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Derivation of the anterior belly of the digastric muscle receiving twigs from the mylohyoid and facial nerves
ANNALS OF ANATOMY
Derivation of the anterior belly of the digastric muscle receiving twigs from the mylohyoid and facial nerves Katsushi Kawai, Masahiro Koizumi, Satoru Honma, Akinari Tokiyoshi, and Kodo Kodama Department of Anatomy, Kumamoto University School of Medicine, 2-2-1 Honjo, Kumamoto, 860-0811, Japan
Summary. The anterior belly of the digastric muscle is usually supplied by the mylohyoid nerve, and in general anatomy textbooks, the anterior belly is invariably described as receiving no other nerve except the mylohyoid nerve. In fact, however, it is sometimes supplied by a branch of the facial nerve in addition to the mylohyoid nerve. Such cases were found in 8 bodies or 9 head sides among 539 bodies or 1078 head sides of Japanese subjects. Those nine cases were investigated in detail and it was clarified that they had the following three characteristics in common: (1) the twig originating from the facial nerve appears as the twig of the stylohyoid branch in most cases, ( 2 ) t h e twig from the facial nerve enters the anterior belly on its lower (shallow) surface and the twig of the mylohyoid nerve on its upper (deep) surface, (3) the twig of the mylohyoid nerve is distributed to the deep region and the twig of the stylohyoid branch is distributed to the shallow region of the anterior belly. F r o m these results, it was concluded that the anterior belly, receiving the twigs of the mylohyoid and facial nerves, had been formed by secondarily combining the most ventral and rostral part of the primordium of the stylohyoid muscle in the second branchial arch with the caudal part of the prim o r d i u m of the anterior belly in the first branchial arch. Key words: Anterior belly - Digastric muscle - Mylohyoid nerve - Facial nerve - Derivation - D o u b l e innervation - Branchial arch
Correspondence to: K. Kawai
Ann Anat (2003) 185:85-90 @ Urban & Fischer Verlag
http://www.urbanfischer.de/journals/annanat
Abbreviations in Figures 1-7: AD = anterior belly of the digastric muscle * (asterisk) twig of the stylohyoid branch CC = common carotid artery IJ = internal jugular vein Mh = mylohyoid muscle mh = mylohyoid nerve Oh = omohyoid muscle PD = posterior belly of the digastric muscle Sh = sternohyoid muscle Smg = submandibular gland St = stylohyoid muscle st = stylohyoid branch of the facial nerve I = first branchial arch II = second branchial arch III = third branchial arch V = trigeminal nerve VII = facial nerve IX = glossopharyngeal nerve
Introduction The anterior belly of the digastric muscle is well known as a muscle that often shows supernumerary muscular bundles, and it is usually supplied by the mylohyoid nerve that diverges from the mandibular division of the trigeminal nerve. In general anatomy textbooks (Warwick et al. 1989; Sinclair 1981; Hollinshead 1974; Woodburne et al. 1988), there is no mention that the anterior belly of the digastric receives any another nerve except the mylohyoid nerve. Eisler (1912), who investigated the muscular system of the h u m a n body in detail and systematically, also stated that the anterior belly of the digastric received the mylohyoid nerve diverging from the third branch of the trigeminal nerve, and said nothing of a facial nerve. In
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Fig. 1. Cross-vision stereophotograph of a case (No. 9 in Table 1) of the anterior belly having the double innervation. The twig (asterisk) of the stylohyoid branch entered the anterior belly (AD) on its lower surface and the twigs of the mylohyoid nerve (mh) on its upper surface. Left side of the face, deep layer. Mandible has been removed. fact, however, as this report shows, it is sometimes supplied by a branch of the facial nerve in addition to the mylohyoid nerve (Fig. 1). In such cases, the boundary and relationship between the regions originating from the first and second branchial arches were investigated in detail. On the basis of the findings from this investigation, we speculated on the derivation of the anterior belly of the digastric having the double innervation and the relative positions of the primordia of the digastric and other muscles around it in the respective branchial arch.
