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J. Anat.
(2003)
202
, pp421–430
© Anatomical Society of Great Britain and Ireland 2003
Blackwell Science, Ltd
Intralaryngeal neuroanatomy of the recurrent laryngeal nerve of the rabbit
Stephen Ryan,
1
Walter T. McNicholas,
2
Ronan G. O’Regan
1
and Philip Nolan
1
1
Department of Human Anatomy and Physiology and
2
Department of Respiratory Medicine, Conway Institute for Biomolecular and Biomedical Research, University College Dublin
2
St. Vincent’s University Hospital, Dublin, Ireland
Abstract
We undertook this study to determine the detailed neuroanatomy of the terminal branches of the recurrent laryn-
geal nerve (RLN) in the rabbit to facilitate future neurophysiological recordings from identified branches of this
nerve. The whole larynx was isolated
post mortem
in 17 adult New Zealand White rabbits and prepared using a
modified Sihler’s technique, which stains axons and renders other tissues transparent so that nerve branches can
be seen in whole mount preparations. Of the 34 hemi-laryngeal preparations processed, 28 stained well and these
were dissected and used to characterize the neuroanatomy of the RLN. In most cases (23/28) the posterior cricoary-
tenoid muscle (PCA) was supplied by a single branch arising from the RLN, though in five PCA specimens there were
two or three separate branches to the PCA. The interarytenoid muscle (IA) was supplied by two parallel filaments
arising from the main trunk of the RLN rostral to the branch(es) to the PCA. The lateral cricoarytenoid muscle (LCA)
commonly received innervation from two fine twigs branching from the RLN main trunk and travelling laterally
towards the LCA. The remaining fibres of the RLN innervated the thyroarytenoid muscle (TA) and comprised two
distinct branches, one supplying the pars vocalis and the other branching extensively to supply the remainder of
the TA. No communicating anastomosis between the RLN and superior laryngeal nerve within the larynx was
found. Our results suggest it is feasible to make electrophysiological recordings from identified terminal branches
of the RLN supplying laryngeal adductor muscles separate from the branch or branches to the PCA. However, the
very small size of the motor nerves to the IA and LCA suggests that it would be very difficult to record selectively
from the nerve supply to individual laryngeal adductor muscles.
Key words
larynx; Sihler’s stain.
Introduction
The recurrent laryngeal nerve (RLN) provides the motor
innervation to all intrinsic laryngeal muscles except the
cricothyroid and is responsible for adjustments in glottic
aperture during the respiratory cycle. The pattern of
respiratory-related discharge observed from whole RLN
recordings is complex, exhibiting activity either exclu-
sively in inspiration or during both respiratory phases
(Green & Nail, 1955; Sica et al. 1984, 1985). As a result
interpretation of whole RLN motor activity in relation
to control and function of laryngeal abductor and
adductor muscles is difficult. Recordings obtained from
motor units in the RLN show that the RLN contains
functionally diverse groups of motoneurones (Sica
et al. 1985; Ryan et al. 2002). It is assumed that these
motoneurones are destined for different muscles groups
on the basis of discharge pattern and the known
electromyographic activity profiles and function of
laryngeal abductor and adductor muscles. RLN motor
units with post-inspiratory discharge are presumed to
innervate laryngeal adductor muscles (Bartlett et al.
1973; Ryan et al. 2002) while units with inspiratory-
related activity are assumed to supply the posterior
cricoarytenoid muscle (PCA), the principal abductor of
Correspondence
Dr Philip Nolan, Department of Human Anatomy and Physiology, Conway Institute for Biomolecular and Biomedical Research, University College Dublin, Earlsfort Terrace, Dublin 2, Ireland. Tel.: +353 17167466; fax: +353 17167417; e-mail: [email protected]
Accepted for publication
28 February 2003
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
422
the vocal cord. These assumptions may not be entirely
valid because (i) the action and functions of individual
laryngeal muscles are incompletely understood, (ii)
laryngeal adductor activity is not confined to expiration
(Insalaco et al. 1990) and (iii) the PCA exhibits tonic
expiratory activity on which phasic inspiratory activity
is superimposed (Sherrey & Megirian, 1980).
