Clinical Anatomy 27:603–609 (2014)
ORIGINAL COMMUNICATION
Gross Anatomical Observations of Attachments of the Middle Pharyngeal Constrictor YUJIRO SAKAMOTO* Basic Sciences of Oral Health Care, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, Japan
The pharyngeal muscles overlap each other and some of their parts have different areas of origin. Such arrangements make the interrelationships among pharyngeal muscles complicated. This study investigated the attachments of the middle constrictor to clarify its configuration and re-examine its functions. The gross anatomies of the pharyngeal and neighboring muscles were examined in 41 cadavers. The middle constrictor arose from the stylohyoid ligament and the hyoid bone, and its fibers were divided into three overlapping groups. The anterosuperior group ascended posterosuperiorly from the ligament and the lesser horn and fanned out. The middle group ascended posterosuperiorly from the greater horn and fanned out. The posteroinferior group fanned out from the posterior part of the greater horn, while the middle constrictor arose internally to the hyoglossus; some fibers often passed externally, and their fibers sometimes intersected around the lingual artery, which ran between them. Some fibers attached to the hyoglossus, occasionally to the stylohyoid and the posterior belly of the digastric, but seldom to the lingual artery and the triticeal cartilage in the thyrohyoid ligament. The three groups were inserted into the pharyngeal raphe, and the descending fibers joined the longitudinal pharyngeal muscles. The ascending and descending fibers rarely reached the top of the pharynx and the thyroid cartilage, respectively. The fiber arrangement suggested that, besides constriction of the pharynx, the ascending and descending fibers of the middle constrictor can act as an elevator muscle, and the irregular attachments could affect the functions of the muscles and vessels. Clin. Anat. 27:603–609, 2014. VC 2013 Wiley Periodicals, Inc. Key words: middle constrictor; hyoglossus; stylohyoid; triticeal cartilage; lingual artery
INTRODUCTION The pharynx is a musculomembranous tube extending from the cranial base to the lower border of the cricoid cartilage. It is important for the swallowing (deglutition) reflex. The pharyngeal muscles comprise the following: circular muscles, which are the superior, middle, and inferior constrictors; and longitudinal elevator muscles, which are the stylopharyngeus, salpingopharyngeus, and palatopharyngeus (Thane, 1894; Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). The constrictors overlap one another and are inserted into the pharyngeal raphe; they consist of various parts because
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there can be considerable independence between the bundles of fibers coming from different areas of the origin line. This can complicate the interrelationships. *Correspondence to: Yujiro Sakamoto, Basic Sciences of Oral Health Care, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1–5-45 Yushima, Bunkyoku, Tokyo 113–8549, Japan. E-mail: [email protected] Received 7 September 2013; Revised 11 October 2013; Accepted 14 October 2013 Published online 17 December 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/ca.22344
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The chondropharyngeal and ceratopharyngeal parts of the middle constrictor arise from the lesser horn of the hyoid bone and the whole of the upper border of the greater horn, respectively (Blount and Lachman, 1953; Standring, 2005). The chondropharyngeal part also arises from the lower part of the stylohyoid ligament (Blount and Lachman, 1953; Standring, 2005). The middle constrictor can also receive fibers from the body of the hyoid bone, the tongue and the posterior part of the mylohyoid line of the mandible, and a slip from the lateral thyrohyoid ligament (the syndesmopharyngeus) is common (Thane, 1894). In addition, the uppermost fibers of the middle constrictor sometimes join the hyoglossus or the stylohyoid (Sakamoto, 2009). The function of the middle constrictor is to constrict the middle part of the pharynx involuntarily during swallowing (Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). The lingual artery passes between the middle constrictor and the hyoglossus. In contrast, the lingual vein has two routes: the dorsal lingual vein, which accompanies the lingual artery; and the deep lingual vein, which lies near the mucous membrane on the inferior surface of the tongue (Standring, 2005). Although the irregular fibers can affect the functions of the muscle and the vessels, the precise configuration of the middle constrictor has not been clarified. It is simpler than the superior constrictor, so it could have been overlooked as a subject for anatomical study. However, previous descriptions of the middle constrictor indicate variable morphology, which could be reflected in its functions. Precise gross anatomical information is necessary to corroborate knowledge of the function of a muscle and for accurate functional diagnosis. The purpose of this study was to investigate the configuration of the middle constrictor and its spatial relationships with neighboring muscles to re-examine its functions.
MATERIALS AND METHODS This study consisted of 82 sides of 41 Japanese cadavers (18 males and 23 females; average age 79.2 years), which were fixed in 8% formalin and preserved in 30% alcohol. The cadavers were donated to Tokyo Medical and Dental University for anatomical education and research. After general dissection of the head and neck, the mandible and the impeditive structures were carefully removed to expose the pharyngeal wall, and the attachments and the configuration of the middle constrictor and its spatial relationships with neighboring muscles, nerves, and blood vessels were examined in detail under a binocular microscope.
