mandible forms by intramembranous ossifica-
tures until stage 13; their enlargement coincides with the proliferation tion of the neural crest-derived mesenchyme lateral to it, Meckel’s car-
of the frontonasal mesenchyme to form the nasal swellings. The hyoid tilage degenerates but its sheath persists as the anterior malleolar and
arches appear at stage 11, the third arches at stage 12 and the fourth sphenomandibular ligaments. At its proximal end, endochondral ossi-


arches by stage 13. The sixth arch can only be identified by the arrange- fication forms two of the middle ear bones, the incus and malleus.
ment of the arch arteries and nerves, and by a slight projection on the These are homologous with the quadrate and articular bones of reptiles,
pharyngeal aspect. The floor of the pharynx is formed mainly by ventral and the joint between them is evolutionarily derived from the reptilian
apposition of the arches. The inferior border of the second arch grows jaw articulation. In reptiles, the quadrate forms from the caudal end
over the lower arches and encloses an ectodermal depression termed of the palatopterygoquadrate cartilage; the mammalian evolutionary
the cervical sinus (Figs 36.3A, 36.4). derivatives of the palatopterygoquadrate are thought to include part of
the greater wing of the sphenoid bone and the roots of its pterygoid
plates, in addition to the incus. The portion of Meckel’s cartilage that
SKELETAL ELEMENTS OF THE
extends from the mental foramen almost to the site of the future man-
PHARYNGEAL ARCHES dibular symphysis probably becomes ossified and incorporated into the
intramembranous mandibular bone; the remainder of the cartilage is
The skeletal and connective tissue elements of arches 1–3 are formed ultimately absorbed.
by condensation of neural crest-derived mesenchyme, which subse- The second arch cartilage, Reichert’s cartilage, extends from the
quently chondrifies in part or all of its length. Where chondrogenesis proximity of the otic capsule dorsally to the median plane ventrally. It


Development of the heaD anD neck
608
4
noItceS
A Pharyngeal pouches Arch 1
Arch 2
Pouch 1 Pouch 2 Pouch 3 Pouch 4
Arch 3
Arch 4
First
pharyngeal pouch Fused
occipital
Second sclerotomes
pharyngeal pouch
Otic
Incus capsule
Third
pharyngeal pouch Malleus Atlas
vertebra
Meckel’s cartilage
Fourth
pharyngeal pouch and Stapes
Hyoid bone
caudal pharyngeal complex
Reichert’s
Cricoid cartilage Thyroid cartilage cartilage
Fig. 36.5 The chondrocranium and arch cartilage derivatives, 7 weeks
B (stage 20).
Petrotympanic
Forming
fissure
tympanic membrane
Squamous portion of temporal bone
Anterior ligament
Sphenomandibular ligaments of malleus
Malleus
Zygomatic process
Incus
Caudal border of second arch Pouch endodermal epithelium Stapes
grows over more caudal arches plus neural crest mesenchyme
form pouch derivatives Tympanic ring
Meckel’s
Styloid process
cartilage
Mandible
C
External acoustic meatus
Tubotympanic recess
Platysma Palatine tonsil Mental ossicles Stylohyoid
ligament
Styloglossus
Thymus and parathyroid III Stylohyoid
Cervical sinus remnants muscle
Greater cornu
Parathyroid IV
Sternocleidomastoid and lateral thyroid Arch 1 and lower body
of hyoid bone
Arch 2
Cricoid cartilage
Arch 3
Arytenoid cartilage
Fig. 36.4 Pharyngeal pouch development. A, The arrangement of the Arch 4
early pharyngeal pouches: on the left, the internal aspect of the Thyroid cartilage
pharyngeal floor viewed from above; on the right, the external aspect of Lesser cornu and upper body of hyoid bone
the pharyngeal floor viewed from below. B, A coronal section of the left
Fig. 36.6 Derivatives of the pharyngeal arch cartilages in a 4–5-month


