Motor innervation of the cricopharyngeus muscle
by the recurrent laryngeal nerve
CAROL SMITH HAMMOND, PAUL W. DAVENPORT,
ALASTAIR HUTCHISON, AND RANDALL A. OTTO
Departments of Communication Processes and Disorders, Physiological Sciences, and Pediatrics,
University of Florida, Gainesville, Florida 32610; and Department of Otolaryngology,
University of Texas at San Antonio, San Antonio, Texas 78285
swallow; esophageal reflux; glottis
THE LARYNGEAL-PHARYNGEAL COMPLEX
is known to be
activated during swallowing (3–5, 9, 13, 15). Recurrent
laryngeal nerve (RLN) dysfunction has been associated
with laryngeal dysfunction, although swallowing dysfunction in patients with RLN paresis (8, 21) has been
reported. The cricopharyngeus muscle (CPM) is the
most inferior pharyngeal muscle and it inserts on the
lamina of the thyroid cartilage and the lateral aspects
of the cricoid cartilage. The lower fibers of the CPM
initially transverse the dorsal pharynx, connecting to
these cartilages, and then distal to the cartilage border
the CPM fibers transition to be continuous with the
circular fibers of the esophagus (24). The upper esophageal sphincter (UES) is formed by the CPM and its
insertions on the thyroid and cricoid cartilages. The
CPM and the cartilages comprise the anterior aspect of
the sphincter while cervical vertebrae form the posterior aspect (3, 18).
Previously, the CPM has been reported to be innervated by the pharyngeal plexus, formed from branches
of the glossopharyngeal, vagus, and sympathetic nerves
(24). The RLN is commonly reported to supply the
muscles of the larynx, except the cricothyroid and the
mucous membrane of the larynx below the vocal folds
and the mucous membrane of the upper part of the
trachea (24). Lund and Ardran (12) concluded that
there was no evidence that the RLN supplied the UES.
However, Ekberg et al. (8) and Shin (21), using cineradiographic investigations of patients with suspected
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paresis of the RLN, demonstrated that impaired laryngeal and pharyngeal functions highly correlated with
swallowing dysfunction. Although it is generally accepted that RLN paralysis results in incomplete closure
of the larynx, glottic closure during swallowing was not
affected by RLN section (22, 23).
Anatomic studies have suggested that the RLN also
supplies the CPM. Rustad and Morrison (16) and
Steinberg and colleagues (25) found in human cadavers
that there were multiple RLN branches of minor and
major size and included branches to the pharynx. The
main trunk of the RLN was found to divide into two
divisions, the cricopharyngeal (CP) nerve and the laryngeal branch of the RLN. The CP nerve was connected to
the CPM and the inferior constrictor. However, there
are no reports on functional innervation of CPM by the
RLN.
The purpose of the present study was to test the
hypothesis that the CPM is, in part, anatomically and
functionally innervated by the RLN. This was investigated by anatomic dissection of RLN, electrical stimulation of the RLN while recording the electromyographic
(EMG) activity of the CPM, and by recording CPM
activity during swallowing pre- and post-RLN section.
Sheep were used as a model for swallowing in this
study because of the anatomic and physiological similarities to humans (1). Anatomic evidence suggests that
the sheep and human larynx are similar in the structure of the oral-laryngeal-pharyngeal complex as far as
the cartilage and bone structures and the muscles of
this area (1). The results demonstrated that the posterior CPM is directly innervated by the RLN.
METHODS
The Animal Care and Use Committee of the J. Hillis Miller
Health Center, University of Florida, reviewed and approved
the protocol of this study.
Anatomic description of the RLN innervation of the CPM.
The anatomic distribution of the RLN in the pharyngeal area
was made by postmortem dissection in sheep (n 5 12). The
neck was dissected to expose the path of the RLN. The
branches of the RLN were identified and traced by dissection.
The RLN was traced to the CPM. The RLN nerve branch
distributed to the CPM was labeled and photographed under
a microscope.