RESULTS The origin of the middle constrictor was identified as the superior surface of the greater horn of the hyoid bone, the lesser horn, and the inferior part of the stylohyoid ligament. The muscle fibers were divided into three groups, which fanned out and overlapped each other (Fig. 1a). The anterosuperior group
ascended posterosuperiorly from the ligament and the lesser horn. At the origin, some fibers joined the hyoglossus from the internal surface (Figs. 1a and 1b). The middle group ascended posterosuperiorly from the anterior part of the greater horn, and the posteroinferior group fanned out from the posterior part of the greater horn. The hyoglossus attached to the external surface of the greater horn, and the lingual artery and its accompanying vein coursed between the middle constrictor and the hyoglossus (Fig. 1c). However, some fibers in the middle group often passed externally to the blood vessels (Fig. 1b) or the vessels pierced the hyoglossus from the external surface in three sides (Fig. 1d). In addition, some fibers of the middle constrictor passed externally to the hyoglossus in 49 sides (Figs. 1d–1f). They attached to the greater horn or merged into the hyoglossus (27 and 29 sides, respectively), but these two attachments seldom coexisted (7 sides). In the case of external attachment, the fibers passed anterosuperiorly (25 sides) or posteroinferiorly (5 sides) to the blood vessels, or both (3 sides). The connecting fibers ran superior or inferior to the vessels (27 and 2 sides, respectively). In addition, some fibers of the middle constrictor joined the thyrohyoid in two sides (Fig. 1a). They passed externally to the hyoglossus or through the interval between the bundles of the hyoglossus. However, some superior fibers of the middle constrictor attached to the surface of the stylohyoid and the posterior belly of the digastric muscle in a grouping near their attachment to the hyoid bone in 33 sides, and some of them joined the stylohyoid but not the digastric in 7 sides (Figs. 2a and 2b). The lingual artery and its accompanying vein passed between this bundle and the greater horn to dive under the hyoglossus. Moreover, some fibers in the posteroinferior group attached to the lingual artery (one side) and the triticeal cartilage (one side) (Figs. 2c and 2d). The triticeal cartilage was identified within the lateral thyrohyoid ligament in 20 sides. Apart from the middle constrictor, some fibers of the hyoglossus arose from the cartilage and ascended internally or externally to the middle constrictor in five sides, and those of the stylopharyngeus were inserted into it in nine sides (Figs. 2e and 2f). However, no muscle attachment to the cartilage was found in the other five sides. The fibers of the middle constrictor as a whole ran posterosuperiorly and fanned out across the stylopharyngeus to be inserted primarily into the pharyngeal raphe, which is not always apparent (Fig. 3a). The superior fibers overlapped the superior constrictor, and the inferior fibers were overlapped with the inferior constrictor. However, some fibers interdigitated with those of the stylopharyngeus in four sides or ran internally to the superior constrictor in four sides or externally to the inferior in eight sides (Figs. 3b–3d). The glossopharyngeal nerve passed between the thyrohyoid ligament and the superior edge of the middle constrictor, but pierced the superior part of the constrictor in five sides (Fig. 3b). In the anterosuperior group, the anterior fibers were inserted into the superior part of the raphe, and more posterior fibers were sequentially inserted more
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Fig. 1. Right (a, e) and left (b–d, f) aspects of the pharynx. GPn, glossopharyngeal nerve; Hb, hyoid bone; HG, hyoglossus; IC, inferior constrictor; Lav, lingual artery and its accompanying vein; MC, middle constrictor; Pp, pharyngeal plexus; Stl, stylohyoid ligament; StP, stylopharyngeus; Tc, thyroid cartilage; TH, thyrohyoid. a (case 1), b (case 2): (HG and inferior constrictor were cut and moved to reveal the MC. Lab was removed in a). The MC fibers are divided into anterosuperior (A), middle (M),
and posteroinferior (P) groups (a). Some fibers of the A group join HG from the internal surface (black arrows). Some fibers of the M group join TH (white arrow in a) or pass externally to Lav (white arrow in b). c (case 3): The MC arises from Hb internally to HG. d (case 4), e, f (case 5): Lav pierces HG from the external surface (d). Some MC fibers run externally to HG (arrows). They pass posteroinferiorly (d) or anterosuperiorly (e) to Lav, or superiorly to Lav to merge into HG (f).
inferiorly. The top of the insertion reached the pharyngobasilar fascia just inferior to the pharyngeal tubercle of the occipital bone in five cadavers, and the inferior constrictor also reached it in two of the cadavers (Fig. 3e). In the middle group, the anterior fibers are attached to the superior part of the raphe, and more posterior ones sequentially to more inferior parts. The superior fibers in this group overlapped the inferior fibers of the anterosuperior group. However, in the posteroinferior group, the external fibers attached to the superior part of the pharyngeal raphe and more internal fibers sequentially attached to inferior part (Fig. 3f). The superior fibers in this group overlapped the inferior fibers of the middle group. In addition, the most posterior
fibers in the middle group and the most posterointernal fibers in the posteroinferior group descended to merge into the stylopharyngeus, the salpingopharyngeus and the palatopharyngeus (Figs. 3f and 4a). Furthermore, some descending fibers in the posteroinferior group attached to the external surface of the superior part of the thyroid cartilage posterior to the origin of the inferior constrictor in 10 sides, and some fibers occasionally joined the superior bundle of the inferior constrictor from the internal surface (Figs. 4a and 4b). The stylohyoid was inserted into the body of the hyoid bone, but a flat slip of the posterior fibers was inserted into the greater horn externally to the hyoglossus, away from the main bundle, in 14 sides
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Fig. 2. Left (a, e), right (b), right posterior (c), right posterolateral (d), and left posterolateral (f) aspects of the pharynx. Hb, hyoid bone; HG, hyoglossus; IC, inferior constrictor; La, lingual artery; MC, middle constrictor; PD, posterior belly of digastric; Pp, pharyngeal plexus; StH, stylohyoid; StP, stylopharyngeus; Tc, thyroid cartilage; Trc, triticeal cartilage. a (case 6), b (case 7): Superior MC fibers attach to StH and PD (black
arrows), and some of them merge into StH (white arrow in b). c (case 8), d (case 9): Some MC fibers attach to La (arrow in c) or Trc (black arrow in d). Some MC fibers pass externally to HG and anterosuperiorly to the vessels (white arrow in d). e (case 10): Some fibers of HG arise from Trc (arrow). f (case 11): (MC was cut and moved to show StP). Some fibers of StP are inserted into Trc (arrow).