side of the pharynx at stage 18, showing changes to the pharyngeal
fetus.
pouches internally and pharyngeal clefts externally. C, A coronal section
of the left side of the pharynx at stage 19. See also Figure 36.18 for
further development.
of arches 1–3, the laryngeal cartilages associated with arches 4 and 6
(thyroid, cricoid and arytenoid) are mesodermal in origin.
ossifies to form the upper part of the body and lesser cornua of the
hyoid bone distally, and the styloid process proximally; between these
two bones, it becomes ligamentous to form the stylohyoid ligament. It MUSCLES OF THE PHARYNGEAL ARCHES
also gives rise to the most ancient of the three auditory ossicles, the
stapes (homologous with the rod-shaped columella auris of reptiles and The striated muscle of each arch (sometimes termed branchiomeric
birds). The cartilages of the third, fourth and sixth arches form only muscle) is derived from the cranial paraxial mesenchyme. Rostral to the
anterior neck skeletal structures: the lower part of the body and greater occipital region, the paraxial mesenchyme of the head is unsegmented,
cornua of the hyoid bone (third arch), and the laryngeal cartilages. and the suggestion that a segmental pattern of seven cranial somito-
Neural crest cells also give rise to ligaments, tendons and connective meres exists is not generally accepted today. In the occipital region of
tissue in these arches. However, in contrast to the NC-derived cartilages the head, epithelialization takes place to form four pairs of somites;


embryonic pharynx and pharyngeal arches
609
63
Retpahc
these are similar to those of the trunk, except that the first pair is rather to the base of the medial pterygoid process, which may be derived from
poorly defined. Myoblasts migrate from the paraxial mesenchyme to the dorsal cartilage of the first arch. All of these muscles are supplied
sites of future muscle differentiation and form pre-muscle condensa- by the mandibular nerve, the mixed nerve of the first arch. The maxillary
tions prior to the development of any skeletal elements. The pattern of division of the trigeminal nerve has no motor component, suggesting
primary myotube alignment for any one muscle is specified by the sur- that no muscles are derived from maxillary mesenchyme.
rounding neural crest-derived mesenchyme and is not related to the The muscles of the second arch migrate widely but retain their origi-
source of the myoblasts. The rate and pattern of muscle maturation are nal nerve supply from the facial nerve; migration is facilitated by the
closely associated with the development of the skeletal elements but early obliteration of part of the first pharyngeal cleft and pouch. Stape-
remain unattached until an appropriate time. Table 36.1 and Fig. 36.7 dius, stylohyoid and posterior belly of digastric remain attached to the
indicate the muscle masses of each arch, their innervation and their hyoid skeleton but the facial musculature, platysma, auricular muscles
derivatives in the adult. and epicranius all lose connection with it.
The muscle mass of the mandibular part of the first arch forms tensor The muscle masses from the third and fourth arches are adapted to
tympani, tensor veli palatini, mylohyoid, anterior belly of digastric, and form the musculature of the pharynx, larynx and soft palate. Stylopha-
the masticatory muscles (see Fig. 36.7 and Table 36.1). Tensor tympani ryngeus is a third arch muscle, cricothyroid develops in the fourth arch,
retains its connection with the skeletal element of the arch through its and the other laryngeal muscles are derived from the sixth arch. The


attachments to the malleus, and tensor veli palatini remains attached precise origin of the remaining palatal muscles and the pharyngeal
Pharyngeal arches:
Arch 1 Arch 2 Arch 3 Arch 4 Arch 6
Prechordal mesenchyme
Extraocular muscles
Muscles: levator palpebrae superioris; superior, medial
and inferior recti; inferior oblique
Nerve: oculomotor III
Muscle: superior oblique III IV
Nerve: trochlear IV
Muscle: lateral rectus
Nerve: abducens VI
Arch 3
Muscle: stylopharyngeus
Nerve: glossopharyngeal IX
VI
Chorda
tympani
branch
of VII
V
VIII
VII
Otocyst
IX
Arch 1
Muscles of mastication
Muscles: (temporalis, masseter, pterygoids), mylohyoid,
X
anterior belly of diagastric, tensor veli palatini
and tensor tympani Arch 4
Nerve: mandibular division of trigeminal V XII Muscles: cricothyroid, inferior
pharyngeal constrictor
Nerve: superior laryngeal
XI branch of vagus X
Arch 6
Muscles: intrinsic laryngeal muscles
(except cricothyroid)
Nerve: recurrent laryngeal
branch of vagus X
Fourth occipital somite
Trapezius and sternocleidomastoid muscles
(accessory nerve XI)
Diaphragm muscle
(phrenic nerve C3–5)
Arch 2 Occipital myotomes
Muscles of facial expression Ganglion Muscles: extrinsic and intrinsic
Muscles: buccinator, auricular muscles, occipitofrontalis, Myotome Fifth cervical lingual muscles
posterior belly of digastric, stylohyoid, stapedius (except palatoglossus)
and platysma Nerve: hypoglossal XII
Nerve: facial nerve VII
Fig. 36.7 The muscular derivatives of the prechordal mesenchyme, unsegmented paraxial mesenchyme and rostral somites.