Electrophysiological identification of CPM innervation by
the RLN in sheep. Functional innervation of the CPM by the
RLN was investigated by using electrical stimulation of the
RLN while simultaneously recording EMG activity from the
CPM in adult sheep (n 5 4). The animals were initially
anesthetized with pentobarbital sodium (32 mg/kg iv). The
sheep was then placed in supine position. The femoral vein
0161-7567/97 $5.00 Copyright r 1997 the American Physiological Society
89
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Hammond, Carol Smith, Paul W. Davenport, Alastair
Hutchison, and Randall A. Otto. Motor innervation of the
cricopharyngeus muscle by the recurrent laryngeal nerve. J.
Appl. Physiol. 83(1): 89–94, 1997.—Patients with recurrent
laryngeal nerve (RLN) paresis demonstrate impaired function of laryngeal muscles and swallowing. The cricopharyngeus muscle (CPM) is a major component of the upper
esophageal sphincter. It was hypothesized that the RLN
innervates this muscle. A nerve branch leading from the RLN
to the CPM was found in adult sheep by anatomic dissection.
Electrical stimulation of the RLN elicited a muscle action
potential recorded by electrodes placed in the ipsilateral
CPM. Swallowing was investigated by mechanical stimulation of oropharynx pre- and postsectioning of the RLN.
Severing of the RLN resulted in a loss of the early phases of
swallow-related CPM electromyographic activity; however,
late-phase CPM electromyographic activity persisted. The
RLN provides motor innervation of the CPM, which also has
innervation from the pharyngeal plexus.
90
MOTOR INNERVATION OF THE CPM BY THE RLN
Data analysis. The mean duration and pattern of the
integrated electrical activities recorded from the bipolar
recording electrodes sutured into the CPM were compared
under both intact and post-RLN section conditions. A one-way
analysis of variance was used to analyze differences in
duration of four swallows in each of the following conditions:
pre-RLN section, post-RLN section, and postvagal section.
When required, Scheffé’s R-test and Fisher test of multiple
comparisons were utilized to determine which group means
differed. Significance level was set at P # 0.05.
RESULTS
Anatomic description of the RLN innervation of the
CPM. A nerve branch connecting the RLN to the CPM
was observed in all sheep (n 5 12). A photomicrograph
is presented illustrating the gross anatomic identification of the CP branch of the RLN (Fig. 1). This nerve
had profuse branches that penetrated the CPM.
Electrophysiological identification of CPM innervation by the RLN in sheep. Electrical stimulation of the
RLN elicited a motor action potential in the ipsilateral
CPM in all animals tested. Figure 2A illustrates the
EMG activity recorded from the CPM with a single
stimulus pulse. An average of 115 stimulations elicited
from the CPM of the same animal is presented in Fig.
2B. The group mean latency from stimulus pulse to
onset of EMG activity was of 3.8 6 0.5 ms (Fig. 2).
The group mean conduction velocity was 30.5 6 6
m/s. When the stimulator was turned off, no muscle
electrical activity was observed. In one animal, the
CPM was dissected and separated from the surrounding musculature with nerve supply intact. The RLNelicited CPM EMG activity was not different from that
observed before CPM separation from surrounding
tissue. Several folded layers of surgical plastic (4 mm
thick) were then placed between the CPM and the
interconnected laryngeal and pharyngeal musculature
to provide further isolation of the CPM. EMG activity
was again present with RLN stimulation and was not
different from previously obtained EMG responses. The
CPM EMG activity was also unaltered when the attachment of the CPM was separated by blunt dissection
from the thyroid and cricoid cartilages (nerve and blood
supply remaining intact).
EMG response of the CPM pre- and post-RLN section.
The CPM EMG activity recorded during swallowing in
four (n 5 4) animals was characterized by an initial
large-amplitude burst of CPM EMG activity, followed
by lower amplitude, longer duration activity (Fig. 3A).