Results In nine cases of the anterior belly having double innervation, the nerve supply and intramuscular distribution of the twigs from the mylohyoid nerve and the stylohyoid branch of the facial nerve are shown in Table 1. In all cases, the anterior belly of the digastric typically received the twig of the mylohyoid nerve on its upper (deep) surface. Simultaneously, in eight cases (Nos. 1, 2, 3, 4, 5, 6, 8, 9), the twig issuing from the stylohyoid branch of the facial nerve descended along the lateral margin of the stylohyoid muscle and entered the anterior belly of the digastric on its lower (shallow) surface across its intermediate tendon as shown in Figure 2. On the other hand, in only one case, No. 7, the twig issuing from the marginal mandibular branch of the facial nerve entered the lateral part of the anterior belly on its lower (shallow) surface. The intramuscular distribution of the twigs of the mylohyoid and facial nerves was observed in detail under a stereomicroscope and i m m e r s e d in water in four cases (Nos. 3, 4, 8, 9). In No. 3, the twig of the mylohyoid nerve was distributed to the deep (upper) region of the anterior belly widely and the twig of the stylohyoid branch of the facial nerve was distributed to the shallow (lower) and central region of the anterior belly (Fig. 3). In No. 4, the twig of the mylohyoid nerve was distributed to the deep (upper) region widely (Fig. 4 b), the twig of
Materials and methods Altogether 539 bodies, or 1078 head sides of Japanese subjects, bequeathed for student dissection over an 18 year period, were examined at Kanazawa University School of Medicine and Kumamoto University School of Medicine. The anterior belly of the digastric supplied by the mylohyoid and facial nerves were found in 8 bodies or 9 head sides (0.83%). Those nine cases were observed macroscopically and sketched carefully. Stereophotographs were also made of some of them. In four cases in good condition, the anterior and posterior bellies of the digastric, the mylohyoid and the stylohyoid muscles were removed together with the relevant nerves for subsequent teasing examination under a stereomicroscope and immersed in water. The intramuscular distribution of the twigs from the mylohyoid and facial nerves in the anterior belly of the digastric were then investigated. 86
from medial to lateral margin (Fig. 5a). In No. 9, the twig of the mylohyoid nerve was distributed to the deep medial region (Fig. 6 b) and the twig of the stylohyoid branch was distributed to the region from central to near lateral margin in the shallow layer of the anterior belly (Fig. 6 a). In these four cases, it was c o m m o n that these two twigs communicated with each other at a few perTable 1. Nerve supply of the anterior belly and its intramuscular ipheral parts. In two cases (Nos. 2, 5), it was confirmed distribution macroscopically that the twig of the mylohyoid nerve communicated with the twig of the stylohyoid branch in Intramuscular distribution Case Side Nerve Surface No. supply which nerve the anterior belly. The anterior belly was not separated Region Communication enters on into two parts as distinct muscular bundles in these six cases. But in No. 6, the anterior belly was divided clearly 1 R mh upper unclear unclear into the lateral shallow and medial deep parts, and the st lower former received the twig from the stylohyoid branch of 2 L mh upper unclear + the facial nerve while the latter the twig of the mylost lower hyoid nerve. There was no communication between these 3 R mh upper deep (widely) + two twigs in this case. In the remaining two cases st lower shallow, (Nos. 1, 7), it was not possible to investigate the intracentral muscular distribution of these twigs because of the cir4 R mh upper deep (widely) + cumstances of the student dissection. st lower shallow, lateral By putting the findings of these nine cases in order, it 5 R mh upper unclear + was clarified that they invariably had the following three st lower c o m m o n characteristics: ( 1 ) t h e twig originating from the 6 R mh upper medial facial nerve appears as the twig of the stylohyoid branch st lower lateral in all cases except one case supplied by the twig of the 7 R mh upper unclear unclear marginal mandibular branch; (2) the twig originating from mm lower lateral the facial nerve, whether it issues from the stylohyoid or 8 R mh upper deep, medial + marginal mandibular branch, always enters the anterior st lower shallow belly on its lower (shallow) surface and the twig of the (widely) mylohyoid nerve on its upper (deep) surface; (3) the twig 9 L mh upper deep, medial + of the mylohyoid nerve, a branch of the trigeminal nerve st lower shallow, cenderived from the first branchial arch is distributed to the tral, lateral deep region and the twig of the stylohyoid branch, a branch of the facial nerve derived from the second branR = right side, L = left side, mh = twig of the mylohyoid nerve, st = twig of the stylohyoid branch, mm = twig of the marginal chial arch is distributed to the shallow region of the anterior belly. mandibular branch
the stylohyoid branch was distributed to the shallow (lower) and lateral region (Fig. 4 a). In No. 8, the twig of the mylohyoid nerve was distributed to the deep region near the medial margin (Fig. 5 b) and the twig of the stylohyoid branch was spread widely in the shallow layer
Fig. 2. Case No. 3. The twig (asterisk) issuing from the stylohyoid branch (st) of the facial nerve (VII) descended along the stylohyoid muscle and entered the anterior belly (AD) on its lower surface across its intermediate tendon. The anterior belly also received the twig of the mylohyoid nerve (mh) on its upper surface as usual.