Development of the heaD anD neck
610
4
noItceS
constrictors is uncertain. Palatoglossus, a muscle of the palate, is inner- Basilar artery Supraorbital artery
vated by the vagus via the pharyngeal plexus and may derive from the Superior cerebellar artery Stem of middle meningeal artery
lower arches.
Stem of future posterior cerebral artery Stapedial artery
Stem of hyoid artery
NERVES OF THE PHARYNGEAL ARCHES Internal carotid artery
Mesencephalic IV
The nerves associated with each arch arise from the adjacent hindbrain arteries
(see Fig. 36.7; see also Figs 12.4, 17.18). They are cranial nerves V
(trigeminal), VII (facial), IX (glossopharyngeal), X (vagal) and XI III VIII IX XI
(accessory). The motor nerves extend from the basal plate of the hind- V VII X
brain to innervate the striated muscle of the arches; they are termed Posterior XII
communicating
special branchial (visceral) efferent nerves because they innervate bran-
artery
chiomeric (pharyngeal) musculature. Sensory nerves extend peripher-
ally and centrally from cranial ganglia that are formed partly from Anterior
neural crest and partly from cells that delaminate from epipharyngeal choroidal artery
placodes; they convey general and special somatic afferent axons. Each Middle cerebral artery
arch is innervated by a mixed nerve, but the nerves of the first three
Anterior cerebral artery
arches also have a purely sensory branch that innervates the arch rostral
to its ‘own’ arch; this sensory nerve is called the pretrematic branch Primitive olfactory artery
because it extends rostral to the cleft or trema between the two arches Common stem of mandibular and maxillary artery Aorta Vertebral
(see Figs 36.3, 36.7). Hence, the nerves to the mandibular arch include artery
the mandibular division of the trigeminal nerve, which is mixed, and Pulmonary artery
Subclavian
the chorda tympani and greater petrosal nerves, purely sensory pretrem- External carotid artery artery


atic branches of the facial nerve. The maxillary branch of the trigeminal
Fig. 36.8 The arterial system of the head at stage 17 (approximately
and the tympanic branch of the glossopharyngeal are also considered
40 days).
to be pretrematic nerves. The ophthalmic branch of the trigeminal
nerve, which supplies the frontonasal area, is not an arch nerve; in
fishes, its ganglion is separate from the first arch nerve ganglion.
The vagus nerve supplies the fourth and sixth arches (see Fig. 36.7). common trunk persists as the root of the middle meningeal artery. More
The recurrent laryngeal branch initially loops under the sixth arch artery distally, the meningeal artery is derived from the proximal part of the
on both sides, but the asymmetric changes to the vascular system affect supraorbital artery. The maxillary branch becomes the infraorbital
the symmetry of this nerve. On the right, when the sixth aortic arch artery and the mandibular branch forms the inferior alveolar artery.
lateral to the right pulmonary artery degenerates, the recurrent laryngeal When the definitive ophthalmic artery differentiates as a branch from
nerve loops under the fourth arch-derived subclavian artery; on the left, the terminal part of the internal carotid artery, it communicates
it loops round the ductus arteriosus, (which is retained as the ligamen- with the supraorbital branch of the stapedial artery, which distally
tum arteriosum in the adult). Further details of cranial nerve develop- becomes the lacrimal artery. The latter retains an anastomotic connec-
ment and composition are provided in Chapter 17. tion with the middle meningeal artery. The dorsal stem of the original
second arch artery remains as one or more caroticotympanic branches
of the internal carotid artery.
BLOOD VESSELS OF THE PHARYNGEAL ARCHES The fourth aortic arch on the right forms the proximal part of the
right subclavian artery, whereas the corresponding vessel on the left
The aortic arches initially develop by vasculogenesis, soon after neural constitutes the arch of the definitive aorta between the origins of the
crest cells have invaded the early pharyngeal arches. Mesoderm-derived left common carotid and left subclavian arteries.