The average duration of the CPM EMG response for a
swallow in the intact animal was 0.68 6 0.06 s. After
the RLN was severed, CPM EMG activity during
swallowing was characterized by low-amplitude activity only. The initial large-amplitude EMG burst was
absent (Fig. 3B).
The average duration of the CPM EMG response
during swallowing after RLN section was 0.34 6 0.03 s.
Table 1 compares the swallow duration pre- and postRLN section. There was a significant difference (P ,
0.0001) in the duration of EMG activity before and after
RLN section.
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and artery were cannulated for supplemental administration
of anesthesia and monitoring of blood pressure, respectively.
Lactated Ringer (10% dextrose solution) was continuously
provided by slow intravenous infusion. Body temperature
was maintained at 38 6 1°C, with periodic use of a heating
pad. The sheep was maintained in a deep plane of anesthesia.
Anesthetic state was assessed by blood pressure, eye-blink,
and tail-pinch responses.
A midline incision was made in the neck from the thyroid
cartilage to the manubrium. A blunt dissection of the omohyoid and sternothyroid muscles exposed the posterior edge of
the thyroid cartilage. A suture was placed along the posterior
edge of the thyroid cartilage, which was used to rotate the
larynx and expose the CPM. Bipolar wire electrodes were
sutured into the CPM, between the posterior pharyngeal
raphe and CPM insertion on the cricoid cartilage. The electrodes were isolated in the CPM by insulation from surrounding tissue. The RLN was isolated along the tracheoesophageal groove ipsilateral to the CPM containing the recording
electrodes. The intact RLN was placed across the bipolar
stimulating electrodes that were electrically isolated from the
surrounding tissue. The identity of the RLN was confirmed by
electrical stimulation (5–500 µA) -elicited contraction of the
laryngeal musculature. The CPM EMG activity was amplified, band-pass filtered (300 Hz to 3 KHz), displayed on an
oscilloscope, and recorded on magnetic tape. The RLN was
stimulated with single pulses of 0.5-ms duration at 1 Hz. The
CPM EMG activity and the stimulator trigger pulse were
recorded on magnetic tape. A minimum of 128 stimulations
were recorded.
Data analysis. The data recorded on magnetic tape were
digitized at 3 kHz (Cambridge Electronic Design). The computer stored the digitized EMG activity and stimulus pulse. A
minimum of 100 CPM responses were then signal averaged,
and latency to muscle-evoked activity was determined. The
latency from stimulus presentation to the arrival of the
stimulus at the CPM muscle, divided by the length of the
nerve from the RLN-stimulating electrode site to the electrodes sutured into the CPM, was used to determine the
conduction velocity.
EMG response of the CPM pre- and post-RLN section.
Swallowing was elicited in four anesthetized adult sheep by
mechanical stimulation of the oropharynx subsequent to the
electrical stimulation of the RLN. A blunt instrument was
placed in the oral cavity, and the oropharynx was gently
probed for three to five strokes until the animal swallowed.
Swallowing was identified by characteristic pharyngeal EMG
activity that accompanies swallowing and visual observation
of the swallowing musculature, which involved the movement
of the oral, pharyngeal, and esophageal systems. Only records
where swallows were seen to proceed from the laryngopharynx in a peristaltic wave caudally through the esophagus
were analyzed. The CPM EMG activity recorded during
swallowing was integrated and displayed on a polygraph and
magnetic tape for subsequent analysis.
The RLN was then ligated bilaterally at two points and
severed between the ligatures. Swallowing was again elicited
by mechanical stimulation, and the CPM EMG activity was
recorded. The vagus nerve was subsequently sectioned bilaterally at the level of the thyroid cartilage to control for any
nerve branches from the vagus nerve that may be involved in
the pharyngeal plexus. Swallowing was again evoked, and
the EMG response was recorded. The RLN stumps proximal
to the CPM were then electrically stimulated, and the CPM
activity was recorded.