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Fig. 3. Case No. 3. Illustration of the intramuscular distribution of the twigs of the mylohyoid and facial nerves. The anterior belly (AD) is reflected laterally. The twig of the mylohyoid nerve (mh) was distributed to the deep (upper) region widely and the twig of the stylohyoid branch (asterisk) was distributed to the shallow (lower) and central region of the anterior belly. There were a few communications (white circles) between the two twigs. form premuscle mass receiving the branches of the facial nerve. During its later development, the branch of the facial nerve to the anterior part of the mass, which would b e c o m e the anterior belly, was intercepted by the newly formed intermediate tendon while the anterior part secondarily received the branch of the mylohyoid nerve instead of the facial nerve. In other words, the change of nerve supply to the anterior belly occurs during the development and in the end the anterior and posterior bellies of the digastric muscle are supplied by different nerves. Before the new detailed reports on the development of the digastric muscle were presented, on the basis of Futamura' s report, it was explained that the anterior belly receiving two twigs from the mylohyoid and facial nerves was an instance which maintained the twig from the facial nerve which usually disappeared by the formation of the
Discussion The anterior belly of the digastric muscle sometimes receives a twig originating from the facial nerve in addition to the mylohyoid nerve. Such cases have been reported by Yoshizaki (1961), Mizukami (1973) and Shigemasa et al. (1982) in Japan. In all cases reported by them, the twig issuing from the stylohyoid branch of the facial nerve descended along the stylohyoid muscle and entered the anterior belly on its lower surface across its intermediate tendon. The findings of these previous reports are much the same as those in this paper. A l t h o u g h the anterior belly of the digastric muscle innervated by the mylohyoid and facial nerves is very rare as shown by low frequency (0.83%), it shows c o m m o n characteristics as mentioned above. We recognized some invariable rules in those characteristics and attempted to consider what their morphological significance could mean. As regards the development of the digastric muscle, F u t a m u r a (1906) described it as follows. In the h u m a n embryo, the digastric muscle appeared at first as a uni-
m'h--%,~ ~ \\~..-~-._
"~.~"'~ ~---:-. /
a) mh
b) Fig. 5. Case No. 8. a: Lower (shallow) surface of the anterior belly (AD). The twig of the stylohyoid branch (asterisk) spread widely in the shallow layer from medial to lateral margin, b: Upper (deep) surface. The twig of the mylohyoid nerve (mh) was distributed to the deep region near the medial margin. Some communications (white circles) were found between these two twigs.
Fig. 4. Case No. 4. a: Lower (shallow) surface of the anterior belly. The twig of the stylohyoid branch (asterisk) was distributed to the shallow and lateral region, b: Upper (deep) surface. The twig of the mylohyoid nerve (mh) was distributed to the deep region of the anterior belly widely. These two twigs communicated with each other at some peripheral points (white circles).
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intermediate tendon during the development. Gasser (1967) showed the double derivation of the digastric muscle in that its posterior belly was derived from the second branchial arch, and that its anterior belly developed caudal to the mylohyoid muscle in the ventral region of the first branchial arch. He also described that the primordium of the stylohyoid muscle was situated rostral to the primordium of the posterior belly and near the original primordium of the anterior belly. According to Ballard
~ m h
b)~ ~ 2 ~ Fig. 6. Case No. 9. a: Lower (shallow) surface of the anterior belly (AD). The twig (asterisk) of the stylohyoid branch (st) was distributed to the region from central to near lateral margin in the shallow layer, b: Upper (deep) surface. The twig of the mylohyoid nerve (mh) was distributed to the deep medial region. It communicated with the twig of the stylohyoid branch at a few peripheral parts (white circles).
