Anatomy of the Human InternalSuperior Laryngeal Nerve

IRA SANDERS* AND LIANCAI MUGrabscheid Voice Center, Department of Otolaryngology,

The Mount Sinai Medical Center, New York, New York 10029

ABSTRACTThe mucosa of the larynx contains one of the most dense concentrations

of sensory receptors in the human body. This sensitivity is used for reflexesthat protect the lungs, and even momentary loss of this function is followedrapidly by life-threatening pneumonia. The internal superior laryngealnerve (ISLN) supplies the innervation to this area, and, to date, thedistribution and branching pattern of this nerve is unknown.

Five adult human larynges were processed by using Sihler’s stain, atechnique that clears soft tissue while counterstaining nerves. The whole-mount specimens were then dissected to demonstrate the branching of theISLN from its main trunk down to the level of terminal axons.

The human ISLN is divided into three divisions: The superior divisionsupplies mainly the mucosa of the laryngeal surface of the epiglottis; themiddle division supplies the mucosa of the true and false vocal folds and thearyepiglottic fold; and the inferior division supplies the mucosa of thearytenoid region, subglottis, anterior wall of the hypopharynx, and upperesophageal sphincter. Several dense sensory plexi that cross the midlinewere seen on the laryngeal surface of the epiglottis and arytenoid region.The human ISLN also appears to supply motor innervation to the interaryte-noid (IA) muscle.

A detailed map is presented of the distribution of the ISLN within thehuman larynx. The areas seen to receive the greatest innervation are thesame areas that have been shown by physiological experiments to be themost sensate: the laryngeal surface of the epiglottis, the false and true vocalfolds, and the arytenoid region. The observation that the human ISLNappears to supply motor innervation to the IA muscle is contrary to currentconcepts of the ISLN as a purely sensory nerve. These findings are relevantto understanding how the laryngeal protective reflexes work during activi-ties like swallowing. The nerve maps can be used to guide surgical attemptsto reinnervate the laryngeal mucosa when sensation is lost due to neurologi-cal disease. Anat. Rec. 252:646–656, 1998. r 1998 Wiley-Liss, Inc.

Key words: internal superior laryngeal nerve; larynx; sensory nerves;nerve staining; sensory innervation of the upper airway; Sihler’sstain

The internal superior laryngeal nerve (ISLN) is knownto be the principal sensory nerve of the larynx (Lemere,1932a; Ogura and Lam, 1953; Williams et al., 1989),although anatomic and electrophysiologic evidence sug-gests that a minor sensory contribution also comes fromthe recurrent laryngeal nerve (RLN) (Lemere, 1932a,b;Hirose, 1961; Suzuki and Kirchner, 1969) and from theexternal superior laryngeal nerve (ESLN) (Lemere, 1932a;Andrew, 1956; Suzuki and Kirchner, 1968). Because theISLN mediates most sensation of the mucosa in the larynx

and the hypopharynx, it plays a vital role in the protectionof the airway by initiating reflex glottic closure duringswallowing, coughing, and vomiting (Wilson, 1905; Storeyand Johnson, 1975; Stedman et al., 1980). The sensory

*Correspondence to: Ira Sanders, M.D., Department of Otolaryn-gology, Box 1189, Mount Sinai Medical Center, New York, NY10029–6574.

Received 24 April 1998; Accepted 16 July 1998

THE ANATOMICAL RECORD 252:646–656 (1998)

r 1998 WILEY-LISS, INC.