MOTOR INNERVATION OF THE CPM BY THE RLN
91
CPM electrical activity during swallowing in the
intact animal, post-RLN section, and after section of
the vagus nerve is presented in Fig. 4. The initial
large-amplitude phase of EMG activity was again
absent after RLN section (Fig. 4B), and vagotomy
produced no additional change in the CPM EMG response (Fig. 4C).
There was a significant difference (P , 0.05) in the
CPM EMG duration between the intact state and both
RLN cut and cranial nerve X cut conditions. There was
no significant difference found between the RLN cut
and vagotomy conditions. Stimulation of the proximal
stump of the severed RLN elicited a CPM EMG action
potential.
DISCUSSION
The results of this study demonstrated that the RLN
innervates the CPM anatomically and functionally.
Anatomic innervation was demonstrated by identification of a branch of the RLN that entered fibers of the
CPM. Functional innervation of the CPM by RLN
motor nerve fibers was demonstrated by muscle-evoked
activity recorded in the CPM resulting from electrical
stimulation of the RLN. Removal of the innervation
altered the CPM EMG pattern of a swallow. These
findings demonstrate that RLN is one component of the
innervation of the CPM and plays an important role in
swallowing. During the oropharyngeal swallow, biomechanical events involving intrinsic glottic as well as
supra- and infrahyoid muscles take place resulting in
the closure of the airway (4, 17–19) and opening of the
UES (2, 10). These events include adduction of the true
vocal folds and arytenoid cartilages followed by vertical
approximation of the adducted arytenoids to the base of
the epiglottis. The descent of the epiglottis covers the
closed glottis, which closes the laryngeal vestibule. The
swallow begins with glottal closure followed by the
entire larynx pulled in a ventrorostral direction. This
displacement results in the positioning of the closed
glottis under the tongue base, away from the path of the
food bolus, providing protection against aspiration and
facilitating closure of the laryngeal vestibule (20, 26,
27).
During the oropharyngeal phase of swallowing, the
UES transiently relaxes and subsequently is pulled
upward and forward by the contraction of the suprahyoid muscles that displace the larynx. This traction
results in the active opening of the UES, which is also
modified by the bolus size (2, 10). Under unimpaired
conditions, oropharyngeal swallowing begins with the
vocal folds adducted and ends when they return to the
resting position (3).
Kahrilas et al. (10) combined videofluoroscopy and
manometry to analyze pharyngeal contraction in humans during swallowing. Profound shortening of the
pharyngeal muscles during bolus transit through the
pharynx eliminated access to the larynx and elevated
the UES ventrorostrally. The UES is a major barrier
preventing refluxed gastric contents from reaching the
upper airway. Cook et al. (2) and Kahrilas et al. (10),
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Fig. 1. Photomicrograph of laryngeal-pharyngeal area of sheep demonstrating cricopharyngeal (CP) branch. 1:
Posterior border of thyroid cartilage; 2: cricopharyngeus muscle (CPM); 3: recurrent laryngeal nerve (RLN); 4: as
the CP branch courses to CPM; 5: laryngeal branch of RLN; 6: glass probe placed deep into CP branch of RLN.
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MOTOR INNERVATION OF THE CPM BY THE RLN
Fig. 2. A: CPM activity elicited by a single stimulation of RLN. B:
averaged CPM activity elicited by multiple stimulations of CPM.
Time from stimulus pulse is plotted on x-axis. Zero time corresponds
to time when the stimulus was applied to RLN. Evoked motor activity
is evident by large change in voltage. Onset of CPM activity is
indicated by arrows.
using combined videofluoroscopy and manometry, reported that the physiological high-pressure zone of the
UES corresponds in size and location to the CPM. The
diameter of the sphincter was directly related to the
volume swallowed. Larger boluses increased the prolongation of the interval of sphincter relaxation. Tonic
CPM activity (7) normally present in the awake animal
was not observed in the present study, probably due to
the use of barbiturate anesthesia and the deep plane of
anesthesia. This is supported by the report of a decrease in UES pressure during non-rapid-eye-movement sleep, which was likely due to a decrease in the
tonic activity of the muscles of this sphincter (11).