angiogenic mesenchyme forms the endothelial lining of the vessels, and The sixth aortic arch is associated with the developing lung buds.
neural crest contributes to the outer layers of the walls (Jiang et al 2000, Initially, each bud is supplied by a capillary plexus from the aortic sac;
Yoshida et al 2008). The first aortic arch artery is part of the original as the sixth aortic arch develops, it becomes the channel for blood from
vascular circuit that links the aortic sac of the heart to the paired dorsal the aortic sac to the developing lung buds as well as to the correspond-
aortae, blood returning to the heart via the allantoic, vitelline and ing dorsal aorta, the latter being the main channel. Soon after forma-
common cardinal veins (see Fig. 13.1C). As the heart descends relative tion of the sixth aortic arch, the outflow tract of the heart is divided by
to the forebrain and other rostral structures, the aortic sac (ventral aortic an influx of neural crest cells, which form the spiral aorticopulmonary
root) gives rise to paired aortic arches at successively more caudal levels, septum (Jiang et al 2000); this separates the aortic sac into the pulmo-
each of which passes laterally on each side of the pharynx to join the nary trunk and ascending aorta. The part of the sixth aortic arch
dorsal aortae. The dorsal aortae are not invested by neural crest cells, between the pulmonary trunk and the dorsal aorta becomes the main
and nor are the more distal (cranial) parts of the carotid arteries, which vascular channel on the left, and is defined as the ductus arteriosus
form by angiogenesis. The whole complement of aortic arches never when the equivalent vessel on the right side is lost. The right dorsal
coexists – the first aortic arch degenerates through remodelling of the aorta caudal to the right subclavian artery also degenerates, leaving
cranial arteries before the sixth is formed. the left dorsal aorta as the definitive descending aorta (Fig. 36.9B). The
When the first and second aortic arch arteries begin to regress, the ductus arteriosus remains the main channel for blood to pass from the


supply to the corresponding pharyngeal arches is derived from a tran- right ventricle to the descending aorta until the lungs and their associ-
sient ventral pharyngeal artery, which terminates by dividing into man- ated blood vessels expand at birth. After birth, the ductus arteriosus is
dibular and maxillary branches. The second aortic arch artery also functionally closed by contraction of the circular muscle of the tunica
degenerates, remaining only as the stem of the stapedial artery. The early media (p. 922), leaving a ligamentous remnant, the ligamentum arte-
vessel anastomoses with the ventral pharyngeal artery, passing, as it riosum (Fig. 36.9C).
does, through the mesenchyme of the stapedial cartilage, which con-
denses around it, forming the foramen of the stapes. At this stage, the
stapedial artery possesses three branches – mandibular, maxillary and PHARYNGEAL ECTODERM AND CLEFTS
supraorbital – which follow the divisions of the trigeminal nerve (Fig.
36.8). The mandibular and maxillary branches diverge from a common Surface ectoderm lines the roof of the embryonic pharynx up to and
stem. including Rathke’s pouch (see Figs 17.13–17.14). It also completely
Further development of the third, fourth and sixth aortic arches (Fig. covers the first arch, including the lateral walls and floor of the pharynx,
36.9) produces the main arteries to the head and the great vessels unlike the more caudal arches, which are lined with pharyngeal endo-
arising from the heart. The common carotid arises from an elongation derm. The external surface ectoderm of the first arch ultimately pro-
of the aortic sac, and the third arch artery becomes the proximal part duces the keratinized stratified squamous epithelium of the epidermis,
of the internal carotid artery. The external carotid artery arises as a including hair follicles, sweat and sebaceous glands, and the specialized
sprout from the common carotid; it incorporates the stem of the ventral epithelium of the vermilion of the lip. Within the oral cavity, first arch