innervation of the human larynx is not well described,even though it was studied first by Simanowsky as early as1883 (Konig and von Leden, 1961; Yatake, 1965). Theanatomy of the ISLN has received an increasing interest inclinical and basic investigations for more than a centuryand has been studied in animals (Vogel, 1952; Feindel,1956; Yatake, 1965; Suzuki and Kirchner, 1968; Tanaka,1986; Yoshida et al., 1986) and in humans (Dilworth, 1921;Vogel, 1952; Ogura and Lam, 1953; Konig and von Leden,1961; Durham and Harrison, 1964; Yatake, 1965; Rueger,1972; Droulias et al., 1976; Hill and Olson, 1979; Chiba etal., 1985) by using various techniques. Previous studieshave demonstrated that the ISLN passes beneath thethyrohyoid muscle and enters the larynx through thethyrohyoid membrane (Durham and Harrison, 1964; Hilland Olson, 1979) or thyroid cartilage. Having entered thelarynx, it gives off two to five branches (Dilworth, 1921;Rueger, 1972). According to the classical description, theISLN provides the sensory innervation of the mucosa inthe region above the level of the vocal cords (Negus, 1949;Ogura and Lam, 1953; Droulias et al., 1976; Meller, 1984;Williams et al., 1989; Garrett and Larson, 1991). Belowthis level, the subglottic mucosa is innervated by the RLN(Lemere, 1932b; Negus, 1949; Meller, 1984; Garrett andLarson, 1991). More recent studies in cats (Tanaka, 1986;

Yoshida et al., 1986) have shown that the ISLN innervatesnot only the supraglottic region ipsilaterally but also thesubglottic region bilaterally. However, little information isavailable to date on whether or not the human ISLNsupplies the subglottic mucosa.

Previous efforts to study the sensory innervation of thelarynx have relied primarily on traditional microscopicdissection (Dilworth, 1921; Lemere, 1932a; Vogel, 1952;Yatake, 1965; Rueger, 1972), the silver impregnation (Ko-nig and von Leden, 1961; Watanabe, 1985), intravenousmethylene blue staining (Feindel, 1950, 1956), electronmicroscopy (Chiba et al., 1985; Watanabe, 1985), electro-physiological techniques (Andrew, 1956; Hirose, 1961;Suzuki and Kirchner, 1968, 1969), and, more recently,horseradish peroxidase (HRP) tracer technique (Tanaka,1986; Yoshida et al., 1986). Although each of the abovetechniques possesses unique and important advantagesfor study of sensory innervation of the larynx, all havecertain limitations inherent in their use, and most of themdo not provide a detailed description and illustration of theperipheral branching and distribution pattern of the ISLN.More recently, Sihler’s stain, a wholemount nerve-stainingtechnique, has been employed to investigate the innerva-tion of the larynx (Sanders et al., 1993a,b; Mu et al., 1994).This technique has several advantages. Perhaps the most

Fig. 1. Posterior view of a human larynx processed with Sihler’s stainwithout removing any anatomical structures. Note that the internalsuperior laryngeal nerve (ISLN) enters the larynx through the thyrohyoidmembrane (open arrow) and subdivides into three major divisions,superior, middle, and inferior, which supply different regions of the larynx.

A solid arrow indicates the first secondary nerve branch of the inferiordivision of the ISLN. E, epiglottis; AE, aryepiglottic fold; A, arytenoidcartilage; MP, mucosa covering the posterior cricoarytenoid muscle; Th,thyroid cartilage.

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valuable contributions of this method are that it can stainthe nerves in large, whole organs, such as the larynx, andcan be used on human postmortem tissue. After they areprocessed with Sihler’s stain, the nerve branches supply-ing the muscles and mucosa of the larynx stand out withgreat clarity and can be traced easily to their terminals. Inaddition to the Galen’s anastomosis, which is a well-knownneural connection between the ISLN and the RLN (Rue-ger, 1972; Williams et al., 1989), multiple anastomosesbetween the ISLN and the RLN within the human interary-tenoid (IA) muscle have been demonstrated by using

Sihler’s stain (Mu et al., 1994). In addition, some branchesof the ISLN appear to terminate the muscle fibers withinthe IA muscle. This finding indicates that the neuralcommunication between the RLN and the SLN is by nomeans limited to the Galen’s anastomosis, and it suggeststhat the ISLN probably also contains motor fibers thatsupply the IA muscle. In summary, Sihler’s stain appearsto show details of nerve distribution in human specimensthat cannot be seen with other methods. The presentinvestigation was initiated to determine the distributionand branching pattern of the human ISLN to further our

Fig. 2. Higher power view of left human ISLN processed with Sihler’s stain. Note that each division of theISLN subdivides into several secondary branches that form three groups: superior (S), middle (M), and inferior(I). A, arytenoid cartilage; AE, aryepiglottic fold. Arrow indicates the first branch of the inferior division of theISLN.