Care must be taken when interpreting recordings
obtained from motor units in the main trunk of the
RLN, as we cannot be certain of their final destination
within the larynx. Zhou et al. (1989) used a novel
approach to studying the motor control of laryngeal
muscles by recording separately from the intralaryn-
geal branches supplying the abductor and adductor
muscles. We intend to perform similar experiments in
our decerebrate rabbit preparation (Ryan et al. 2002).
However, in a complex structure such as the larynx,
gross dissection is not always a reliable means of trac-
ing the neural pathway from extramuscular to intra-
muscular terminal branches, as the latter are very small
and hard to distinguish from blood vessels and connec-
tive tissue, even with the aid of a dissecting microscope.
Furthermore, when tracing nerve branches deeper into
the muscles they innervate, preserving one branch often
necessitates unwanted destruction of other motor
and/or sensory nerves to the same structure.
The primary aim of this study is to characterize accu-
rately the anatomical distribution of intralaryngeal
branches of the RLN so that for future studies of elec-
trophysiological terminal branches of this nerve we
could be confident of the final destination of motor
axons while recording their activity. In addition, we
sought to determine whether the branching pattern of
intramuscular nerves was consistent with compartmen-
talization of laryngeal muscles in the rabbit, as recent
evidence suggests that in both dog and human, individ-
ual laryngeal muscles (Drake et al. 1993; Sanders et al.
1993a, 1994a,b; Bryant et al. 1996) and in particular the
PCA, are organized into anatomically and functionally
distinct neuromuscular compartments. Wu & Sanders
(1992) have refined a relatively old histological tech-
nique, Sihler’s stain, to investigate intramuscular
branching of motor nerves without the problems asso-
ciated with the use of microdissection or serial histolog-
ical sections. Modified Sihler’s stain renders the whole
specimen relatively translucent while counterstaining
its nerve supply (Wu & Sanders, 1992) and has the
advantage of preserving the three-dimensional struc-
ture of the whole specimen.
Methods
Seventeen adult New Zealand White rabbits weighing
2.5–4.5 kg were killed using a lethal overdose of
sodium pentobarbitone (200 mg kg
−
1
; Sagatal, Rhone
Merieux, Ireland) administered intravenously through
a marginal ear vein. A ventral midline neck incision was
made to expose the trachea and larynx. The large veins
of the neck were divided and heparanized saline
(500 mL) was infused at 90 mmHg pressure through
cannulae inserted into both common carotid arteries.
The whole larynx, including a portion of the trachea
approximately 5 mm long, was isolated
post mortem
and prepared using a modified Sihler’s staining tech-
nique in seven stages. Reagents were obtained from
Sigma Aldrich, UK, unless otherwise stated.
1. Fixation.
The whole larynx was immersed immedi-
ately after removal in 10% unneutralized formalin for
2 weeks.
2. Maceration and de-pigmentation.
The fixed specimens
were removed from the formalin and washed in dis-
tilled water for 30 min before being placed in a solu-
tion containing 3% aqueous potassium hydroxide (KOH)
with three drops of 3% hydrogen peroxide (H
2
O
2
)
added to every 100 mL of solution. They were allowed
to incubate in this solution at room temperature. The
solution was changed every second day initially, and
at least once a week thereafter, or whenever the solution
became cloudy. Maceration continued for 3 weeks until
the tissues became translucent.
3. Decalcification.
After washing in distilled water for
30 min, the laryngeal specimens were transferred into
Sihler’s I solution for 2 weeks to decalcify the speci-
mens. Sihler’s I solution was prepared as follows: one
part glacial acetic acid, one part glycerin in six parts 1%
aqueous chloral hydrate. The specimens were trans-
ferred to fresh solution every 2–3 days.