5
~
D
Fig. 7. Scheme to show the relative position and the movement of the primordium of each muscle in the branchial arches. The primordia of the mylohyoid muscle (Mh) and the anterior belly (AD) are situated in the most ventral region of the first branchial arch (I) and arranged in rostro-caudal direction, holding the mylohyoid nerve (mh) between them. In the second branchial arch (II), the primordium of the stylohyoid muscle (St) is situated relatively ventral and rostral to that of the posterior belly (PD). The anterior belly receiving the twigs of the mylohyoid and facial nerves is formed secondarily combining the most ventral and rostral part of the primordium of the stylohyoid muscle with the caudal part of the primordium of the anterior belly.
(1964), the primordia of the mylohyoid and the anterior belly are situated at the ventral region in the first branchial arch. At the present time, the theory that the anterior and posterior bellies of the digastric muscle have different derivations is generally accepted. With regard to the derivation of the muscle, a theory was presented by Fiirbringer at the end of 19th century and supported by Nishi (1938) in Japan, called the theory of nerve-muscle specificity. That theory explains that the relationship between the muscle and its nerve supply is maintained through out the entire phylogenetic process, and which nerve supplies the muscle is an important clue to decide the derivation of the muscle and the homology between it and other muscles. In other words, the derivation of the muscle is shown by its nerve supply. When the three common characteristics mentioned in the result section were examined, being based on these two theories, it was possible and logical to conjecture that the anterior belly receiving the twigs from the mylohyoid and the facial nerves was formed by combining the premuscle mass of the first branchial arch with that of the second branchial arch. In addition, the first characteristic meant that the premuscle mass participating in the formation of the anterior belly had been derived from the primordium of the stylohyoid muscle in the second branchial arch. The second and third characteristics show that the part derived from the primordium of the stylohyoid muscle is combined with the primordium of the anterior belly from its caudal and somewhat dorsal position. These characteristics apply to the fact that the primordium of the anterior belly separates caudally from that of the mylohyoid muscle in the first branchial arch and the second branchial arch is situated caudal to the first branchial arch, and the findings reported by Gasser (1967) and Ballard (1964). As a result, it is supposed that the primordium of each muscle is situated in the first and second branchial arches and moves as shown in Figure 7. The primordia of the mylohyoid muscle and the anterior belly are situated in the most ventral region of the first branchial arch and arranged in a rost-caudal direction, holding the mylohyoid nerve between them. In the second branchial arch, the primordium of the stylohyoid muscle is situated relatively ventral and rostral to that of the posterior belly. The anterior belly in question, receiving the twigs of the mylohyoid and facial nerves, is formed by combining secondarily the most ventral and rostral part of the primordium of the stylohyoid muscle in the second branchial arch with the caudal part of the primordium of the anterior belly in the first branchial arch. It seems that the extent of the area to which the twig of the stylohyoid branch is distributed reflects the size of the premuscle mass which was separated from the primordium of the stylohyoid muscle and combined secondarily with that of the anterior belly. The fact that these two twigs communicate with each other at a peripheral point seems to suggest that the combination of these two premuscle masses derived from the first and second branchial arches occurred at an early point in its development.
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The p h e n o m e n o n that one muscle at first glance is formed by the combination of plural primordia having different derivations in fact is not limited to the head and cervical regions of the h u m a n body. K o d a m a (1986) reported similar p h e n o m e n a in the muscles of trunk such as the supracostal muscle. K o d a m a described that the form of muscle was determined by the place where it existed rather than its derivation, and called it the local factor to the muscle morphogenesis. The anterior belly having two derivations in this paper is the same as the usual anterior belly derived from one derivation in appearance. In this case, it is thought that the local factor to the muscle morphogenesis reflects the formation of the anterior belly of the digastric muscle.