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understanding of the reflex activities of the upper airwayinitiated by the ISLN and for guiding sensory reinnerva-tion of the totally paralyzed larynx and possible futurehuman laryngeal transplantation.

MATERIALS AND METHODSFive adult human larynges and hypopharynges were

used for determining the branching and distribution pat-tern of the ISLN. The larynges were stained with modifiedSihler’s technique and were dissected under a dissectingmicroscope.

Modified Sihler’s StainThe larynges and hypopharynges were fixed for at least

4 weeks by immersion in 10% unneutralized formalin. Thefixed specimens were then immersed in 3% potassiumhydroxide solution for 3 weeks with several changes. Themacerated specimens were decalcified in Sihler’s solution I(1 part glacial acetic acid, 1 part glycerin, and 6 parts 1%aqueous chloral hydrate) for 2 weeks with several changes.The decalcified specimens were stained in Sihler’s solutionII (1 part stock Ehrlich’s hematoxylin, 1 part glycerin, and6 parts 1% aqueous chloral hydrate) for 4 weeks. Thestained specimens were destained in Sihler’s solution I forabout 3 hours. The destained specimens were then put into0.05% lithium carbonate solution for 1 hr to darken thenerves. Putting the specimens into 50% glycerin for 2 to 3days cleared the excess of stain. Finally, the clearedspecimens were kept in 100% glycerin with a few thymolcrystals for preservation and transparency.

Microdissection and PhotographyThe microdissection was composed of two steps. First,

the stained whole larynx was dissected under a dissectingmicroscope (OPMI 99; Zeiss, Thornwood, NY) at a magnifi-cation of 31.6 without removing any anatomical struc-tures. The ISLN on each side was followed through thethyrohyoid membrane to its terminals. After the majorperipheral course and branching of the ISLN were mappedout, the whole larynx was photographed. Second, most ofthe laryngeal cartilages were removed, and the individualparts supplied by the ISLN were dissected with the aid of adissecting microscope (TYP 355110; Wild, Heerbrugg, Swit-zerland) at a magnification of 310–30 by using microsurgi-cal instruments after transillumination by a Xenon lightsource (model 610; Karl Storz Endoscopy-America, Inc.,CA). The dissected specimens were photographed with anOM-4 Olympus camera (Tokyo, Japan) under transillumi-nation from a Xenon light source.

RESULTSIn this study, the peripheral nerve branching and distri-

bution of the human ISLN were illustrated clearly in thelarynges that were processed by modified Sihler’s stain. Inall dissections, the ISLN enters the larynx by way of thethyrohyoid membrane (Fig. 1). Shortly after it penetratesthe thyrohyoid membrane, the ISLN usually distributesinto three major divisions: the superior, middle, andinferior divisions. Each division then subdivides into twoto ten secondary nerve branches. In general, the superiordivision gives off two or three branches, the middle divi-

Fig. 3. Illustration of the superior and middle groups of nerve branches of the human ISLN. Note that thesuperior group (S) is composed of two secondary branches, and the middle group (M) is composed of four tosix secondary branches. The inferior division (I) is the thickest among the three divisions. E, epiglottis.

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sion gives off four to six branches (Figs. 2, 3), and theinferior division gives off eight to ten branches (Fig. 1).Therefore, three corresponding groups of the nervebranches were identified, and each of them supplies dis-tinct regions in the upper aerodigestive tract (Figs. 1–3).