4. Staining.
Following decalcification, each larynx was
washed in distilled water for 30 min and incubated in
Sihler’s II solution. Sihler’s II solution was prepared
using one part Ehrlich’s Haematoxylin (Lennox Labora-
tory Supplies, Ireland), one part glycerin, and six parts
1% aqueous chloral hydrate. The solution was changed
once per week. Each specimen was regularly examined
under a dissecting microscope. The staining procedure
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
423
was carried out for at least 3 weeks or until the large
nerves within the specimens turned dark purple and
the terminal nerve branches were well stained.
5. Destaining.
Each larynx was washed in distilled water
(30 min) then immersed in Sihler’s I solution to remove
excess stain. We found that 30 min exposure time is
adequate, with longer periods resulting in loss of fine
detail due to excessive loss of stain from fine terminal
nerve branches.
6. Clearing.
Before clearing, specimens were washed in
distilled water (30 min). Clearing involved immersing
the tissues in increasing concentrations of glycerin
(40%, 60%, 80% and 100%) in dark conditions. The
specimen remained in 40% and 60% glycerin for
2 days, and one day each in 80% and 100% glycerin.
7. Trimming.
Each specimen was divided along the
midline and the 34 hemi-laryngeal preparations were
examined under a dissecting microscope (Wild M50),
trans
-illuminated with a variable fibre-optic light
source, and carefully dissected to examine the intra-
laryngeal course of the RLN and its terminal branches. All
laryngeal muscles were dissected from their cartilagi-
nous attachments and examined as whole-mount prep-
arations. Drawings and photomicrographs were taken
during the dissecting process.
Results
Thirty-four hemi-laryngeal preparations were examined
and, of these, 28 were adequately stained. The RLN
approached the larynx as a single trunk and entered it
through a groove between the oesophagus and trachea
on the posterior tracheal surface. The intralaryngeal
neuroanatomy of the RLN revealed the following inner-
vation pattern for individual laryngeal muscles.
Pca
As the RLN entered the larynx, passing over the crico-
thyroid joint, the nerve supply of the PCA branched
medially from the main trunk (Fig. 1). In 23 of 28 PCA
specimens, one single branch arose from the main
trunk of the RLN to innervate the PCA. Upon entering
the muscle this branch subdivided into two or three
smaller intramuscular nerve branches (Fig. 2). Because
of the extensive arborization of these intramuscular
nerve branches, no clear evidence was found to
indicate any discrete compartmentalization of the
intramuscular nerve supply. In only five of the PCA
specimens examined (four of which were located on
the right-hand side of the larynx) two or three distinct
branches arose from the RLN main trunk to supply the
PCA (not shown).
Interarytenoid muscle (IA)
The nerve supply to the IA arose from the main trunk
of the RLN rostral to the branch(es) supplying the PCA
(Fig. 1). In three specimens the nerve supply to the IA
originated from the medial branch supplying the thyro-
arytenoid muscle (TA). The IA branch ran diagonally,
upwards and medially, along the anterior border of the
PCA and next to the cricoarytenoid joint before enter-
ing the inferior lateral border of the IA (Figs 1 and 2).
In 25 of 28 cases the IA branch ran as a single trunk
before dividing into two fine filaments prior to its entry
into the IA (Figs 1 and 3). However, in three of 28 laryn-
geal preparations two small filaments arose from the
RLN main trunk but quickly rejoined, continuing as a
single branch and separating into two twigs before
innervating the IA (not shown). These twigs further sub-
divided upon entering the muscle (4–5 intramuscular
nerve branches), forming a complex branching anatomy
of the intramuscular nerve branches (Fig. 3).
Lateral cricoarytenoid muscle (LCA)
After providing branches to supply the PCA and IA, the
RLN continued cranially, either as a single trunk or two
parallel divisions (medial and lateral), to the superior
border of the cricoid, where it turned sharply antero-
medially. As it approached the superior border of the
cricoid, one or two very fine twigs branched from the
RLN and travelled laterally to innervate LCA (Fig. 4).
However, in two specimens one of the two twigs sup-
plying LCA arose from the IA branch (Sanders et al.
1994a). The most consistent feature of the intramuscular
neuroanatomy of the LCA innervation was division into
2–5 smaller terminal nerve branches, which exhibited
extensive arborization throughout the muscle (Fig. 4).
