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Home , Ansa cervicalis, Lesser occipital nerve, Sternohyoid muscle

Okajimas Folia Anat. Jpn., 69(6): 361-368, March, 1993

A Case of the Human Sternocleidomastoid Muscle Additionally Innervated by the Hypoglossal

By

Masahiro KOIZUMI, Masaharu HORIGUCHI, Shin'ichi SEKIYA, Sumio ISOGAI and Masato NAKANO

Department of Anatomy, Iwate Medical University School of Medicine. Morioka, 020 Japan

-Received for Publication, October 19, 1992-

Key Words: Sternocleidomastoid muscle, , Superior sternoclavicular muscle (Hyrtl), Dual nerve supply, Gross anatomy

Summary: An anomalous nerve supply from the hypoglossal nerve (XII) to the sternocleidomastoid muscle (SM) was observed in the right of an 82-year-old Japanese female. This nerve branch arose from the hypoglossal nerve at the origin of the superior root of the . The nerve fiber analysis revealed that this branch consisted of fibers from the hypoglossal nerve, the first and the second cervical and had the same component as the superior root of the ansa cervicalis. SM appeared quite normal and the most part was innervated by the accessory nerve and a branch from the . The anomalous branch from XII supplied the small deep area near the anterior margin of the middle of the sternomastoid portion of SM. It is reasonable to think that the small deep area of SM, which was innervated by the anomalous branch from XII, occurs as the result of fusion of the muscular component from . If the muscular component does not fuse with SM, it is thought to appear as an aberrant muscle such as the superior sternoclavicular muscle (Hyrtl) which is also supplied from a branch of the superior root of the ansa cervicalis.

The human sternocleidomastoid muscle is usually and subsequently some motor fibers in the accessory innervated by the accessory nerve and a branch from nerve also migrated to the cervical nerves. the cervical plexus. During the student course of On the other hand, some authors cast doubt on gross anatomy dissection at Iwate Medical University this migration (Kumaki, 1970) and understood this School of Medicine in 1992, in addition to this dual independent motor supply to a deep portion of SM innervation, a rare nerve supply from a branch of of the cervical nerve was due to the fact that the deep the hypoglossal nerve was observed in the right neck portion of SM derived from the myotome and was of an 82-year-old Japanese female who had expired probably homologous with the omocervicalis muscle from cerebral infarction. found in most other mammals (McKenzie, 1962). The dual innervation of SM by two different In our case, the anomalous nerve branch to SM nerves, one from the eleventh cranial nerve (accessory originated from the hypoglossal nerve, the twelfth nerve) and the other from the sternocleidomastoid cranial nerve. Phylogenetically the hypoglossal nerve branch from the cervical plexus (the ), is understood to be originally the uppermost motor is well-known and has been discussed among many roots of the spinal nerve which are taken into the anatomists. It is widely accepted that the access- cranium at a later stage (Streeter, 1905). Therefore, ory nerve is motor and the sternocleidomastoid our findings also suggest the intimate relationship branch is mostly sensory. However, the finding between SM and cervical muscles which was of that a branch from the cervical plexus sometimes myotomic origin. innervates independently a part of SM confirms From this point of view, our findings are con- the motor supply to SM through the cervical nerve sidered to be quite important in discussing the mor- (Yoshizaki, 1961; Caliot et al. 1984; Ookubo et al. phological significance of the dual innervation of SM, 1987). According to phylogenetical and ontogenetical which is still argued by many anatomists as to the studies of the accessory nerve and the musculature, relationship between SM and the cervical muscles, Straus et al. (1936) considered that the sensory ele- especially infrahyoid muscles. ment, included in the accessory nerve in lower ver- tebrates and embryos of mammals, migrated at later stages to the dorsal roots of adjacent cervical nerves,

361 362 M. Koizuini et al.

Findings branch from the cervical plexus. This cervical branch was composed of the second (C2) and third (C3) After appearing from the jugular foramen, the cervical nerves. Then XI passed underneath the SM external branch of the accessory nerve (XI) crossed and supplied the trapezius muscle at its deep surface superficially to the internal jugular vein from ventral communicating with a branch from C3 and the fourth to dorsal direction and branched off to the deep (C4) cervical nerve. In addition to these nerves, surface of SM at approximately the junction of the a fine nerve (*) supplied the anterior region of the upper and middle thirds of SM (Fig. 1). Before middle third of SM at the deep surface. This anom- entering SM, this branch from XI joined with a alous nerve branch arose from the ventral surface

Fig. 1. Representation of the right lateral neck deep to platysma. The origin of the sterno- cleidomastoid muscle (SM) is cut and reflected cranially through the space between internal and external jugular veins. In addition to the normal nerve supply from a branch of accessory nerve and cervical plexus (Rsm), a part of SM is innervated by a branch of hypoglossal nerve (solid line). This anomalous nerve branch derives from the origin of superior root of the ansa cervicalis and supplies SM at its deep surface (*).