Superior Division of the Human ISLNThe superior division of the human ISLN is composed of

two or three secondary branches and five to seven tertiarybranches (Figs. 2, 3). Only the most superior branchsupplies the lingual surface of the epiglottis and lateralglossoepiglottic fold. The others supply the laryngeal sur-face of the epiglottis. The nerve branches reach the laryn-geal surface of the epiglottis by penetrating the aryepiglot-tic fold. Usually, the secondary nerve branches on eachside run up in the lateral margin of the epiglottis. Duringtheir courses, they break up numerous fine twigs thatspread out to join with those from the opposite side. Theseinterlaced twigs form a complex network underlying themucosa, which extends over the laryngeal surface of theepiglottis (Fig. 3). The neural pattern in the laryngealsurface of the epiglottis is brought out more clearly underhigher magnification (Fig. 4). In contrast, the lingualsurface receives much less nerve supply than the laryngealsurface of the epiglottis.

Middle Division of the Human ISLNThe middle division of the human ISLN consists of four

to six secondary branches and many tertiary branches thatsupply the aryepiglottic fold, the mucosa above the vocalfold, the laryngeal vestibulum, and the posterolateralaspects of the arytenoid cartilage (Figs. 2, 3). The mucosaof the false and true vocal folds and the aryepiglottic foldsreceives a rich sensory nerve supply from the ISLN (Figs.5, 6). There are countless terminal twigs that connect witheach other, forming an extremely dense network in themucosa of the false and true vocal folds (Fig. 6).

Inferior Division of the Human ISLNThe inferior division of the human ISLN is composed of

eight to ten secondary branches and several dozen tertiarybranches. The inferior or descending division of the ISLNis the largest in diameter and runs the longest distance. Itruns downward in the medial wall of the pyriform sinusand breaks up eight to ten secondary branches, whichtravel medially (Fig. 1). The first branch of this groupsupplies the posterior part of the aryepiglottic fold and theouter side of the tip of the arytenoid cartilage (Figs. 1, 2,arrows), and the next two or three branches supply themucosa on the posterior surface of the arytenoid (Figs, 1, 7)

Fig. 4. Higher power view of the upper portion of the epiglottis (E) shown in Figure 3. Note that the terminalbranches supplying the laryngeal surface of the epiglottis connect with each other to form an extremely densenetwork.

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and innervate the IA muscle (Fig. 8). The arytenoid regionreceives a rich sensory nerve supply (Fig. 7). The second-ary branches that enter the IA muscle are subdivided intomore than ten tertiary branches, which supply the IAmuscle, the mucosa of the posterior wall of the glottis, themedial aspect of arytenoid cartilage, and the mucosa of theposterior subglottic region (Fig. 8). In the IA muscle,several neural anastomoses between the ISLN and theRLN were recognized on each side (Fig. 8, arrows). Theinferior division of the ISLN continues running down onthe posterior surface of the posterior cricoarytenoid muscle,where it gives off four to six secondary branches and

several dozen tertiary branches that supply the mucosa ofthe anterior wall of the hypopharynx and that are oftenseen in a brush-like arrangement (Fig. 1). Usually, theinferior division of the ISLN gives off a branch to join theposterior branch of the RLN, forming Galen’s anastomosis.

DISCUSSIONAt present, there is no detailed information about the

anatomy of the human ISLN. This report is the first todemonstrate the entire peripheral distribution of thehuman ISLN to the upper airway by using a wholemount

Fig. 5. Higher power view of the nerve supply of the right human aryepiglottic fold (AE). Note that thearyepiglottic fold receives a rich innervation from the middle division of the ISLN. A, arytenoid cartilage; E,epiglottis.

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nerve staining technique, Sihler’s stain. The most impor-tant findings provided by this study are that the humanISLN subdivides into three divisions, each supplying distinctregions. In addition, the laryngeal surface of the epiglottis,the false and true vocal folds, and the arytenoid regionhave rich sensory innervation. Finally, the ISLN appearsto contribute innervation to the IAmuscle. These neuroana-tomical data have clinical and physiological significance.