TA
The remaining fibres of the RLN innervated the TA.
Two separate neuromuscular compartments were
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
424
identified, one supplying the pars vocalis, the other
branching extensively to supply the remainder of the
TA (Figs 5 and 6).
Communicating branches between individual
intralaryngeal nerves
Communicating twigs between individual intralaryn-
geal nerves often occurred, the most common of which
was that between the primary branch supplying the
PCA and IA (Fig. 2). Others included a communication
between terminal nerve endings supplying the TA and
IA (
n
= 2) and the IA and LCA (
n
= 2). A common com-
municating branch in one specimen between the PCA,
IA and TA muscles (Fig. 1) was also found. Except in one
preparation no evidence of any neural connection
between the intramuscular neural plexus supplying the
IA and the internal branch of the superior laryngeal
nerve (iSLN Nordland, 1930; Mu et al. 1994) was found.
Discussion
Our results clearly demonstrate that the RLN provides
separate and anatomically distinct branches to laryn-
geal abductor (PCA) and adductor muscles (TA, IA, LCA)
and verify that in the rabbit at least, it is possible to
record from branches of the RLN and be confident that
one is separately recording motor neurones destined
for abductor as opposed to adductor muscles. However,
because of the very small size of the motor nerves to the
IA and LCA it would be very difficult to record selectively
from the nerve supply to individual adductor muscles.
The distribution of intramuscular branches of the
PCA neither confirms nor rules out the possibility that
Fig. 1 Innervation of the intralaryngeal muscles by the recurrent laryngeal nerve (RLN). This photograph shows a view of the branching anatomy of the main trunk of the RLN (A) to supply the posterior cricoarytenoid muscle (B), the interarytenoid muscle (C) and the lateral cricoarytenoid (D). The muscle nerve branches supplying the thyroarytenoid proper (E) and pars vocalis (F) neuromuscular compartments of the thyroarytenoid (E) are also shown. The RLN, its terminal branches and the muscles they supply have been dissected from their respective laryngeal insertions.
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
425
this muscle is composed of two or three anatomically
and functionally separate compartments. In the major-
ity of specimens examined a single branch from the
RLN main trunk supplied the PCA. The intramuscular
distribution of this branch was such that it subdivided
into two or three smaller intramuscular nerve branches
whose terminal endings exhibited extensive arboriza-
tion branching irregularly throughout the muscle. We
could not distinguish separate compartments on the
basis of this branching pattern. This contrasts with
other studies in dog (Diamond et al. 1992; Drake et al.
1993; Sanders et al. 1993a) and human (Sanders et al.
1994a) PCA muscles, where the PCA was organized into
separate bellies or compartments each receiving dis-
tinct innervation from primary branches of the RLN
supplying this muscle (Diamond et al. 1992; Drake et al.
1993; Sanders et al. 1993a, 1994a). It is difficult to con-
clude with certainty whether a muscle is divided into
neuromuscular compartments based only on anatomi-
cal studies of neural branching pattern. The division of
the PCA into distinct compartments in other species is
based on a greater body of evidence, including histo-
chemical (Sanders et al. 1993a) and functional (Diamond
et al. 1992; Sanders et al. 1993a) evidence.
Fig. 2 Posterior view of the left posterior cricoarytenoid muscle (PCA). The PCA (A) has been removed and squashed to demonstrate the intramuscular branches of the PCA. In this photograph only one branch from the recurrent laryngeal nerve (RLN, E) supplying the PCA was identified. The PCA nerve bifurcates upon entering the muscle, forming three distinguishable intramuscular branches. A communicating twig (B) between the PCA (A) and the branch to the interarytenoid muscle (C), and the remainder of the RLN main trunk destined for laryngeal adductor muscles (D) are also shown.
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
426
A powerful yet under-utilized technique is to obtain
selective electromyographic (EMG) recordings from
different regions of the muscle. Woo & Bortoff (1987)
described different EMG responses in the medial and
lateral divisions of rat PCA during various anaesthetic
and respiratory conditions. Sanders et al. (1994b),
investigating the pattern of vocal fold motion evoked
by direct electrical stimulation of different muscle bel-
lies within the PCA, found that each belly is capable of
moving the arytenoid in different ways. We have pre-
viously shown in the rabbit that there are two distinct
types of RLN motor units with inspiratory discharge,
phasic inspiratory and tonically active units whose
activity is inhibited during inspiration (Ryan et al. 2002).