Abbreviations for figures Am: great auricular nerve, C: clavicular origin of sternocleidomastoid muscle, C1-C4: ventral division of the first-fourth cervical nerves, LH: infrahyoid muscles, Je: external jugular vein, Ji: internal jugular vein. LC: , M: mastoid insertion of sternocleidomastoid muscle, 0: occipital insertion of sternocleidomastoid muscle, OH!: inferior belly of . OHS: superior belly of omohyoid muscle, Omi: , PL: platysma, Rs: superior root of ansa cervicalis. Rsm: nerve branch to sternocleidomastoid muscle, Rsm-C: nerve branch to sternocleidomastoid muscle from cervical plexus, Rsm-XI: nerve branch to sternocleidomastoid muscle from accessory nerve, S: sternal origin of sternocleidomastoid muscle, SH: , SHS: superior portion of sternohyoid muscle, SM: sternocleidomastoid muscle, ST: , TH: , TR: trapezius muscle, Ts: sympathetic trunk. VII: facial nerve. X: vagus nerve, IX: glossopharyngeal nerve, XI: accessory nerve, XII: hypoglossal nerve. Sternocleidomastoid muscle innervated by the hypoglossal nerve 363 of the hypoglossal nerve (XII) at the origin of the XII and the cervical nerves from Cl + 2 (rectangular superior root of the ansa cervicalis. There were inset in Fig. 2). The nerve branch to the superior three inferior roots of the ansa cervicalis, two were belly of the omohyoid muscle (OHS) and the superior from C2 and the other from C3 + C4. All ran deep to part of the sternohyoid muscle (SHS) was derived the internal jugular vein to form the ansa cervicalis from the superior root (Rs) of the ansa cervicalis, with the superior root from XII. SM itself appeared which also contained the nerve fibers from XII, Cl quite normal. and C2. Other infrahyoid muscles were innervated Then XI and XII were released from the jugular by the branches of the ansa cervicalis. foramen and the hypoglossal canal, respectively, The XI and Rsm-C joined with each other and and the roots of the cervical plexus from Cl to C4 then spread out in many fine branches just before were cut off. Finally, SM with the relevant structures entering SM (Fig. 3). The fact that the nerve fibers was removed for the minute study of nerve fibers from XI (Rsm-XI) and Rsm-C were mixed together under a stereomicroscope. The results were as quite intimately suggested that each muscular branch follows. to SM contained both fibers from XI and the cervical The nerve fiber analysis showed that the cervical nerves (Fig. 4). The branch indicated by • in Fig. 3 nerve branch to SM (Rsm-C) carried the fibers carried only the accessory nerve fibers, but it com- from C2 and C3 (Fig. 2). The branch (*) from XII municated with the other branches in SM. According originated from the complex part at which the vagus to Yoshizaki (1961), SM consisted of four parts, that nerve, XII and Cl + 2 were joining and supplied is, the sternomastoid (S-M), sternooccipital (SAD), SM without communicating with any other muscular cleidomastoid (C-M) and cleidooccipital (C-0) branches. More detailed examination revealed that portions. Most muscular branches supplying SM this hypoglossal branch consisted of the fibers from entered the deep surface of the cleidomasoid portion

Fig. 2. The nerve fiber analysis of the superior root of ansa cervicalis (lateral view). The more detailed examination of the shaded area is shown in the rectangular inset. The origin of the anomalous nerve branch (solid line) is bifurcated. One is from the hypoglossal nerve and the other from the branch including the first (Cl) and second (C2) cervical nerver fibers. The nerve to the superior belly of omohyoid muscle and superior part of sternohyoid muscle is branched from the superior root of ansa cervicalis (Rs), which includes fibers from Cl, C2 and hypoglossal nerve (XII). Other infrahyoid muscles are supplied by the branches from the ansa cervicalis. 364 M. Koizumi et al.