(Figs. 4c and 4d). The hypoglossal nerve, which traveled externally to the hyoglossus and internally to the stylohyoid and the digastric, ran internally (10 sides) or externally (3 sides) to the posterior slip. In the internal cases, the thyrohyoid branch of the hypoglossal nerve passed externally to the slip (six sides), or between the main bundle and the slip (three sides), or pierced the slip (two sides).
the same time, some additional or irregular attachments at the origin and insertion and variations in the relationships with neighboring structures were revealed. Although the middle constrictor has been divided into two parts on the basis of differences in the origin, the findings of this study suggest that it can be divided into other groupings based on the arrangement of the fibers. This study indicated that the middle constrictor comprises three groups of fibers. The anterosuperior group ascended from the stylohyoid ligament and lesser horn and fanned out, the middle group ascended from the greater horn and fanned out, and the posteroinferior group fanned out from the greater horn. The middle group overlapped the anterosuperior and was overlapped by the posteroinferior. The middle
DISCUSSION This gross anatomical study investigated the configuration of the middle constrictor and reconfirmed that it arises from the hyoid bone and the stylohyoid ligament and is inserted into the pharyngeal raphe. At
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Fig. 3. Right posterior (a, b), left posterior (c), posterior (d, e), and right posterolateral (f) aspects of the pharynx. A, anterosuperior group; GPn, glossopharyngeal nerve; Hb, hyoid bone; IC, inferior constrictor; M, middle group; MC, middle constrictor; P, posteroinferior group; Pbf, pharyngobasilar fascia; Pp, pharyngeal plexus; Pr, pharyngeal raphe; Pt, pharyngeal tubercle; SC, superior constrictor; StP, stylopharyngeus; Tc, thyroid cartilage. a (case 12): The MC is inserted into Pr. The MC overlaps SC and is overlapped by IC. b (case 13): The MC (black arrows) and StP (white arrows) fibers interdigitate, and
GPn pierces the superior part of the MC (arrow head). The superior edge of MC was moved to reveal the interdigitation. c (case 14), d (case 13): Some SC and MC fibers pass externally to the MC (arrow in c) and IC (arrows in d), respectively. e (case 15): The insertions of MC (black arrows) and IC (white arrow) reach Pbf. f (case 16): (IC was cut and moved to reveal the MC). The external fibers of P attach to the superior part of Pr, more internal ones sequentially to more inferior parts (black arrows), and the most posterointernal fibers (white arrow) descend to merge into the longitudinal pharyngeal muscles (asterisk).
constrictor is inserted into the pharyngeal raphe (Thane, 1894; Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). At the same time, some fibers of the stylopharyngeus merge into the constrictors (Blount and Lachman, 1953; Standring, 2005), and the stylopharyngeus, salpingopharyngeus, and palatopharyngeus descend in close contact and blend with each other at the inferior part of the pharynx (Thane, 1894; Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). Furthermore, the superior constrictor and the palatopharyngeus are often interconnected or considerably entangled (Townshend, 1940; Harrington, 1944), and the upper fibers of the
superior constrictor are closely connected with the posterior fibers of the palatopharyngeus (McMyn, 1940). In this study, the middle constrictor was inserted into the pharyngeal raphe, and the descending fibers of the middle and posteroinferior groups merged into the longitudinal pharyngeal muscles. It seems that the palatopharyngeus connects with the superior constrictor at the superior part of the pharynx, and three longitudinal pharyngeal muscles as a whole join the descending fibers of the middle constrictor at the inferior part. However, the insertion of the most superior fibers reaches the basilar portion of the occipital bone (Blount and Lachman, 1953), and
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Fig. 4. Right posterior (a), left posterior (b), and left (c, d) aspects of the pharynx. Hb, hyoid bone; HG, hyoglossus; HGn, hypoglossal nerve; IC, inferior constrictor; MC, middle constrictor; PD, posterior belly of digastric; Pp, pharyngeal plexus; SLn, superior laryngeal nerve; StH, stylohyoid; Tc, thyroid cartilage; TH, thyrohyoid. a, b (case 17): (IC in a was cut and moved to reveal the MC). The most posterointernal fibers in the posteroinferior group (black arrow) descend to merge into the longitudinal pharyngeal muscles (asterisk), and some of the muscles attach to TC (white arrows) or connect to IC (arrow head in a). c (case 14), d (case 18): The posterior slip of StH attach to the greater horn (black arrows). HGn runs externally (c) or internally (d) to the posterior slip, and its TH branch pierces the slip in d (white arrows).