pharyngeal artery, and its maxillary branch communicates with the ectoderm forms the mucous membranes of the internal surface of the
common trunk of origin of the maxillary and mandibular branches of lips and cheeks, the palate, the anterior part of the tongue, the epithelial
the stapedial artery and annexes these vessels. The proximal part of the components of the salivary and mucous glands, and the enamel organs


embryonic pharynx and pharyngeal arches
611
63
Retpahc
A I B Internal carotid artery
External carotid artery Left common carotid artery
II
Ventral aortic root Right common carotid artery Left aortic arch IV
between aortic Ductus arteriosus
arches III and IV III Brachiocephalic trunk
Vertebral
Right IV artery
pulmonary artery Right
subclavian Left
VI artery subclavian
3–7 artery
Internal
3 thoracic
artery
4 Ascending 8 Left
aorta
Vertebral artery 5 pulmonary
6 Dorsal aortic root P truu nlm konary artery
Right Superior
subclavian artery 7 Seventh dorsal intercostal
intersegmental artery
Degenerating 9
Internal 8 artery eighth segment Left dorsal
thoracic artery Superior of right dorsal aortic root
aortic root
9 intercostal artery
10 F brir as nt cin ht e frr oc mostal 10 Dorsal aorta
the dorsal aorta
11 11
C Aortic arch III Ventral aortic root between
aortic arches III and IV
Internal carotid artery
(aortic arch III) External carotid artery Aortic arch IV Ventral aortic root between
aortic arches IV and VI
Common Aortic arch VI
Left vertebral artery
carotid artery Seventh dorsal intersegmental artery
Dorsal aortic root segments 3–7
Ascending cervical artery
Right dorsal aortic Dorsal aortic root segments 8, etc. Longitudinal anastomoses
root (segments 3–7) Left subclavian artery
Right
Superior intercostal artery
subclavian artery
Right aortic arch IV
Brachiocephalic trunk 1
Left dorsal aortic root
(segments 3–7)
Left aortic arch IV 2
3–7
8
9
3
10
11
4
Ligamentum arteriosum Internal thoracic artery
Fig. 36.9 Aortic arch arteries and their derivatives.
of the developing teeth (see Figs 36.14–36.15). The first pharyngeal cleft mesenchyme that develops into the sternocleidomastoid and trapezius


is obliterated ventrally; its dorsal end deepens to form the external muscles. Caudally, the smaller epipericardial ridge separates the sinus
acoustic meatus, including its ceruminous glands and the outer surface from the pericardium. Fusion of the hyoid arch with the cardiac eleva-
of the tympanic membrane (see Fig. 36.4B,C). Three auricular hillocks tion covers the cervical sinus, excluding the third, fourth and sixth
form on the first and second arches, each side of the first pharyngeal arches from contributing to the skin of the neck; it also results in
cleft, beginning at stage 15; they form the auricle of the external ear platysma muscle, bounded both superficially and deep with superficial
(p. 659). fascia, passing along the neck to the anterior thoracic wall.
The external contours of the arches and clefts are modified as the
skeletal and muscular elements develop. During the fifth week, the
second, third and fourth pharyngeal clefts form the rostral and caudal PHARYNGEAL ENDODERM AND POUCHES
parts of a retrohyoid depression, the cervical sinus (see Fig. 36.4C).
Cranially, the sinus is bounded by the hyoid arch; dorsally, by a ridge The four pharyngeal pouches appear in sequence craniocaudally
produced by ventral extensions from the occipital myotomes and by during stages 10–13. The rostral pharynx is broad and dorsoventrally