Fig. 3. Thc branching pattern of Rsm and intramuscular nerve distribution of SM in our case (dorsal view). SM is composed of four parts, sterno(S)-mastoid(M), sterno-occipital(0), cleido(C)-mastoid and cleido-occipital portions. C-M portion is deepest. All branches to S-M and S-0 portions penetrate C-M portion. The portion of nerves indicated by double line and solid line arc situated out and in the muscle respectively. And the hatched nerves run under or in the C-M portion. The branches indicated by • and • supply the C-M portion. Thc anomalous nerve branch from XII (*) supplies only small middle part of S-M portion and communicates with the branch which supplies the main part of S-M portion (*). Detailed fiber analysis of the communication between the branch from the accessory nerve (Rsm-XI) and muscular branch from the cervical plexus (Rsm-C) is shown in Fig. 4 The branches indicated by a, b and A to I arc coincidental with thc branches shown by thc same letters in Fig. 4. Sternocleidomastoid muscle innervated by the hypoglossal nerve 365

Fig. 4. The precise fiber analysis of the nerve branches indicated by a, b, A-1 in Fig. 3. Rsm from XI (Rsm-XI) and Rsm-C communicate with each other quite closely and all branches indicated by a, b and A-I most likely include cervical nerve fibers in addition to the accessory nerve fibers. which was the deepest part of SM and the cleido- the ansa cervicalis). Therefore, the case of Pye- occipital portion, while the branch from XII entered Smith et al. is considered to be equivalent to our case the sternomastoid portion. in which the hypoglossal branch to SM derived from The study of the intramuscular distribution of the origin of the superior root of the ansa cervicalis. nerves revealed that the branch from XII supplied Eisler (1912) stated that the occurrence of the only a small part of the sternomastoid portion and motor supply of the hypoglossal nerve to SM was the remaining part was innervated by the branches closely related to the appearance of the anomalous of XI with cervical nerves. The communication (* in muscle called the superior sternoclavicular muscle Fig. 3) between the branch from XII (4) and the one (Hyrtl) on the surface of clavicula, which was also from XI with Rsm-C (b in Fig. 3) was found. innervated by the descending branch of the hypo- glossal nerve. According to his description, this superior sternoclavicular muscle (Ss) was defined as Discussion the muscle which arose from the upper margin of the , ran deep to the origin of SM on the In the study of SM, Maubrac (1884) and Pye- surface of the clavicula and ended by attaching to Smith et al. (1870/71) described the additional nerve the clavicula. Then, together with Ss , the sternofacial supply of the hypoglossal nerve. According to Eisler muscle, the singular supraclavicular muscle (Gruber) (1912) and Testut (1911), Breglia (1890) also reported and the cleidohyoid muscle were grouped as the the cases with the branch from the hypoglossal Ss and its equivalent muscles based on the equal nerve additionally supplying SM. Among these innervation from the descending branch of the hypo- three reports, only Pye-Smith et al. described that glossal nerve (superior root of the ansa cervicalis). the nerve concerned in the case was the descending Recent reports (Koda et al. 1985. Kida et al. 1985) branch from the hypoglossal nerve (superior root of also described precisely the innervation of Ss by a 366 M. Koizumi et al.