The function of the esophaglottal closure reflex is to
adduct the vocal folds and close the entrance to the
trachea in response to abrupt esophageal distention.
Shaker et al. (20) reported that the onset of vocal fold
Fig. 3. Integrated CPM activity recorded during a mechanically
stimulated swallow in 1 sheep. EMG activity was integrated with a
100-ms time constant. A: three separate swallows in same sheep with
RLN intact. Arrow indicates onset of swallow-related integrated
EMG activity. B: three separate swallows in same sheep as in A after
RLN was severed. Integrated EMG activity was recorded and displayed at same amplification in both conditions.
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adduction preceded the onset of UES relaxation and
inferred that the likely efferent fibers controlling the
esophagoglottal reflex were located in the RLN and
that the target muscles were the glottal adductors. The
results of the present study demonstrate the importance of RLN innervation of the CPM for normal
swallowing.
Anatomy. The innervation of the CPM by the CP
branch of the RLN is similar between humans (25) and
sheep (1). Results of the present gross dissection of the
laryngeal-pharyngeal area in sheep revealed that a
branch of the RLN enters in the muscular wall of the
CPM in sheep. Selective stimulation of the RLN elicited
EMG activity in the CPM, which can only result from
neuromuscular innervation between the motor nerve
fibers of the RLN and CPM muscle fibers. The latency
and conduction velocities indicate that the motor nerve
fibers innervating the CPM are myelinated nerve fibers
(9). Sasaki and Isaacson (17) studied fiber types of the
RLN at the level where the nerve entered the larynx in
the dog and reported that a majority of the RLN axons
were myelinated fibers. There were a small number of
fibers .16 µm in diameter, and the majority were
between the 6–12 µm range. The functional differences
in RLN fibers resulted in some fibers allocated for
adduction and others for abduction. Diamond et al. (6)
reported that the RLN, which supplied the posterior
cricoarytenoid muscle in the dog, had three fascicles
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MOTOR INNERVATION OF THE CPM BY THE RLN
Table 1. Duration of CPM EMG activity during swallows recorded in sheep pre- and post-RLN section
Intact RLN
Post-RLN Section
Sheep
No.
Mean swallow
EMG
duration, s
No. swallows
measured
Swallow EMG
duration
range, s
Mean swallow
EMG
duration, s
No. swallows
measured
Swallow EMG
duration
range, s
1
2
3
4
0.71
0.74
0.63
0.62
4
5
4
5
0.6–0.8
0.7–0.8
0.6–0.7
0.5–0.7
0.38
0.33
0.30
0.35
4
5
4
5
0.3–0.4
0.3–0.4
0.3
0.3–0.4
CPM, cricopharyngeus muscle; RLN, recurrent laryngeal nerve.
Fig. 4. Integrated CPM activity recorded during a mechanically
stimulated swallow. EMG activity was integrated with a 100-ms time
constant. A: integrated EMG activity for 1 swallow in a sheep with
RLN and dependent vagus nerve intact. B: integrated EMG activity
recorded for 1 swallow after only the RLN was severed in same sheep
as in A. C: integrated EMG activity recorded for 1 swallow after RLN
and dependent vagus nerve were both severed in same sheep as in A.
Arrows indicate onset of the swallow.
ing a shortening of the pharynx with initial largeamplitude activity, followed by sustained closure of the
esophagus with low-level tonic CPM EMG activity.