Development of the heaD anD neck
612
4
noItceS
compressed (see Fig. 36.18A). Laterally, the endoderm of the pouches lomandibular fusion. The period from 7 to 8 weeks is the final period
approaches the ectoderm of the pharyngeal clefts to form thin closing of major morphogenetic change in facial development. In addition to
membranes (see Fig. 36.4). The approximating ectoderm and endo- formation of the mouth and cheeks, it is marked by further narrowing
derm between the first cleft and pouch form the outer and inner surfaces of the nasal region and philtrum, and ascent of the ears. By stage 20,
of the tympanic membrane. The ventral end of the first pouch is obliter- the face is recognizably human, although differential growth will con-
ated, but its dorsal end persists and expands as the head enlarges. This, tinue to bring about changes in proportion and relative position of the
together with the adjoining lateral part of the pharynx, possibly with a features.
contribution from the dorsal part of the second pharyngeal pouch, The contribution made by the frontonasal process to surface
constitutes the tubotympanic recess. The recess forms the middle ear epithelial derivatives extends from the skin of the forehead, over the
cavity, the pharyngotympanic tube and their extensions. Expansion of supraorbital and glabellar regions, including the upper eyelid and con-
the middle ear cavity around the ear ossicles occurs late during fetal life, junctiva, to the external aspect of the nose and philtrum of the upper
by breakdown of the mesenchyme around the ossicles so that the cavity lip. During later development, the maxillary nerve invades the skin of
comes to surround them, except at their attachments to the tympanic the philtrum and nasal alae, so that the trigeminal nerve distribution
membrane and fenestra ovalis (fenestra vestibuli, oval window). does not completely coincide with the tissue origins (compare Figs
The ectoderm of the pharyngeal clefts and the endoderm of the 36.10F and 36.11).
pouches become increasingly separated by mesenchyme. The blind


recesses of the second, third and fourth pouches are prolonged dorsally
and ventrally as angular, wing-like diverticula (see Fig. 36.18); the NASAL CAVITIES AND PALATE
pouch endoderm thickens and evaginates into localized neural crest-
derived mesenchymal condensations. Further development of the After formation of the nasal pits, the original olfactory placodal cells
second, third and fourth pouches is summarized in Figure 36.18 and lie deep within the pit, adjacent to the underlying telencephalon. They
described in the associated text. differentiate into olfactory neuroblasts, supporting (sustentacular) cells
Rarely, failure of normal modification of the pharyngeal clefts and and stem cells. Neurites begin to extend from the olfactory neuroblasts,
pouches may lead to the formation of fistulae, external or internal reaching the olfactory region of the telencephalon by stage 16 (sixth
sinuses, and cysts (see Commentary 2.2). Lateral cervical cysts are now week). The earliest pioneer neurites cross a mesenchyme-filled gap
considered to be lymphoepithelial in origin. between the placode and the brain. The remaining placodal cells dif-
ferentiate into columnar supporting cells, rounded basal cells and, by
invagination, the duct-lining and secretory acinar cells of the glands of
FACE, NASAL CAVITIES AND PALATE, ORAL Bowman. Basal infiltration by lymphocytes is a relatively late event.
Once the nasal cavities have formed, the roof of the oral cavity is
CAVITY AND TONGUE
regarded as the primitive palate (not to be confused with the primary
palate, which forms from the most rostral part of the primitive palate).
FACE Each nasal cavity has an arcuate shape, extending upwards over the
primary palate to the differentiating olfactory epithelium and then
By stage 12, migration of the most rostral neural crest cell population down again towards the oral cavity, from which it is separated by an
is complete and the sequence of morphogenetic changes that will form epithelial choanal membrane (see Fig. 17.13). Towards the end of stage