this study also demonstrated that the ascending fibers seldom reached the top of the pharynx. The inferior fibers descend to the lower end of the pharynx (Blount and Lachman, 1953; Standring, 2005). The descending fibers could possibly reach the bottom of the pharynx together with the longitudinal muscles. It was also found that the descending fibers occasionally attached to the thyroid cartilage. The middle constrictor constricts the middle part of the pharynx during swallowing (Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). However, the various directions of the fibers imply that the action of the middle constrictor differs among sites. This is the case with other fan-shaped muscles such as the trapezius and temporalis (Grant and Smith, 1953; Sinclair, 1972;
Johnson and Ellis, 2005; Standring, 2005). The actions of the superior and inferior fibers in the former and the posterior fibers in the latter can differ from that of the muscle as a whole depending on the situation. It is reasonable to infer that the three groups of fibers together constrict the pharynx in collaboration with the contralateral muscle. It is possible that the ascending fibers, especially in the anterosuperior group, elevate the hyoid bone, while the descending fibers, especially in the middle and posteroinferior groups, elevate the inferior part of the pharynx. If the ascending fibers do not act, the descending fibers could pull down the hyoid bone. The middle constrictor is likely to be not only a circular sphincter muscle but also a longitudinal elevator muscle. The middle constrictor and the hyoglossus arose from the superior and external surfaces of the greater horn, respectively, and the lingual artery and its accompanying vein coursed between them. The fibers of the middle constrictor in this region ascended posterosuperiorly in parallel with these blood vessels and did not intersect with those of the hyoglossus over the vessels. For these reasons, the interval between the middle constrictor and the hyoglossus seems to be a neutral zone during muscular activity. However, their positional relationships varied in this study. Some fibers in the middle group frequently passed externally to the vessels, and those of the middle constrictor often passed externally to the hyoglossus. In addition, the vessels seldom pierced the hyoglossus. In these cases, the fibers of the middle constrictor and the hyoglossus crossed each other around the vessels, which could therefore be squeezed by the muscles. Because the lingual vein has two routes passing internally and externally to the hyoglossus, the venous blood can flow through the external route. However, arterial flow could be retarded during their activity. Moreover, some fibers attached to the lingual artery in only a few cases; in these cases, the arterial flow would be affected by muscle activity. However, it has been reported that the middle constrictor sometimes attaches to the anterior and posterior parts of the greater horn with separation into two bundles (Sonoda and Tamatsu, 2008). This previous finding could reflect the variation found in the present study. Otherwise, the glossopharyngeal nerve seldom pierced the middle constrictor. It was also found that a slip of the posterior fibers of the stylohyoid occasionally attached to the greater horn, and the thyrohyoid branch of the hypoglossal nerve pierced the slip in some cases. In such cases, muscular activity would strain the nerves and could affect their function. The middle constrictor can receive fibers from the body of the hyoid bone, the tongue, and the posterior part of the mylohyoid line of the mandible, and the posterior belly of the digastric can be connected by a slip to the middle or inferior constrictor (Thane, 1894). Although attachment to the mandible was not confirmed in this study, some fibers of the anterosuperior group joined the hyoglossus, indicating a connection with the tongue. In addition, the superior fibers of the middle constrictor sometimes attach to the stylohyoid and the posterior belly in a lump. Because this was found near their attachment to the
The Attachments of the Middle Constrictor hyoid bone, some such fibers can attach to the body of the hyoid bone. The stylohyoid can also be duplicated, and the second slip varies in its insertion, sometimes inserting into the lesser horn of the hyoid bone, or accompanying or replacing the stylohyoid ligament (Thane, 1894; Grant and Smith, 1953; Bergman et al., 1988). Furthermore, there is a close relationship between the stylohyoid and the posterior belly of digastric, and they can fuse with one another (Grant and Smith, 1953; Bergman et al., 1988). The stylohyoid and the posterior belly are probably used as a muscle attachment site instead of the ligament, and their close relationship causes this attachment. However, some fibers occasionally joined the stylohyoid but not the posterior belly in this study. Because the former, arising from the styloid process, is more parallel to the ligament than the latter, the fibers of the middle constrictor could easily join the former. The findings imply that the anterior region of the origin is not always sufficient as the attachment site for the anterosuperior group. It was also found that some fibers of the middle constrictor seldom join the thyrohyoid and sometimes interdigitate with those of the superior and inferior constrictors and the stylopharyngeus. In these situations, the muscles pull each other, potentially affecting their independence of function or promoting their interactions. A slip from the lateral thyrohyoid ligament is common in the middle constrictor (Thane, 1894), and some fibers arose from the lateral thyrohyoid ligament in one side. They attached to the triticeal cartilage, which was identified in 20 sides (24.4%) in this study. The triticeal cartilage is found within the posterior free edge of the thyrohyoid membrane, lateral thyrohyoid ligament, about half way between the superior horn of the thyroid cartilage and the tip of the greater horn of the hyoid bone (Standring, 2005). Its functions are unknown, although they could serve to strengthen this connection. This study demonstrated that some fibers of the hyoglossus or stylopharyngeus, also linked to it though muscle attachment, were absent in five sides. The findings imply that one function of the triticeal cartilage is as a muscle attachment site. Consequently, the middle constrictor consists of three overlapping groups of fibers that display a fan-shaped arrangement: the anterosuperior, middle, and posteroinferior groups. The differing fiber directions imply that the fibers also differ in their actions within their different sites. The findings suggest that the middle constrictor acts not only as a circular
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sphincter muscle but also as a longitudinal elevator muscle, and it could play an important role as the coordinator between the circular and longitudinal pharyngeal muscles for the sequential actions constituting the swallowing reflex. Although these suggestions are derived from morphological observations in this study, they are likely to be beneficial for functional and clinical analyses of the pharynx.
ACKNOWLEDGMENTS The author does not have any conflict of interest. The author expresses special thanks to the donors of the cadavers used in this study.
REFERENCES Bergman RA, Thompson SA, Afifi AK, Saadeh FA. 1988. Muscles. In: Bergman RA, Thompson SA, Afifi AK, Saadeh FA, editors. Compendium of Human Anatomic Variation: Text, Atlas, and World Literature. Baltimore, Munich: Urban & Schwarzenberg. p 1–56. Blount RF, Lachman E. 1953. The digestive system. In: Schaeffer JP, editor. Morris’ Human Anatomy. 11th Ed. Toronto: The Blakiston Company. p 1292–1424. Grant JCB, Smith CG. 1953. The musculature. In: Schaeffer JP, editor. Morris’ Human Anatomy. 11th Ed. Toronto: The Blakiston Company. p 399–609. Harrington R. 1944. A study of the mechanism of velopharyngeal closure. J Speech Dis 9:325–345. Johnson D, Ellis H. 2005. Pectoral girdle and upper limb. In: Standring S, Ellis H, Healy JC, Johnson D, Williams A, editors. Gray’s Anatomy. 39th Ed. Edinburgh: Elsevier Churchill Livingstone. p 799–942. McMyn JK. 1940. The anatomy of the salpingo-pharyngeus muscle. J Laryngol Otol 55:1–22. Sakamoto Y. 2009. Classification of pharyngeal muscles based on innervations from glossopharyngeal and vagus nerves in human. Surg Radiol Anat 31:755–761. Sinclair DC. 1972. Muscles and fasciae. In: Romanes GJ, editor. Cunningham’s Textbook of Anatomy. 11th Ed. London: Oxford University Press. p 259–397. Sonoda N, Tamatsu Y. 2008. Observation on the attachment of muscles onto the hyoid bone in human adults. Okajimas Folia Anat Jpn 85:79–90. Standring S. 2005. Head and neck. In: Standring S, Ellis H, Healy JC, Johnson D, Williams A, editors. Gray’s Anatomy. 39th Ed. Edinburgh: Elsevier Churchill Livingstone. p 439–723. € fer EA, Thane GD, editors. Thane GD. 1894. Myology. In: Schfera Quain’s Elements of Anatomy. 10th Ed. New York: Longman Green and Co. p 199–350. Townshend RH. 1940. The formation of passavant’s bar. J Laryngol Otol 55:154–165.