References Ballard WW (1964) Comparative Anatomy and Embryology. Ronald Press Company, New York EislerP (1912) Die Muskeln des Stammes. In: BardelebenK (Ed) Handbuch der Anatomie des Menschen, vol 2, Teil 2. Fischer, Jena, pp 274-284 Futamura R (1906) Uber die Entwickelung der Facialismuskulatur des Menschen. Anat Hefte 30:435-516 Gasser RF (1967) The Development of the Facial Muscles in Man. Am J Anat 120:357-376
Hollinshead WH (1974) Textbook of Anatomy, 3rd ed. Harper Row Publishers, Hagerstown, p 769 Kodama K (1986) Morphological Significance of the Supracostal Muscles, and the Superficial Intercostal Nerve - A New Definition. Kaibogaku Zasshi 61:107-129 (in Japanese) Mizukami S (1973) Innervation of the anterior belly of the digastric muscle. Kaibogaku Zasshi 48:24 (in Japanese) Nishi S (1938) Muskelsystem, Muskel und Nerv. In: Bolk L e t al. (Eds) Handbuch der vergleichenden Anatomie der Wirbeltiere, Bd5. Urban & Schwarzenberg, Berlin und Wien, pp 344-346 Shigemasa K, Kobayashi M, Nomoto A, Koyano T, Kinoshita T, Kitagawa T, Tezuka M, Takemoto R (1982) Double Innervation of the Anterior Belly of the Digastric Muscle. Nihon Univ Dent J 56:636-641 (in Japanese) Sinclair DC (1981) Muscles and fasciae. In: Romanes GJ (Ed) Cunningham's Textbook of Anatomy, 12th ed. Oxford University Press, Oxford, pp 284, 756-757 Warwick R, Williams PL, Dyson M, Bannister LH (1989) Gray's Anatomy, 37th ed. Churchill Livingstone, Edinburgh, pp 11071113 Woodburne RT, Burkel WE (1988) Essentials of Human Anatomy, 8th ed. Oxford University Press, New York, p 205 Yoshizaki F (1961) A case of double innervation of the anterior belly of the digastric muscle by the mylohyoid and facial nerves. Journal of Okayama Medical Association 73:173-175 (in Japanese)
Accepted July 8, 2002
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Derivation of the anterior belly of the digastric muscle receiving twigs from the mylohyoid and facial nerves Katsushi Kawai, Masahiro Koizumi, Satoru Honma, Akinari Tokiyoshi, and Kodo Kodama Department of Anatomy, Kumamoto University School of Medicine, 2-2-1 Honjo, Kumamoto, 860-0811, Japan
Summary. The anterior belly of the digastric muscle is usually supplied by the mylohyoid nerve, and in general anatomy textbooks, the anterior belly is invariably described as receiving no other nerve except the mylohyoid nerve. In fact, however, it is sometimes supplied by a branch of the facial nerve in addition to the mylohyoid nerve. Such cases were found in 8 bodies or 9 head sides among 539 bodies or 1078 head sides of Japanese subjects. Those nine cases were investigated in detail and it was clarified that they had the following three characteristics in common: (1) the twig originating from the facial nerve appears as the twig of the stylohyoid branch in most cases, ( 2 ) t h e twig from the facial nerve enters the anterior belly on its lower (shallow) surface and the twig of the mylohyoid nerve on its upper (deep) surface, (3) the twig of the mylohyoid nerve is distributed to the deep region and the twig of the stylohyoid branch is distributed to the shallow region of the anterior belly. F r o m these results, it was concluded that the anterior belly, receiving the twigs of the mylohyoid and facial nerves, had been formed by secondarily combining the most ventral and rostral part of the primordium of the stylohyoid muscle in the second branchial arch with the caudal part of the prim o r d i u m of the anterior belly in the first branchial arch. Key words: Anterior belly - Digastric muscle - Mylohyoid nerve - Facial nerve - Derivation - D o u b l e innervation - Branchial arch
Correspondence to: K. Kawai
Ann Anat (2003) 185:85-90 @ Urban & Fischer Verlag
http://www.urbanfischer.de/journals/annanat
Abbreviations in Figures 1-7: AD = anterior belly of the digastric muscle * (asterisk) twig of the stylohyoid branch CC = common carotid artery IJ = internal jugular vein Mh = mylohyoid muscle mh = mylohyoid nerve Oh = omohyoid muscle PD = posterior belly of the digastric muscle Sh = sternohyoid muscle Smg = submandibular gland St = stylohyoid muscle st = stylohyoid branch of the facial nerve I = first branchial arch II = second branchial arch III = third branchial arch V = trigeminal nerve VII = facial nerve IX = glossopharyngeal nerve
Introduction The anterior belly of the digastric muscle is well known as a muscle that often shows supernumerary muscular bundles, and it is usually supplied by the mylohyoid nerve that diverges from the mandibular division of the trigeminal nerve. In general anatomy textbooks (Warwick et al. 1989; Sinclair 1981; Hollinshead 1974; Woodburne et al. 1988), there is no mention that the anterior belly of the digastric receives any another nerve except the mylohyoid nerve. Eisler (1912), who investigated the muscular system of the h u m a n body in detail and systematically, also stated that the anterior belly of the digastric received the mylohyoid nerve diverging from the third branch of the trigeminal nerve, and said nothing of a facial nerve. In
0940-9602/03/185/1-85 $15.00/0
Fig. 1. Cross-vision stereophotograph of a case (No. 9 in Table 1) of the anterior belly having the double innervation. The twig (asterisk) of the stylohyoid branch entered the anterior belly (AD) on its lower surface and the twigs of the mylohyoid nerve (mh) on its upper surface. Left side of the face, deep layer. Mandible has been removed. fact, however, as this report shows, it is sometimes supplied by a branch of the facial nerve in addition to the mylohyoid nerve (Fig. 1). In such cases, the boundary and relationship between the regions originating from the first and second branchial arches were investigated in detail. On the basis of the findings from this investigation, we speculated on the derivation of the anterior belly of the digastric having the double innervation and the relative positions of the primordia of the digastric and other muscles around it in the respective branchial arch.
