PHYSIOLOGY OF DEGLUTITION
Definition and Purpose of Swallowing
Swallowing is usually defined as a reflex, coordinated set of
muscle contractions which act to propel food from the mouth into
the esophagus. This is accurate as to the alimentary function, but
leaves out another vital role for this behavior: Swallowing is
also a protective reflex of the upper airway, to prevent the entry
of saliva or ingested liquids into the trachea. This role is
indicated by the fact that squirting water into the larynx will
initiate swallowing in several different species, and only certain
areas in the larynx are sensitive to water in this way (Storey,
1968).
By making audio recordings from a throat microphone, Lear et
al. (1965) were able to determine the frequency of swallowing at
different times over a 24-hour period. The results are shown in
Table I:
Table I. Average number of swallows recorded in humans during
day and night. (From Lear et al., 1965).
_________________________________________________
While eating
200
Awake, between meals
345
Asleep (mostly before waking)
Total
45
590
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Apparently, we do most of our swallowing between meals, for
the purpose of clearing the airway of saliva and liquids taken
into the mouth. The process of swallowing a liquid once it has
reached the posterior pharynx is similar to swallowing a semisolid
bolus of food, but the events leading up to that point differ
substantially.
Three Phases of Swallowing
While mastication is a rhythmic behavior, occurring in cycles
and coordinated by a central pattern generator, deglutition
happens as a unitary event, triggered by appropriate conditions.
Like mastication, swallowing may be initiated either voluntarily
or reflexly. It too involves both striated and smooth muscles, and
so may not be classified either as a "somatic" or "autonomic"
reflex.
The act of swallowing is often divided into oral, pharyngeal
and esophageal phases, based on anatomy and the sequence of movements which take place. The first phase is often described as
"voluntary," rather than reflex, since we can swallow whenever
there is something in the mouth. (However, not much thought may go
into initiating a swallow while eating.) The events which occur in
each phase are the following:
Oral Phase
The tip of the tongue forms a bolus of food, which is placed
in the midline. The lips are then closed, the jaw is elevated and
the teeth may come into occlusal contact. At this point the soft
palate is raised, sealing off the nasal cavity from the mouth.
(You can tell this is an early event by swallowing and then trying
to breathe.) The tip of the tongue presses firmly against the hard
palate, just behind the incisors. The tongue then rolls backward
on the hyoid bone, pressing against the palate and forcing the
bolus back.
Pharyngeal Phase
The bolus, somewhat wetted with saliva, contacts the mucosa
of the fauces and pharynx. Respiration stops. (This is the "apnea
of deglutition".) The larynx is elevated, and the glottis is
closed, sealing off the airway from the pharynx. The bolus tips
the epiglottis backward, and the epiglottis acts as a chute,
guiding the bolus into the esophagus. (The epiglottis is not essential, however; respectable swallows can be performed after the
epiglottis has been removed.)
The pharyngeal constrictor muscles now contract in a wave from
superior to inferior, forcing the bolus into the esophagus. The
pressure in the pharynx at this point may reach 100 mm Hg. As the
bolus reaches the posterior pharynx, the hypopharyngeal, or
superior esophageal sphincter relaxes, permitting the bolus to
enter the esophagus.
The oral and pharyngeal phases together take about one second
to occur.
Esophageal Phase
After the bolus passes through it, the hypopharyngeal
sphincter actively closes, to prevent reflux into the pharynx. A
peristaltic wave then begins at the upper end of the esophagus.
The wave moves downward, taking 7-9 seconds to travel the length
of the esophagus.
Before the wave, and the bolus, reach bottom, the larynx descends,
and the airway is reopened (oronasal passage and glottis). The
tongue moves forward again, and respiration resumes.
Over twenty individual muscles contribute to each swallow, in
a carefully coordinated sequence, or pattern. Electromyographic
recordings have been obtained in several different muscles in the
dog during a swallow, as shown in Figure 6. The sequential
activation of muscles from superior to inferior can be seen.
Although some slight reductions may occur before the increases in
muscle activity seen, the main mechanism for moving food through
the mouth is by a pressure wave.
The escape routes are sealed off
and and pressure is increased locally, propelling the bolus
forward. A sequence of muscle activation such as that shown is
called a fixed-action pattern, and is seen in motor control
systems throughout the animal kingdom. We shall see below how this
pattern is triggered and organized in the nervous system.
Drinking
The above description of swallowing applies to solid or
semisolid foods. During drinking of liquids, we use a different,
but also stereotyped, pattern of movements. At first, when the
liquid is brought in contact with the lips, suction is created by
retracting the tongue and maintaining a seal between the tongue
and palate. The posterior part of the tongue is then depressed,
allowing the fluid to run into the pharynx. The jaw is closed, and
swallowing begins. The esophagus fills, the fluid taking less than
one second to reach the bottom. Then a wave of peristalsis moves
to the bottom in seven or so seconds, and the gastro-esophageal
sphincter opens.