Branching Pattern of the Human ISLNand its Clinical Implications

Better knowledge of the branching pattern of the humanISLN in the upper airway will help in attempts at sensory

reinnervation for paralyzed or transplanted larynx. In thelate 1960s and early 1970s, Work and Boles (1965), Oguraet al., (1966), and Takenouki et al., (1967) pioneeredtransplantation of the canine larynx. Interest in laryngealtransplantation is currently increasing (Kluyskens andRingoir, 1970; Silver et al., 1970; Broniatowski, 1988;Broniatowski et al., 1989; Strome and Strome, 1994;Strome et al., 1994; Anthony et al., 1995, 1996; Weed et al.,1995; Birchall, 1997; Kevorkian et al., 1997), and the firsthuman laryngeal transplant was performed in January of1998 (Birchall, 1998). Laryngeal transplantation is desir-able and practical (Birchall, 1997), but one of the problemsthat needs to be solved is how to restore the motor and

Fig. 6. Higher power view of the sensory innervation of the right human false vocal fold (F) and the truevocal fold (T). Note that very delicate terminals derived from the middle division of the ISLN densely supply themucosa of the false and true vocal folds.

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sensory reinnervation (Birchall, 1997). Great progress inmotor reinnervation of the transplanted and paralyzedlarynx has been made by using the nerve-muscle pedicletechnique (Takenouki and Sato, 1968; Tucker, 1976), ansacervicalis-RLN anastomosis (Crumley, 1991), end-to-endRLN anastomosis (Sato and Ogura, 1978; Ezaki et al.,1982), and laryngeal pacing (Kaneko et al., 1985; Bronia-towski et al., 1990; Kojima et al., 1990; Sanders, 1991).These techniques for rehabilitating the movements of theparalyzed vocal cord are showing promise. However, littleprogress has been made regarding the sensory reinnerva-tion of the totally paralyzed or transplanted larynx. Sil-ver’s study (Silver et al., 1970) confirmed that sensoryinnervation is necessary to prevent aspiration.

Our anatomical findings are in good agreement withthose by Yatake (1965), who reported that the ISLN inhumans was divided into three main branches after pen-etrating the thyrohyoid membrane. This study has demon-strated that the nerve branches from the superior divisionof the ISLN run upward and supply the epiglottis. Thenerve branches from the middle division run horizontallyand innervate supraglottic mucosa. These two groups ofnerve branches branch off the ISLN shortly after it passesthrough the thyrohyoid foramen. In contrast, the inferiordivision of the ISLN is the largest in diameter and has themost complex distribution. At first, it runs medially andinferiorly to the level of the posterior end of the aryepiglot-

tic fold, where it gives off its first branch to the tip of thearytenoid cartilage and then it goes downward along thelateral side of the arytenoid, supplying the posteriorsurface of the arytenoid region and the IA muscle. Finally,it continues down to reach the laterosuperior aspect of theposterior cricoaryterioid (PCA) muscle, where it gives offfour to six secondary branches that supply the mucosa ofthe anterior wall of the hypopharynx. The junction of thearyepiglottic fold with the arytenoid cartilage appears tobe the dividing line of the innervation fields of the middleand inferior divisions of the ISLN.

In the surgical operation supraglottic laryngectomy, atleast one ISLN is removed, and aspiration is responsiblefor significant postoperative morbidity. Preservation of theISLN is very important, and clinical studies support thiscontention (Ward et al., 1977; Weaver and Fleming, 1978).The present study shows clearly that the superior divisionof the ISLN supplies the epiglottis and that the middledivision innervates the inside of the larynx. It is reason-able to say that these two divisions are responsible for theprotective function of the larynx. Therefore, reinnervationof the two divisions is essential for restoring the protectivereflex of the larynx. Knowing the branching pattern andsome key landmarks for localizing the major branches ofthe ISLN would be helpful during sensory reinnervation ofthe larynx.

Fig. 7. Higher power view of the sensory nerve supply of the human arytenoid region. Note that this area isinnervated by a dense plexus derived from the inferior division of the ISLN.