Similar populations of inspiratory motor units have
been demonstrated in the cat (Murakami & Kirchner,
1972; Sica et al. 1985). Given that the PCA is the principal
abductor of the vocal cords and is the only laryngeal
muscle innervated by the RLN that exhibits inspiratory
activities under normal conditions (Suzuki & Kirchner,
1969), it is presumed that both these inspiratory RLN
motor units innervate the PCA. A multi- or single unit
EMG recording from the PCA would determine whether
these different motor units are located in distinct
anatomical regions or compartments of the PCA.
In relation to laryngeal adductor muscles, we clearly
identified separate branches arising from the main
trunk that travelled separately to innervate the TA,
LCA and IA. The motor innervation of the IA in all cases
arose from the ipsilateral RLN alone and ran along the
rostral border of the PCA. Previous investigations on
the innervation pattern of the IA have been performed
Fig. 3 Posterior view of the right interarytenoid muscle (IA). A single nerve branch arising from the recurrent laryngeal nerve bifurcates (B) to form two small neural filaments close to its insertion into the IA (A). The intramuscular branching anatomy of these filaments forms a complex anastomatic network.
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
427
on specimens from human subjects. One study (Mu
et al. 1994) found that all human IA muscles studied
receive a ‘bilateral’ nerve supply from both RLNs
together with nerve twigs derived from the descending
division of the iSLN. However, Nordland (1930) found
that 18 of 19 human IA muscles were exclusively inner-
vated by the iSLN. We documented only one rabbit
hemi-laryngeal specimen where the IA received a com-
municating branch between the ipsilateral iSLN and
RLN. In all remaining laryngeal preparations each IA
received an ipsilateral nerve supply from the RLN only.
The LCA plays an important role in adducting the
vocal cords in phonation and reflex glottic closure
(Tanaka & Tanabe, 1986) but may also produce laryngeal
abduction (Stroud & Zwiefach, 1956). While these dif-
fering functions might be reflected in separation of
the LCA into functionally different neuromuscular com-
partments we and others (Sanders et al. 1993b) have
found the LCA to comprised a single neuromuscular
compartment with a homogeneous motor nerve plexus
(Sanders et al. 1993b). We found the nerve branches
supplying the LCA arose from the RLN usually as two
separate fascicles or rarely as two twigs, one from the
IA branch (Wu & Sanders, 1992; Sanders et al. 1993b)
and one from the RLN main trunk.
The TA had two distinct neuromuscular compart-
ments (Sanders et al. 1993c; Wu et al. 1994; Inagi et al.
1998), the pars vocalis and the TA proper. We did not
identify any other prominent source of or communicat-
ing anastomoses with the neural supply to the TA con-
trary to observations made in other species (Dilworth,
1921; Kambic et al. 1984; Wu et al. 1994). For instance,
the presence of communicating anastomoses between
the RLN and SLN has been demonstrated several times
in studies of the human larynx (Dilworth, 1921; Kambic
et al. 1984; Wu et al. 1994; Sanudo et al. 1999). Wu
Fig. 4 Posterior view of the right lateral cricoarytenoid muscle (LCA). The LCA (A) receives two small filaments (B), one arising from each of the two medial and lateral divisions (C) of the recurrent laryngeal nerve destined for the thyroarytenoid muscle. The intramuscular branching anatomy demonstrates 2–5 further subdivisions of the filaments innervating the muscle.