ORIGINAL COMMUNICATION
Gross Anatomical Observations of Attachments of the Middle Pharyngeal Constrictor YUJIRO SAKAMOTO* Basic Sciences of Oral Health Care, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, Japan
The pharyngeal muscles overlap each other and some of their parts have different areas of origin. Such arrangements make the interrelationships among pharyngeal muscles complicated. This study investigated the attachments of the middle constrictor to clarify its configuration and re-examine its functions. The gross anatomies of the pharyngeal and neighboring muscles were examined in 41 cadavers. The middle constrictor arose from the stylohyoid ligament and the hyoid bone, and its fibers were divided into three overlapping groups. The anterosuperior group ascended posterosuperiorly from the ligament and the lesser horn and fanned out. The middle group ascended posterosuperiorly from the greater horn and fanned out. The posteroinferior group fanned out from the posterior part of the greater horn, while the middle constrictor arose internally to the hyoglossus; some fibers often passed externally, and their fibers sometimes intersected around the lingual artery, which ran between them. Some fibers attached to the hyoglossus, occasionally to the stylohyoid and the posterior belly of the digastric, but seldom to the lingual artery and the triticeal cartilage in the thyrohyoid ligament. The three groups were inserted into the pharyngeal raphe, and the descending fibers joined the longitudinal pharyngeal muscles. The ascending and descending fibers rarely reached the top of the pharynx and the thyroid cartilage, respectively. The fiber arrangement suggested that, besides constriction of the pharynx, the ascending and descending fibers of the middle constrictor can act as an elevator muscle, and the irregular attachments could affect the functions of the muscles and vessels. Clin. Anat. 27:603–609, 2014. VC 2013 Wiley Periodicals, Inc. Key words: middle constrictor; hyoglossus; stylohyoid; triticeal cartilage; lingual artery
INTRODUCTION The pharynx is a musculomembranous tube extending from the cranial base to the lower border of the cricoid cartilage. It is important for the swallowing (deglutition) reflex. The pharyngeal muscles comprise the following: circular muscles, which are the superior, middle, and inferior constrictors; and longitudinal elevator muscles, which are the stylopharyngeus, salpingopharyngeus, and palatopharyngeus (Thane, 1894; Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). The constrictors overlap one another and are inserted into the pharyngeal raphe; they consist of various parts because
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there can be considerable independence between the bundles of fibers coming from different areas of the origin line. This can complicate the interrelationships. *Correspondence to: Yujiro Sakamoto, Basic Sciences of Oral Health Care, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1–5-45 Yushima, Bunkyoku, Tokyo 113–8549, Japan. E-mail: [email protected] Received 7 September 2013; Revised 11 October 2013; Accepted 14 October 2013 Published online 17 December 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/ca.22344
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The chondropharyngeal and ceratopharyngeal parts of the middle constrictor arise from the lesser horn of the hyoid bone and the whole of the upper border of the greater horn, respectively (Blount and Lachman, 1953; Standring, 2005). The chondropharyngeal part also arises from the lower part of the stylohyoid ligament (Blount and Lachman, 1953; Standring, 2005). The middle constrictor can also receive fibers from the body of the hyoid bone, the tongue and the posterior part of the mylohyoid line of the mandible, and a slip from the lateral thyrohyoid ligament (the syndesmopharyngeus) is common (Thane, 1894). In addition, the uppermost fibers of the middle constrictor sometimes join the hyoglossus or the stylohyoid (Sakamoto, 2009). The function of the middle constrictor is to constrict the middle part of the pharynx involuntarily during swallowing (Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). The lingual artery passes between the middle constrictor and the hyoglossus. In contrast, the lingual vein has two routes: the dorsal lingual vein, which accompanies the lingual artery; and the deep lingual vein, which lies near the mucous membrane on the inferior surface of the tongue (Standring, 2005). Although the irregular fibers can affect the functions of the muscle and the vessels, the precise configuration of the middle constrictor has not been clarified. It is simpler than the superior constrictor, so it could have been overlooked as a subject for anatomical study. However, previous descriptions of the middle constrictor indicate variable morphology, which could be reflected in its functions. Precise gross anatomical information is necessary to corroborate knowledge of the function of a muscle and for accurate functional diagnosis. The purpose of this study was to investigate the configuration of the middle constrictor and its spatial relationships with neighboring muscles to re-examine its functions.
MATERIALS AND METHODS This study consisted of 82 sides of 41 Japanese cadavers (18 males and 23 females; average age 79.2 years), which were fixed in 8% formalin and preserved in 30% alcohol. The cadavers were donated to Tokyo Medical and Dental University for anatomical education and research. After general dissection of the head and neck, the mandible and the impeditive structures were carefully removed to expose the pharyngeal wall, and the attachments and the configuration of the middle constrictor and its spatial relationships with neighboring muscles, nerves, and blood vessels were examined in detail under a binocular microscope.