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Distribution Patterns of the Human ISLNand Some Physiological Considerations

Our findings are in line with the results reported byearlier investigators (Berlin and Lahey, 1929; Weeks andHinton, 1942; Kotby and Haugen, 1970; Meller, 1984;Tanaka, 1986) concerning the innervation of the IA muscleby way of the ISLN. This finding has been ignored entirelyor rejected by some investigators (Lemere, 1932a,b; Rue-ger, 1972), who reported that the ISLN passes through theIA muscle on its way to the mucosa of the larynx. Ourpresent and previous (Mu et al., 1994) studies demonstrate

that the inferior division of the ISLN gives off nervebranches to supply the IA muscle. Furthermore, multipleneural anastomoses between the ISLN and the RLNwithin the IA muscle suggest that axons pass between thetwo nerves. This would allow ISLN axons to pass into theRLN and innervate other laryngeal muscles. For example,observations of the nerve branch to the posterior cricoary-tenoid muscle show axons entering from the superiordirection (Sanders et al., 1995). The ISLN in humans mayfurnish motor fibers to the IA muscle. If this is true, thenthe significance of the double innervation of the IA muscle

Fig. 8. Higher power view of the nerve branches of the inferior division (I) of the ISLN that supply theinterarytenoid (IA) muscle, the posterior wall of the glottis (PG), and the posterior subglottic mucosa (SM) afterthe cricoid and arytenoid cartilages have been removed. Several neural anastomoses (arrows) between theISLN and the recurrent laryngeal nerve (RLN) within the IAmuscle are identified.A, part of the arytenoid cartilage.

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is possible evidence for explaining the positions of theparalyzed vocal cords and some neurophysiological andpathological conditions of the larynx.

In the light of our present knowledge of this subject, theISLN innervates the supraglottic mucosa (Negus, 1949;Ogura and Lam, 1953; Droulias et al., 1976; Meller, 1984;Williams et al., 1989; Garrett and Larson, 1991), and thesubglottic mucosa is supplied by the RLN (Lemere, 1932b;Negus, 1949; Suzuki and Kirchner, 1969; Meller, 1984; Wil-liams et al., 1989; Garrett and Larson, 1991) and by theESLN (Lemere, 1932a; Andrew, 1956; Suzuki and Kirchner,1968). However, our observations show that the inferiordivision of the human ISLN contributes innervation to theposterior subglottic mucosa. It seems reasonable to saythat the classical anatomical description that the ISLN sup-plies only the supraglottic mucosa needs a minor revision.

Distribution of the human ISLN is characterized by aconsistent pattern of regionalization. In other words, eachdivision of the ISLN is responsible for supplying sensationto a distinct anatomical region, although a small amount ofoverlapping innervation exists. The consistency of theregional supply suggests that nerve anastomosis to aparticular branch would reliably innervate the area thatthe branch is known to supply. Mechanoreceptors in thecat’s supraglottic mucosa were identified by recordingafferent impulses in the ISLN (Sampson and Eyzaguirre,1964). It is reasonable to predict that afferent dischargescould be recorded from filaments of the inferior divisionrather than from other divisions of the ISLN in response tosome stimuli applied to the posterior subglottic mucosa.

Innervation Density CorrelatesWith Other Studies

Many morphological studies on the sensory innervationof the larynx are directed to the description of the nerveendings and various receptors in the laryngeal mucosa(Konig and von Leden, 1961; Chiba et al., 1985; Watanabe,1985) as they are closely related to the laryngeal reflex(Storey, 1968; Harding et al., 1978). The present studydemonstrates that the density of the mucosal innervationis quite different from region to region. The most denseinnervation was found to be in the laryngeal surface of theepiglottis, the false and true vocal folds, and the arytenoidregion. Our findings concur with those observed in the catby using the HRP tracer technique (Tanaka, 1986; Yoshidaet al., 1986), physiological experiments, and clinical experi-ence. This suggests that the innervation density observedby using Sihler’s stain reflects the density of mechanorecep-tors. In addition, it appears that the distribution of mecha-noreceptors is not diffuse and homogeneous. Instead,sensory receptors and innervation density are concen-trated in relatively small key areas.

ACKNOWLEDGMENTSThe authors thank the Department of Pathology of the

Mount Sinai Medical Center for providing the humanlarynges for this study.

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