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
428
et al. (1994) found that the communicating nerve is
composed of fascicles that are organized into sensory
and intramuscular motor nerve branches. The sensory
component supplies the subglottic area. The intramus-
cular branch usually joined the RLN within the TA. These
investigators propose that the human communicating
nerve is ‘an extension of the external superior laryngeal
nerve that innervates the vocal cord’ connecting the
cricothyroid and TA muscles. We were unable to identify
this communicating nerve in the rabbits. The only other
mammal in which this nerve has been demonstrated
was the dog (Dedo & Ogura, 1965). The function of this
nerve may perhaps be related to vocalization or phona-
tion, functions well ascribed to the TA. Both species in
which the communicating nerve has been identified
(human and dog) produce vocal sounds. Phonation is
not, however, a well-developed function in rabbits,
and this may explain why we failed to identify a com-
municating branch in our laryngeal specimens.
In conclusion, Sihler’s stain is a powerful tool provid-
ing valuable information regarding the neuroanatomy
of the larynx. The primary benefit arising from this
study is that we now know the precise anatomical dis-
tribution of RLN branches to abductor and adductor
muscles. This will be a valuable asset when performing
future investigations to examine the respiratory role of
Fig. 5 Anteromedial view of the recurrent laryngeal nerve (RLN) branches to the thyroarytenoid (TA), lateral cricoarytenoid (LCA) and interarytenoid (IA) laryngeal adductor muscles. The adductor branches of the RLN supplying the TA and LCA approach superior to the arytenoid cartilage (E). Two or three small twigs are seen branching from the RLN to supply the LCA (C). The RLN continues to supply two larger branches (A and B) to the TA muscle. Branch A divides to diffusely innervate the TA muscle proper whereas branch B medial to the arytenoid cartilage innervates the pars vocalis. Also shown is the nerve supply to the IA muscle (D).
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
429
different laryngeal motor neurone pools in relation to
their known function of regulating airway patency and
expiratory airflow. However, with regard to the organ-
ization of the PCA into discrete neuromuscular com-
partments, our results using neuroanatomical tracing
techniques neither confirm nor refute their presence in
the rabbit.
References
Bartlett D, Jr, Remmers JE, Gautier H
(1973) Laryngeal regula-tion of respiratory airflow.
Resp
.
Physiol
.
18
, 194–204.
Bryant NJ, Woodson GE, Kaufman K, Rosen C, Hengesteg A,
Chen N, Yeung D
(1996) Human posterior cricoarytenoidmuscle compartments.
Anat
.
Mechanics
.
Arch
.
Otol
.
HeadNeck Surg
.
122
, 1331–1336.
Dedo HH, Ogura JH
(1965) Vocal cord electromyography in thedog.
Laryngoscope
75
, 201–211.
Diamond AJ, Goldhaber N, Wu BL, Biller H, Sanders I
(1992)The intramuscular nerve supply of the posterior cricoaryte-noid muscle of the dog.
Laryngoscope
102
, 272–276.
Dilworth TFM
(1921) The nerves of the human larynx.
J
.
Anat
.
56
, 48–52.
Drake W, Li Y, Rothschild MA, Wu B, Biller HF, Sanders I
(1993)A technique for demonstrating the entire nerve branchingof a whole muscle: Results in 10 canine posterior cricoaryte-noid muscles.
Laryngoscope
103
, 141–148.
Green JH, Nail E
(1955) The respiratory function of laryngealmuscles.
J
.
Physiol
.
129
, 134–141.
Fig. 6 Anteromedial view of the recurrent laryngeal nerve (RLN) branches to the thyroarytenoid muscle (TA). Before innervating the TA the adductor branch of the RLN bifurcates (C). One supplies the TA proper (A) dividing further into smaller intramuscular branches that extend rostrally through the TA towards the base of the epiglottis. A second branch (B) courses anteriorly and medially along the border of the arytenoid cartilage (removed) to innervate the pars vocalis.
Rabbit laryngeal neuroanatomy, S. Ryan et al.
© Anatomical Society of Great Britain and Ireland 2003
430
Inagi K, Schultz E, Ford CN
(1998) An anatomic study of the ratlarynx: establishing the rat model for neuromuscular func-tion.
Otol
.
Head Neck Surg
.
118
, 74–81.
Insalaco G, Kuna ST, Cibella F, Villeponteaux RD
(1990)Thyroarytenoid muscle activity during hypoxia, hypercapnia,and voluntary ventilation in humans.