RESULTS The origin of the middle constrictor was identified as the superior surface of the greater horn of the hyoid bone, the lesser horn, and the inferior part of the stylohyoid ligament. The muscle fibers were divided into three groups, which fanned out and overlapped each other (Fig. 1a). The anterosuperior group
ascended posterosuperiorly from the ligament and the lesser horn. At the origin, some fibers joined the hyoglossus from the internal surface (Figs. 1a and 1b). The middle group ascended posterosuperiorly from the anterior part of the greater horn, and the posteroinferior group fanned out from the posterior part of the greater horn. The hyoglossus attached to the external surface of the greater horn, and the lingual artery and its accompanying vein coursed between the middle constrictor and the hyoglossus (Fig. 1c). However, some fibers in the middle group often passed externally to the blood vessels (Fig. 1b) or the vessels pierced the hyoglossus from the external surface in three sides (Fig. 1d). In addition, some fibers of the middle constrictor passed externally to the hyoglossus in 49 sides (Figs. 1d–1f). They attached to the greater horn or merged into the hyoglossus (27 and 29 sides, respectively), but these two attachments seldom coexisted (7 sides). In the case of external attachment, the fibers passed anterosuperiorly (25 sides) or posteroinferiorly (5 sides) to the blood vessels, or both (3 sides). The connecting fibers ran superior or inferior to the vessels (27 and 2 sides, respectively). In addition, some fibers of the middle constrictor joined the thyrohyoid in two sides (Fig. 1a). They passed externally to the hyoglossus or through the interval between the bundles of the hyoglossus. However, some superior fibers of the middle constrictor attached to the surface of the stylohyoid and the posterior belly of the digastric muscle in a grouping near their attachment to the hyoid bone in 33 sides, and some of them joined the stylohyoid but not the digastric in 7 sides (Figs. 2a and 2b). The lingual artery and its accompanying vein passed between this bundle and the greater horn to dive under the hyoglossus. Moreover, some fibers in the posteroinferior group attached to the lingual artery (one side) and the triticeal cartilage (one side) (Figs. 2c and 2d). The triticeal cartilage was identified within the lateral thyrohyoid ligament in 20 sides. Apart from the middle constrictor, some fibers of the hyoglossus arose from the cartilage and ascended internally or externally to the middle constrictor in five sides, and those of the stylopharyngeus were inserted into it in nine sides (Figs. 2e and 2f). However, no muscle attachment to the cartilage was found in the other five sides. The fibers of the middle constrictor as a whole ran posterosuperiorly and fanned out across the stylopharyngeus to be inserted primarily into the pharyngeal raphe, which is not always apparent (Fig. 3a). The superior fibers overlapped the superior constrictor, and the inferior fibers were overlapped with the inferior constrictor. However, some fibers interdigitated with those of the stylopharyngeus in four sides or ran internally to the superior constrictor in four sides or externally to the inferior in eight sides (Figs. 3b–3d). The glossopharyngeal nerve passed between the thyrohyoid ligament and the superior edge of the middle constrictor, but pierced the superior part of the constrictor in five sides (Fig. 3b). In the anterosuperior group, the anterior fibers were inserted into the superior part of the raphe, and more posterior fibers were sequentially inserted more
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Fig. 1. Right (a, e) and left (b–d, f) aspects of the pharynx. GPn, glossopharyngeal nerve; Hb, hyoid bone; HG, hyoglossus; IC, inferior constrictor; Lav, lingual artery and its accompanying vein; MC, middle constrictor; Pp, pharyngeal plexus; Stl, stylohyoid ligament; StP, stylopharyngeus; Tc, thyroid cartilage; TH, thyrohyoid. a (case 1), b (case 2): (HG and inferior constrictor were cut and moved to reveal the MC. Lab was removed in a). The MC fibers are divided into anterosuperior (A), middle (M),
and posteroinferior (P) groups (a). Some fibers of the A group join HG from the internal surface (black arrows). Some fibers of the M group join TH (white arrow in a) or pass externally to Lav (white arrow in b). c (case 3): The MC arises from Hb internally to HG. d (case 4), e, f (case 5): Lav pierces HG from the external surface (d). Some MC fibers run externally to HG (arrows). They pass posteroinferiorly (d) or anterosuperiorly (e) to Lav, or superiorly to Lav to merge into HG (f).
inferiorly. The top of the insertion reached the pharyngobasilar fascia just inferior to the pharyngeal tubercle of the occipital bone in five cadavers, and the inferior constrictor also reached it in two of the cadavers (Fig. 3e). In the middle group, the anterior fibers are attached to the superior part of the raphe, and more posterior ones sequentially to more inferior parts. The superior fibers in this group overlapped the inferior fibers of the anterosuperior group. However, in the posteroinferior group, the external fibers attached to the superior part of the pharyngeal raphe and more internal fibers sequentially attached to inferior part (Fig. 3f). The superior fibers in this group overlapped the inferior fibers of the middle group. In addition, the most posterior
fibers in the middle group and the most posterointernal fibers in the posteroinferior group descended to merge into the stylopharyngeus, the salpingopharyngeus and the palatopharyngeus (Figs. 3f and 4a). Furthermore, some descending fibers in the posteroinferior group attached to the external surface of the superior part of the thyroid cartilage posterior to the origin of the inferior constrictor in 10 sides, and some fibers occasionally joined the superior bundle of the inferior constrictor from the internal surface (Figs. 4a and 4b). The stylohyoid was inserted into the body of the hyoid bone, but a flat slip of the posterior fibers was inserted into the greater horn externally to the hyoglossus, away from the main bundle, in 14 sides
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Fig. 2. Left (a, e), right (b), right posterior (c), right posterolateral (d), and left posterolateral (f) aspects of the pharynx. Hb, hyoid bone; HG, hyoglossus; IC, inferior constrictor; La, lingual artery; MC, middle constrictor; PD, posterior belly of digastric; Pp, pharyngeal plexus; StH, stylohyoid; StP, stylopharyngeus; Tc, thyroid cartilage; Trc, triticeal cartilage. a (case 6), b (case 7): Superior MC fibers attach to StH and PD (black
arrows), and some of them merge into StH (white arrow in b). c (case 8), d (case 9): Some MC fibers attach to La (arrow in c) or Trc (black arrow in d). Some MC fibers pass externally to HG and anterosuperiorly to the vessels (white arrow in d). e (case 10): Some fibers of HG arise from Trc (arrow). f (case 11): (MC was cut and moved to show StP). Some fibers of StP are inserted into Trc (arrow).