twig of the muscular branch to the superior belly of aberrant which extended between omohyoid muscle from the ansa cervicalis, like the the deep surface of the mastoid origin of SM and cases observed by Eisler. In our case, the muscular the intermediate of the omohyoid muscle branch in question (* in Fig. 2) arose from the hy- beneath SM. The superior belly was supplied by XI poglossal nerve just proximal to the origin of the and the inferior belly was innervated by a branch superior root of the ansa cervicalis and was composed arising from the ansa cervicalis just proximal to the of the fibers from the hypoglossal nerve and cervical origin of the branch to the superior belly of the nerves (Cl + C2). Consequently, the hypoglossal omohyoid muscle. Yamasaki concluded in his paper branch to SM in our case was considered to be that this aberrant digastric muscle occurred as the equivalent to the branches reported by Eisler, result of the fusion of two different muscular com- Koda and Kida. ponents; one from the cleidomastoid portion of Concerning the derivation of Ss, Eisler proposed SM and the other from the superior belly of the a cervical muscular mass which was supplied by Cl omohyoid muscle. We recognize that this finding through the superior root of the ansa cervicalis. also shows the possibility of exchange of muscular He discussed that when this cervical muscular mass components between SM and the infrahyoid muscles. occurred independently, it appeared to be Ss and Thereafter, we concluded that our notable case when the muscular mass fused to the deep surface in this paper occurred as the result of the fusion of of SM, it happened to be the case in which a part of a muscular slip deriving from the infrahyoid muscles SM was innervated by a branch from the descending to the deep surface of SM. When this kind of branch of XII (superior root of ansa cervicalis). muscular slip happens independently, it appears to Furthermore, he believed that this cervical muscular be Ss or the inferior belly of the anomalous muscle mass belonged to the more dorsal muscle group observed by Yamasaki (1983). In our case, the fact other than the infrahyoid muscle group, but there is that the intramuscular distribution of the branch no obvious evidence. Jinguji et al. (1983) described from XII was restricted to the small part near the in their report about the singular supraclavicular anterior margin of the middle of SM, which was muscle that the anomalous muscle supplied by a situated just over the infrahyoid muscles, supports branch of cervical plexus was wrapped in a superficial this conclusion. layer of the cervical together with SM and was not likely the split of infrahyoid muscles but the muscular slip which was fused to SM in normal References appearance. They did not mention the origin of this 1) Breglia.:Osservazioni e considerazioni sullo sterno-cleido- muscular slip. However, according to their findings mastoideodell'uomo. Riforma medica, 1890 (cited from that the nerve supply to this muscle was from the Eisler,1912). ansa cervicalis and that the branch ran superficial to 2) Caliot, P., Cabanie,P., Bousquet,V. and Midy,D.: A the omohyoid muscle, it is reasonable to suppose contributionto the studyof the innervationof the sterno- cleidomastoidmuscle. Anat. Clin. 6: 21-28, 1984. that this anomalous muscle belongs to the same 3) Eisler,P.: DieMuskeln des Stammes. In Bardeleben K, ed. group as the infrahyoid muscles. In other words, Handbuchder Anatomiedes Menschen.Bd.II, Abt.II, during development a part of the infrahyoid muscle TellI Jena,Gustav Fischer 239-240, 248-252, 1912. 4) Jinguji,Y. andTakisawa, A.: A rare caseof m.supraclavi- group is thought to separate and descend along the cularissingularis (Gruber) in a Japanesecadaver. Acta. deep surface of SM to the clavicula. Anat.Nippon 58: 630-633,1983. (in Japanese with English Further, Eisler reported one interesting case in summary) which the nerve supplying Ss was coming through 5) Kida,M., Yamada,T. K. and Kumaki,K.: On the inner- SM. He described that unfortunately the origin of vationof M.sternoclavicularissuperior (HYRTL). Acta. this nerve was damaged and was not confirmed. Anat.Nippon 60: 671,1985. (in Japanese) 6) Koda,M., Fukushima,0., Hayakawa,T., Kosugi,K. and However, judging from the fact that this nerve to Ss Yamashita,H.: A case of 'M.supraclavicularis singularis sent some branches in SM, it is likely that the origin (Gruber).Acta. Anat. Nippon 60: 672,1985. (in Japanese) of this nerve was XI including the cervical nerve 7) Kudo, H. and Kida, M. : A case of double innervated fibers. This case suggested the intimate relationship M.sternoclavicularissuperior (Hyrt1). Acta. Anat. Nippon between SM and Ss. Recently a special case in which 67: 511,1992. (in Japanese) 8) Kumaki,K.: Thecervical and the spinalaccessory nerves. — Ss was innervated dually by a twig of the muscular An accountby meansof fibreanalysis. Acta. Anat. Nippon branch to SM and the superior root of the ansa 45: 311-344,1970 (in Japanesewith English summary) cervicalis was observed by Kudo et al. (1992). We 9) Maubrac,0.: Recherchesanatomiques et physiologiques consider that this special case, together with the surle musclesterno-cleido-mstoidien. Internat. Monatsschr. f Anat. u 1: 94-119, 1884. above mentioned case of Eisler, suggests the mi- 10) McKenzie,J.: The morphologyof the sternomastoid and gration of a part of the muscular component of SM trapeziusmuscles. J. Anat.61: 526-531,1955. to Ss. Moreover, Yamasaki (1983) reported the 11) Ookubo,M., Iimura, A., Nakamura,Y., Ichikawa,S. and Sternocleidornastoid muscle innervated by the hypoglossal nerve 367

Uchino, S.: A rare case of direct nerve supply from the nerves in the occipital region of the human embryo. Amer. cervical plexus to the sternocleidomastoid muscle. J. Tokyo. J. Anat. 4: 83-116, 1905. Med. College 45: 837-839. (in Japanese) 15) Testut, L.: Traitd d'anatomie humaine. 6th ed. Paris, Octave 12) Pye-Smith, P. H., Howse, H. G. and Davies-Colley, Doin ct Fils 765-766, 1911. J. N. C.: Notes of abnormalities observed in the dissecting 16) Yamasaki, M. and Takahashi, H.: Unknown digastric muscle room during the winter sessions of 1868-9 and 1869-70. on the lateral neck region. Acta. Anat. Nippon 58: 526— Guy's Hosp. Reports 16: 147-163, 1870-71. 532, 1983. (in Japanese with English summary) 13) Straus, W. L. Jr. and Howell, A. B.: The spinal accessory 17) Yoshizaki, F.: Innervation of the sternocleidomastoid nerve and its musculature. Quart. Rev. Biol. 11: 387-407, muscle of man and the rabbit. Okayama Igakkai Zasshi 73: 1936. 159-171, 1961. (in Japanese with English summary) 14) Streeter, G. L.: The development of the cranial and spinal