Failure of either the hypopharyngeal or gastroesophageal
sphincters to open is called "achalasia" (usually applied to the
lower sphincter). If untreated, this condition may lead to accumulation of meals in the esophagus and reflux into the pharynx
while lying horizontally (Davenport, 1982).
The Infant Swallow
Prior to eruption of the deciduous teeth, the principal form
of nutrition in neonates is by suckling. Considerable intake of
amniotic fluid by this method also takes place in the fetus
(Dellow, 1976). Infants are able to swallow at the same time as
suckling, with the jaws apart and the tongue slightly protruded.
The forces for propulsion of fluid toward the pharynx are derived
from the facial muscles - the orbicularis oris, buccinator,
risorius, etc. - and from vigorous thrusting with the tongue, with
little involvement of the mandible or elevator muscles.
This pattern of swallowing may persist into adolescence,
resulting in tongue thrust and protrusion of the anterior teeth
(Barrett and Hanson, 1974). The reason for failure of the adult
swallow to develop is unclear. Various etiologies have been
proposed, from improper bottle feeding (Straub, 1960) to childhood
respiratory diseases which make it painful to swallow using the
pharyngeal muscles. The tongue-thrust swallow pattern is treated
by guided practice while looking in a mirror. The goal is to learn
to swallow without moving anything but the larynx. Significant
improvements in the swallowing habit can be made by this method,
helping to ensure that any concurrent orthodontic treatment will
succeed.
The Muscles of Deglutition
Examples of the major muscles and their cranial nerve
supplies are shown in Figure 7. The sequence of activation of the
various muscles during each phase of swallowing is roughly
indicated by the Arabic numberals. With the exception of the
hypoglossal nucleus, the wave of activity sweeps down the
brainstem nuclei in order during the swallow, producing the
stereotyped response. This pattern of activity is generated by a
system of interneurons in the medulla called the swallowing
center. Coordinated signals from this region sequentially activate
the brainstem motor nuclei.
It is possible to identify the swallow pattern of excitation
of various muscles by recording their electromyographic activity
(Doty et al., 1967; Storey, 1968) or the activity of associated
motor axons (Sumi, 1970). In the latter case, the pattern of nerve
activation has been shown to persist after the muscles have been
denervated or paralyzed with curare (Miller, 1972). This unaltered
sequence of nerve activity (called fictive swallowing) is
convincing evidence for the role of a central pattern generator.
The Esophagus
The muscles of the upper one-third of this structure in
humans are striated, those of the middle third are striated and
smooth, and the bottom third are smooth. In some animals, dogs and
mice, for instance, the entire esophagus is striated. The
gastroesophageal sphincter is not morphologically specialized, but
it behaves like a sphincter, remaining contracted until a swallow
occurs.
Esophageal peristalsis consists of a wave of contraction
which propels the bolus of food along (Davenport, 1982). (This is
to be contrasted with intestinal peristalsis, which is a wave of
relaxation followed by a wave of contraction.) Esophageal peristalsis travels at 2-4 cm/sec. The pressure wave is generated by
sequential firing of vagal and glossopharyngeal motor fibers, superimposed on the activity of the intrinsic esophageal nerve
plexuses. Continuity of the muscle is not necessary; the esophagus
can be transected without interfering with peristalsis. However,
the efferent nerve supply is necessary. Vagotomy results in an
uncoordinated contraction of various parts of the esophagus.
Receptor Areas for Swallowing
Although it may be initiated centrally, swallowing also
requires sensory input from the periphery, i.e. stimulation of the
receptor areas in the mouth and pharynx. Wassilieff (1888)
reported that swallowing in humans was made impossible by
cocainization of the layngeal and pharyngeal mucosa. Pommerenke
(1928) applied mechanical stimuli with a glass rod to various
parts of the oral cavity in 126 student subjects and reported the
percentage of tests resulting in swallows (Table II). (Some
subjects' throats were quite sensitive to touch, and some were so
insensitive they could be clamped with a hemostat!) The result of
this study was that light touch was the most effective in
provoking swallowing when applied to the anterior pillar, and
heavy touch was most effective on the posterior pharynx.
Apparently, the mechanical contact of food in these areas acts as
a trigger for swallowing. Both the anterior pillar and posterior
pharynx are innervated by cranial nerves IX and X.
Table II. Sensitivity of various areas of the mouth and
pharynx for triggering swallowing. Percentage of light
and heavy contacts resulting in swallows shown, as well
as percent not responding with swallows. (From
Pommerenke, 1928.)
__________________________________________________________
Light
touch
Heavy
touch
No
response
Base of tongue
36.6
1.3
62.1
Deep post. pharynx
18.8
50.5
30.7
Post pharynx
27.8
47.5
24.7
Soft palate
4.0
15.2
80.8
Tonsil
28.6
19.1
52.3
Uvula
30.4
1.6
68.0
Post. pillar
30.4
28.0
41.6
Ant. pillar
60.3
16.7
23.0
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In a subsequent study, Storey (1968) recorded
electromyographic activity in three of the muscles of swallowing
during application of distilled water to the larynx of cats. This
treatment reliably caused swallowing, identified by the sequential
activation of the mylohyoid, thyroarytenoid and inferior constrictor muscles. The stimulus in this case was not mechanical, since
isotonic saline did not produce the reflex.