(Figs. 4c and 4d). The hypoglossal nerve, which traveled externally to the hyoglossus and internally to the stylohyoid and the digastric, ran internally (10 sides) or externally (3 sides) to the posterior slip. In the internal cases, the thyrohyoid branch of the hypoglossal nerve passed externally to the slip (six sides), or between the main bundle and the slip (three sides), or pierced the slip (two sides).
the same time, some additional or irregular attachments at the origin and insertion and variations in the relationships with neighboring structures were revealed. Although the middle constrictor has been divided into two parts on the basis of differences in the origin, the findings of this study suggest that it can be divided into other groupings based on the arrangement of the fibers. This study indicated that the middle constrictor comprises three groups of fibers. The anterosuperior group ascended from the stylohyoid ligament and lesser horn and fanned out, the middle group ascended from the greater horn and fanned out, and the posteroinferior group fanned out from the greater horn. The middle group overlapped the anterosuperior and was overlapped by the posteroinferior. The middle
DISCUSSION This gross anatomical study investigated the configuration of the middle constrictor and reconfirmed that it arises from the hyoid bone and the stylohyoid ligament and is inserted into the pharyngeal raphe. At
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Fig. 3. Right posterior (a, b), left posterior (c), posterior (d, e), and right posterolateral (f) aspects of the pharynx. A, anterosuperior group; GPn, glossopharyngeal nerve; Hb, hyoid bone; IC, inferior constrictor; M, middle group; MC, middle constrictor; P, posteroinferior group; Pbf, pharyngobasilar fascia; Pp, pharyngeal plexus; Pr, pharyngeal raphe; Pt, pharyngeal tubercle; SC, superior constrictor; StP, stylopharyngeus; Tc, thyroid cartilage. a (case 12): The MC is inserted into Pr. The MC overlaps SC and is overlapped by IC. b (case 13): The MC (black arrows) and StP (white arrows) fibers interdigitate, and
GPn pierces the superior part of the MC (arrow head). The superior edge of MC was moved to reveal the interdigitation. c (case 14), d (case 13): Some SC and MC fibers pass externally to the MC (arrow in c) and IC (arrows in d), respectively. e (case 15): The insertions of MC (black arrows) and IC (white arrow) reach Pbf. f (case 16): (IC was cut and moved to reveal the MC). The external fibers of P attach to the superior part of Pr, more internal ones sequentially to more inferior parts (black arrows), and the most posterointernal fibers (white arrow) descend to merge into the longitudinal pharyngeal muscles (asterisk).
constrictor is inserted into the pharyngeal raphe (Thane, 1894; Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). At the same time, some fibers of the stylopharyngeus merge into the constrictors (Blount and Lachman, 1953; Standring, 2005), and the stylopharyngeus, salpingopharyngeus, and palatopharyngeus descend in close contact and blend with each other at the inferior part of the pharynx (Thane, 1894; Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). Furthermore, the superior constrictor and the palatopharyngeus are often interconnected or considerably entangled (Townshend, 1940; Harrington, 1944), and the upper fibers of the
superior constrictor are closely connected with the posterior fibers of the palatopharyngeus (McMyn, 1940). In this study, the middle constrictor was inserted into the pharyngeal raphe, and the descending fibers of the middle and posteroinferior groups merged into the longitudinal pharyngeal muscles. It seems that the palatopharyngeus connects with the superior constrictor at the superior part of the pharynx, and three longitudinal pharyngeal muscles as a whole join the descending fibers of the middle constrictor at the inferior part. However, the insertion of the most superior fibers reaches the basilar portion of the occipital bone (Blount and Lachman, 1953), and
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Fig. 4. Right posterior (a), left posterior (b), and left (c, d) aspects of the pharynx. Hb, hyoid bone; HG, hyoglossus; HGn, hypoglossal nerve; IC, inferior constrictor; MC, middle constrictor; PD, posterior belly of digastric; Pp, pharyngeal plexus; SLn, superior laryngeal nerve; StH, stylohyoid; Tc, thyroid cartilage; TH, thyrohyoid. a, b (case 17): (IC in a was cut and moved to reveal the MC). The most posterointernal fibers in the posteroinferior group (black arrow) descend to merge into the longitudinal pharyngeal muscles (asterisk), and some of the muscles attach to TC (white arrows) or connect to IC (arrow head in a). c (case 14), d (case 18): The posterior slip of StH attach to the greater horn (black arrows). HGn runs externally (c) or internally (d) to the posterior slip, and its TH branch pierces the slip in d (white arrows).