Both actions prevent aspiration and/or reflux by anchoring the skeleton to allow for the ventrorostral movement of the larynx to protect the airway and the
peristaltic movement of the food bolus down the esophagus by striated musculature. In the case of RLN
dysfunction, aspiration can occur because access was
allowed to the larynx due to failure of pharyngeal
shortening and support of the musculoskeleton in
preparation for the ventrorostral lifting of the laryngeal complex and loss of laryngeal adductor motor
output. The swallowing CPM EMG response observed
in these sheep (Fig. 5) demonstrates the function of the
CPM during swallowing and the necessity of RLN
innervation; i.e., shortening of fibers that facilitates
rapid closure of proximal esophagus and rapid elevation and shortening of the pharynx, allowing the laryngeal area to be protected from infiltration by the bolus
(14).
Fig. 5. Line drawing demonstrating proposed movement of hypopharyngeal area of the human. Arrows point to direction of movement
proposed to occur due to CPM contraction as a result of stimulation
by CP branch of RLN. 1: Thyroid cartilage; 2: cricoid cartilage; 3:
CPM; 4: CP branch; 5: RLN. [Adapted from Nanson (14).]
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that innervated the three muscle divisions of the
posterior cricoarytenoid muscle. These fascicles differed in axon type, composition, and in percentages of
sensory, autonomic, and motor fibers. Thus the results
of this study support the hypothesis that the RLN
innervates the CPM with a branch identified as the CP
branch of the RLN.
Physiology. Coordination of the digestive and respiratory systems during swallowing is well established (17,
19). Shaker et al. (20) studied the esophagoglottal
reflex, elicited by abrupt esophageal distension, and
found the response was characterized by vocal fold
adduction, anterior movement of the glottis, opening of
the UES and relaxation of the proximal esophagus. The
UES and glottis act independently of each other in
response to esophageal distension and are likely to be
activated by different receptors, but their responses to
esophageal distension are complementary. In the present study, the early-phase, large-amplitude CPM EMG
response may correspond to fast contraction of the
CPM, which supports the musculoskeletal complex of
the pharynx in preparation for rapid pharyngeal shortening. In the intact mammal, the CPM may be mediat-
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MOTOR INNERVATION OF THE CPM BY THE RLN
Address for reprint requests: P. W. Davenport, Dept. of Physiological Sciences, Box 100144, JHMHC, Univ. of Florida, Gainesville, FL
32610 (E-mail: [email protected]).
Received 9 July 1996; accepted in final form 27 February 1997.
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Shin et al. (23) suggested that the inferior constrictor
muscle (which includes the CPM) functions in cooperation with the intrinsic laryngeal adductor muscles to
reinforce glottic closure during swallowing. The retention of low-level EMG activity after RLN section demonstrates that the CPM has other innervation, presumably from the superior laryngeal nerve. It will be
important to further investigate regional differences in
the distribution in the posterior CPM for RLN and
superior laryngeal nerve nerve fibers. There may be
specific differences in the types of motor units that
innervate the CPM. It appears from the present results
that the RLN fibers mediate the rapid, large-amplitude
CPM EMG response and that another pathway mediates the subsequent low-amplitude, sustained CPM
EMG response. The RLN may facilitate a rapid closure
of the proximal esophagus and rapid elevation and
shortening of the pharynx, which allows the laryngeal
area to be protected from infiltration by the bolus.
In summary, the present study demonstrates anatomic and functional innervation of the CPM by the
RLN. Gross anatomic dissection revealed that a branch
of the RLN enters the muscular wall of the CPM.
Selective stimulation of the RLN elicited EMG activity
in the CPM, which can only result from neuromuscular
connections between the motor nerve fibers of the RLN
and CPM fibers. The normal pattern of CPM swallowing EMG activity in sheep is dependent on an intact
RLN. Swallow CPM EMG activity elicited by mechanical stimulation of the oropharyngeal area was altered
by a shortened duration and loss of CPM EMG largeamplitude activity after section of the RLN. Lowamplitude activity was retained by the CPM during
swallowing after RLN section, demonstrating that the
CPM has dual innervation from the RLN and from
another, as yet unidentified, nerve.