This response to water application has also been found in the
lamb, guinea pig and rabbit (Dubner et al., 1978), and is mediated
through the superior laryngeal nerve, a branch of X. The most
sensitive areas of the larynx for the water response are around
the epiglottis. There are both free nerve endings and taste
receptors in this region, so either could be the water receptors.
These receptors are also readily stimulated by saliva, which is
98% water, compared to plasma which is only 91% water. Thus, when
food wetted with saliva contacts the area around the epiglottis,
this acts as a powerful chemical stimulus for swallowing.
Sensory Pathways
Afferent activity in either the IXth or Xth cranial nerves
can act to trigger swallowing. The most reliable nerve for
initiating swallowing is the superior laryngeal branch of X. The
frequency of afferent stimulation has a strong effect on whether
or not a swallow will occur, but does not affect either the timing
or strength of the swallow. In humans, unilateral or bilateral
section of the glossopharyngeal nerve does not interfere with
swallowing (Ballantine et al., 1954), but section of the vagus
prevents it.
The afferent fibers of swallowing receptors enter the CNS in
the tractus solitarius and terminate in the nucleus of the tractus
solitarius (Jean, 1990). Swallowing can also be produced by
stimulation of part of the frontal cortex (Sumi, 1969); the pathway from this area terminates in the nucleus of the tractus
solitarius.
The Gag Reflex
The pharyngeal or gag reflex is triggered by mechanical
stimuli applied in a similar region of the pharynx to that which
triggers swallowing. This reflex consists of contraction of the
pharyngeal constrictors in response to touching the posterior wall
of the pharynx, and though harmless, often occurs in dental
practice. The afferent pathway for the gag reflex is the
glossopharyngeal nerve, and the efferent motor nerves are the
glossopharyngeal and vagus nerves.
Location of the Brainstem Swallowing Center
There are actually two swallowing centers, one on each side
of the brain stem, controlling the muscles its own side. In a
careful series of transection experiments Doty et al. (1967) found
the active networks to be located in the medial brainstem, between
the posterior pole of the facial nucleus and the rostral pole of
the inferior olive. This is shown in Figure 9. Electrical
recordings were obtained in several muscles participating in
swallowing, initiated by stimulating the superior laryngeal nerve.
Transections or hemisections above A-13 just started to interfere
with the tongue muscles innervated by the hypoglossal nerve. Those
below A-63 just affected components mediated by the trigeminal
nerve, such as the mylohyoid.
Further detailed studies by Jean (1972, 1978) and others
analyzed the activity of neurons within the central pattern generator, and showed that such neurons are located only in two
regions of the medulla: (1) a dorsal region including the nucleus
of the tractus solitarius and (2) a ventral region corresponding
to the lateral reticular formation above the nucleus ambiguus.
These are the two areas where the entire pattern of swallowing is
generated and coordinated. Activity from these interneurons sequentially excites the motor nuclei of the swallowing muscles,
producing the pattern of swallowing. The nucleus of the tractus
solitarius is strongly involved, which is interesting since this
is the location of second-order neurons in the taste sensory
pathway (Scott and Yaxley, 1989). This is likely to be the site of
triggering of the swallow reflex by water stimulation around the
epiglottis.
A schematic outline of the swallowing system is shown in the
next figure. Either oral or voluntary CNS inputs may trigger
swallowing in the generator neurons. These then excite the
switching neurons, which in turn excite neurons in the various
motor nuclei involved in swallowing.
The swallowing center, like the masticatory pattern generator, produces a complex coordinated set of outputs to several
cranial motor nuclei. This occurs either under voluntary control
or in response to appropriate intraoral stimuli. The pattern generator for deglutition, like the masticatory center, is located in
the medial medulla. Mastication is rhythmical; swallows occur one
at a time. Sensory inputs may interrupt the chewing cycle but are
unlikely to interfere with swallowing. The entire pattern of
swallowing is necessary to fulfill a basic function, and loss of
any part of the system can be life-threatening.
Disorders of Swallowing (Dysphagia)
Neurological disorders
- Stroke
- Parkinson’s
- Huntington’s
- Infections (rabies, tetanus)
- Amyotrophic lateral sclerosis
- Multiple sclerosis
- Neoplasms
- Neuropathies
a. recurrent laryngeal neuropathy
b. diabetes
c. carcinoma
Mechanical disorders
- Removal or reconstruction of oral, pharyngeal or
laryngeal structures during surgery for cancer
- Acute inflammation
a. laryngitis
b. pharyngitis
c. chemical inflammation
Macroglossia
- Secondary to radiotherapy or surgery of the tongue
- due to hypothyroidism.
Surgery
- Especially surgical resection for carcinoma of the
tongue; laryngectomy; tracheotomy tubes.
- Most patients have significant dysphagia
Next we shall examine the coordination of speech, and the
overlapping of neuromuscular functions with those of mastication
and deglutition.