the face begins (Fig. 36.10). Neural crest cells have populated the man- 18, the choanal membranes degenerate to form internal openings, the
dibular arch and its maxillary extension, and formed the frontonasal choanae, lateral to the primary palate; the nasal cavities are now a duct
mesenchyme that covers the telencephalon and caudal diencephalon from the external environment to the oral cavity. Within the nasal
(see Fig. 36.2D). They also contribute to the primordium of the trigemi- cavity, the ectodermal lining and subjacent mesenchyme differentiate
nal nerve, whose first fibres begin to extend at stage 13. The three divi- to form the mucous membrane of the nasal vestibule, conchae and
sions of the trigeminal nerve will provide sensory innervation to the paranasal sinuses, and the olfactory epithelium.
frontonasal, maxillary and mandibular parts of the face. At stage 17, the internal aspect of each maxillary process begins to
Localized mesenchymal proliferation results in the formation of four bulge into the oral cavity as a palatal process; the palatal processes are
paired processes: the medial and lateral nasal, maxillary and mandibu- the primordia of the secondary palate (Fig. 36.12). The tongue is well
lar processes. The lateral and medial nasal processes surround the nasal developed by this stage, and its domed form fills the space between the
placodes, causing them to sink deep to the surface, forming the nasal nascent palatal shelves laterally and the primitive palate above. The
pits. The two medial nasal processes approach each other to form the mandible is still short, relative to the maxillary region, and does not
nasal septum between them and extend downwards to form the pre- extend as far as the primary palate. Further growth of Meckel’s cartilages
maxillary component of the upper lip and jaw and the primary palate. brings the mandibular region and tongue forwards, extending to a posi-
Concomitant with formation of the nasal processes, proliferation of the tion below the primary palate. At the same time, the (secondary) palatal
maxillary mesenchyme forms the maxillary processes. These make processes continue to grow, projecting vertically downwards on either


contact with the medial and lateral nasal processes at stages 16–17 (see side of the tongue. At stage 23 (56–57 days), the tongue descends and
Fig. 36.10E). Fusion of the maxillary processes with the medial nasal the palatal shelves rotate, bringing the shelves to a horizontal position
processes unites the premaxillary and maxillary parts of the upper jaw above the tongue (Fig. 36.12B). The rapidity of the process of shelf
and lip; failure of this process on one or both sides causes unilateral or elevation is caused, at least in part, by swelling of the palatal mesen-
bilateral cleft lip (see Fig. 36.17). Superiorly, this fusion closes the cleft chyme due to accumulation and hydration of hyaluronan in the extra-
at the lower edge of the nasal pits, completing the future nostrils. Fusion cellular matrix (Ferguson 1991). This occurs during a period of
of the maxillary with the lateral nasal processes is a much simpler continuous growth in head height but almost no growth in head width.
process and rarely gives rise to abnormality. At stage 16, the epithelium This latter factor is important because, if palatal shelf elevation is
of the groove between these fusing processes thickens to form the lac- delayed so that it occurs during a period of growth in facial width, the
rimal lamina, the primordium of the lacrimal system. At stage 19, it unfused processes may be unable to make contact in the midline, result-
separates from the surface ectoderm, forming the lacrimal cord beneath ing in a cleft palate (see Fig. 36.17). Other factors affecting palatal
the surface. The cord becomes canalized to form the nasolacrimal duct closure include the growth in length of Meckel’s cartilages and the
in the tenth week (de la Cuadra-Blanco et al 2006). The original site of change in position of the maxillae relative to the anterior cranial base;
the lacrimal lamina marks the lateral division between frontonasal and both of these have the effect of lifting the head and upper jaw away
maxillary contributions to the face, the territories whose sensory nerve from the mandible during weeks 9 and 10, facilitating withdrawal of


supply is from the ophthalmic and maxillary divisions of the trigeminal the tongue from between the palatal shelves and hence creating space
nerve, respectively (Fig. 36.11). for their elevation. Mouth opening, tongue protrusion and hiccup
At the start of facial development, the stomodeal opening extends movements have also been noted at this time, and it may be that these
across the whole width of the embryonic head. A wide mouth is main- movements and their associated pressure changes assist palatal shelf
tained until differential growth brings the eyes and the lateral parts of elevation. Generally, palatal shelf elevation occurs slightly later in
the maxillary–mandibular structures from the sides to the front of the female embryos than in males.
face (stage 18 to stage 23, 7–8 weeks). Although differential growth Midline fusion of the two palatal shelves involves adherence and
makes the mouth opening proportionately smaller, progressive fusion breakdown (by apoptosis) of the apposed epithelial surfaces. They also
of the lateral regions of the maxillary and mandibular processes also fuse with the posterior border of the primary palate, except over a small
makes an important contribution to decreasing the width of the mouth median area, where a nasopalatine canal maintains connection between
and to forming the cheeks. Differences in mouth width within the the nasal and oral cavities for some time and marks the future position
human population are mainly due to variation in the extent of maxil- of the incisive fossa. During the period of palatal shelf development, a