J
.
Appl
.
Physiol
.
69
,268–273.
Kambic V, Zargi M, Radsel Z.
(1984) Topographic anatomy ofthe external branch of the superior laryngeal nerve.
J
.
Laryngol
.
Otol
.
98
, 1121–1124.
Mu L, Sanders I, Wu BL, Biller H
(1994) The intramuscularinnervation of the human interarytenoid muscle.
Laryngo-scope
104
, 33–39.
Murakami Y, Kirchner JA
(1972) Respiratory movements of thevocal cords: an electromyographic study in the cat.
Laryngo-scope
82
, 454–467.
Nordland M
(1930) The larynx as related to surgery of thethyroid. Based on an anatomical study.
Surg
.
Gyn. Obst
.
51
,449–459.
Ryan S, McNicholas WT, O’Regan RG, Nolan P
(2002) Effectof upper airway negative pressure and lung inflation onlaryngeal motor unit activity in rabbit.
J
.
Appl
.
Physiol
.
92
,269–278.
Sanders I, Wu B, Biller HF
(1993a) The three bellies of thecanine posterior cricoarytenoid muscle: implications for under-standing laryngeal function.
Laryngoscope
103
, 171–177.
Sanders I, Mu L, Wu BL, Biller HF
(1993b) The intramuscularnerve supply of the human lateral cricoarytenoid muscle.
Acta Otolaryngol
.
113
, 679–682.
Sanders I, Wu BL, Mu L, Li Y, Biller H
(1993c) The innervationof the human larynx.
Arch
.
Otol
.
Head Neck Surg
.
119
, 934–939.
Sanders I, Jacobs Wu B, Mu L, Biller HF
(1994a) The innervationof the human posterior cricoarytenoid muscle: Evidence for
at least two neuromuscular compartments.
Laryngoscope
104
, 880–884.
Sanders I, Rao F, Biller HF
(1994b) Arytenoid motion evokedby regional electrical stimulation of the canine posteriorcricoarytenoid muscle.
Laryngoscope
104
, 456–462.
Sanudo JR, Maranillo E, Leon X, Mirapeix RM, Orus C, Quer M
(1999) An anatomical study of anastomoses between thelaryngeal nerves. Laryngoscope 109, 983–987.
Sherrey JH, Megirian D (1980) Respiratory EMG activity ofthe posterior cricoarytenoid, cricothyroid and diaphragmmuscles during sleep. Resp. Physiol. 39, 355–365.
Sica AL, Cohen MI, Donnelly DF, Zhang H (1984) Hypoglossalmotorneuron responses to pulmonary and superior laryngealafferent inputs. Resp. Physiol. 56, 339–357.
Sica AL, Cohen MI, Donnelly DF, Zhang H (1985) Responses ofrecurrent laryngeal motoneurons to changes in pulmonaryafferent inputs. Resp. Physiol. 62, 153–168.
Stroud MH, Zwiefach E (1956) Mechanism of the larynx andrecurrent nerve palsy. J. Laryngol. Otol. 70, 80–96.
Suzuki M, Kirchner JA (1969) The posterior cricoarytenoid asan inspiratory muscle. Ann. Otol. 78, 849–864.
Tanaka S, Tanabe M (1986) Glottal adjustment for regulatingvocal intensity: an experimental study. Acta Otol. 102, 315–324.
Woo P, Bortoff A (1987) Regional differences in electromyo-graphic activity of the posterior cricoarytenoid muscle in therat. Otol. Head Neck Surg. 97, 150.
Wu BL, Sanders I (1992) A technique for demonstrating thenerve supply of whole larynges. Arch. Otol. 118, 822–827.
Wu BL, Sanders I, Mu L, Biller H (1994) The human communi-cating nerve. Arch. Otol. Head Neck Surg. 120, 1321–1328.
Zhou D, Huang Q, St. John WM, Bartlett D Jr (1989) Respira-tory activities of intralaryngeal branches of the recurrentlaryngeal nerve. J. Appl. Physiol. 67, 1171–1178.