this study also demonstrated that the ascending fibers seldom reached the top of the pharynx. The inferior fibers descend to the lower end of the pharynx (Blount and Lachman, 1953; Standring, 2005). The descending fibers could possibly reach the bottom of the pharynx together with the longitudinal muscles. It was also found that the descending fibers occasionally attached to the thyroid cartilage. The middle constrictor constricts the middle part of the pharynx during swallowing (Blount and Lachman, 1953; Sinclair, 1972; Standring, 2005). However, the various directions of the fibers imply that the action of the middle constrictor differs among sites. This is the case with other fan-shaped muscles such as the trapezius and temporalis (Grant and Smith, 1953; Sinclair, 1972;
Johnson and Ellis, 2005; Standring, 2005). The actions of the superior and inferior fibers in the former and the posterior fibers in the latter can differ from that of the muscle as a whole depending on the situation. It is reasonable to infer that the three groups of fibers together constrict the pharynx in collaboration with the contralateral muscle. It is possible that the ascending fibers, especially in the anterosuperior group, elevate the hyoid bone, while the descending fibers, especially in the middle and posteroinferior groups, elevate the inferior part of the pharynx. If the ascending fibers do not act, the descending fibers could pull down the hyoid bone. The middle constrictor is likely to be not only a circular sphincter muscle but also a longitudinal elevator muscle. The middle constrictor and the hyoglossus arose from the superior and external surfaces of the greater horn, respectively, and the lingual artery and its accompanying vein coursed between them. The fibers of the middle constrictor in this region ascended posterosuperiorly in parallel with these blood vessels and did not intersect with those of the hyoglossus over the vessels. For these reasons, the interval between the middle constrictor and the hyoglossus seems to be a neutral zone during muscular activity. However, their positional relationships varied in this study. Some fibers in the middle group frequently passed externally to the vessels, and those of the middle constrictor often passed externally to the hyoglossus. In addition, the vessels seldom pierced the hyoglossus. In these cases, the fibers of the middle constrictor and the hyoglossus crossed each other around the vessels, which could therefore be squeezed by the muscles. Because the lingual vein has two routes passing internally and externally to the hyoglossus, the venous blood can flow through the external route. However, arterial flow could be retarded during their activity. Moreover, some fibers attached to the lingual artery in only a few cases; in these cases, the arterial flow would be affected by muscle activity. However, it has been reported that the middle constrictor sometimes attaches to the anterior and posterior parts of the greater horn with separation into two bundles (Sonoda and Tamatsu, 2008). This previous finding could reflect the variation found in the present study. Otherwise, the glossopharyngeal nerve seldom pierced the middle constrictor. It was also found that a slip of the posterior fibers of the stylohyoid occasionally attached to the greater horn, and the thyrohyoid branch of the hypoglossal nerve pierced the slip in some cases. In such cases, muscular activity would strain the nerves and could affect their function. The middle constrictor can receive fibers from the body of the hyoid bone, the tongue, and the posterior part of the mylohyoid line of the mandible, and the posterior belly of the digastric can be connected by a slip to the middle or inferior constrictor (Thane, 1894). Although attachment to the mandible was not confirmed in this study, some fibers of the anterosuperior group joined the hyoglossus, indicating a connection with the tongue. In addition, the superior fibers of the middle constrictor sometimes attach to the stylohyoid and the posterior belly in a lump. Because this was found near their attachment to the
The Attachments of the Middle Constrictor hyoid bone, some such fibers can attach to the body of the hyoid bone. The stylohyoid can also be duplicated, and the second slip varies in its insertion, sometimes inserting into the lesser horn of the hyoid bone, or accompanying or replacing the stylohyoid ligament (Thane, 1894; Grant and Smith, 1953; Bergman et al., 1988). Furthermore, there is a close relationship between the stylohyoid and the posterior belly of digastric, and they can fuse with one another (Grant and Smith, 1953; Bergman et al., 1988). The stylohyoid and the posterior belly are probably used as a muscle attachment site instead of the ligament, and their close relationship causes this attachment. However, some fibers occasionally joined the stylohyoid but not the posterior belly in this study. Because the former, arising from the styloid process, is more parallel to the ligament than the latter, the fibers of the middle constrictor could easily join the former. The findings imply that the anterior region of the origin is not always sufficient as the attachment site for the anterosuperior group. It was also found that some fibers of the middle constrictor seldom join the thyrohyoid and sometimes interdigitate with those of the superior and inferior constrictors and the stylopharyngeus. In these situations, the muscles pull each other, potentially affecting their independence of function or promoting their interactions. A slip from the lateral thyrohyoid ligament is common in the middle constrictor (Thane, 1894), and some fibers arose from the lateral thyrohyoid ligament in one side. They attached to the triticeal cartilage, which was identified in 20 sides (24.4%) in this study. The triticeal cartilage is found within the posterior free edge of the thyrohyoid membrane, lateral thyrohyoid ligament, about half way between the superior horn of the thyroid cartilage and the tip of the greater horn of the hyoid bone (Standring, 2005). Its functions are unknown, although they could serve to strengthen this connection. This study demonstrated that some fibers of the hyoglossus or stylopharyngeus, also linked to it though muscle attachment, were absent in five sides. The findings imply that one function of the triticeal cartilage is as a muscle attachment site. Consequently, the middle constrictor consists of three overlapping groups of fibers that display a fan-shaped arrangement: the anterosuperior, middle, and posteroinferior groups. The differing fiber directions imply that the fibers also differ in their actions within their different sites. The findings suggest that the middle constrictor acts not only as a circular
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sphincter muscle but also as a longitudinal elevator muscle, and it could play an important role as the coordinator between the circular and longitudinal pharyngeal muscles for the sequential actions constituting the swallowing reflex. Although these suggestions are derived from morphological observations in this study, they are likely to be beneficial for functional and clinical analyses of the pharynx.
ACKNOWLEDGMENTS The author does not have any conflict of interest. The author expresses special thanks to the donors of the cadavers used in this study.
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