Results In nine cases of the anterior belly having double innervation, the nerve supply and intramuscular distribution of the twigs from the mylohyoid nerve and the stylohyoid branch of the facial nerve are shown in Table 1. In all cases, the anterior belly of the digastric typically received the twig of the mylohyoid nerve on its upper (deep) surface. Simultaneously, in eight cases (Nos. 1, 2, 3, 4, 5, 6, 8, 9), the twig issuing from the stylohyoid branch of the facial nerve descended along the lateral margin of the stylohyoid muscle and entered the anterior belly of the digastric on its lower (shallow) surface across its intermediate tendon as shown in Figure 2. On the other hand, in only one case, No. 7, the twig issuing from the marginal mandibular branch of the facial nerve entered the lateral part of the anterior belly on its lower (shallow) surface. The intramuscular distribution of the twigs of the mylohyoid and facial nerves was observed in detail under a stereomicroscope and i m m e r s e d in water in four cases (Nos. 3, 4, 8, 9). In No. 3, the twig of the mylohyoid nerve was distributed to the deep (upper) region of the anterior belly widely and the twig of the stylohyoid branch of the facial nerve was distributed to the shallow (lower) and central region of the anterior belly (Fig. 3). In No. 4, the twig of the mylohyoid nerve was distributed to the deep (upper) region widely (Fig. 4 b), the twig of
Materials and methods Altogether 539 bodies, or 1078 head sides of Japanese subjects, bequeathed for student dissection over an 18 year period, were examined at Kanazawa University School of Medicine and Kumamoto University School of Medicine. The anterior belly of the digastric supplied by the mylohyoid and facial nerves were found in 8 bodies or 9 head sides (0.83%). Those nine cases were observed macroscopically and sketched carefully. Stereophotographs were also made of some of them. In four cases in good condition, the anterior and posterior bellies of the digastric, the mylohyoid and the stylohyoid muscles were removed together with the relevant nerves for subsequent teasing examination under a stereomicroscope and immersed in water. The intramuscular distribution of the twigs from the mylohyoid and facial nerves in the anterior belly of the digastric were then investigated. 86
from medial to lateral margin (Fig. 5a). In No. 9, the twig of the mylohyoid nerve was distributed to the deep medial region (Fig. 6 b) and the twig of the stylohyoid branch was distributed to the region from central to near lateral margin in the shallow layer of the anterior belly (Fig. 6 a). In these four cases, it was c o m m o n that these two twigs communicated with each other at a few perTable 1. Nerve supply of the anterior belly and its intramuscular ipheral parts. In two cases (Nos. 2, 5), it was confirmed distribution macroscopically that the twig of the mylohyoid nerve communicated with the twig of the stylohyoid branch in Intramuscular distribution Case Side Nerve Surface No. supply which nerve the anterior belly. The anterior belly was not separated Region Communication enters on into two parts as distinct muscular bundles in these six cases. But in No. 6, the anterior belly was divided clearly 1 R mh upper unclear unclear into the lateral shallow and medial deep parts, and the st lower former received the twig from the stylohyoid branch of 2 L mh upper unclear + the facial nerve while the latter the twig of the mylost lower hyoid nerve. There was no communication between these 3 R mh upper deep (widely) + two twigs in this case. In the remaining two cases st lower shallow, (Nos. 1, 7), it was not possible to investigate the intracentral muscular distribution of these twigs because of the cir4 R mh upper deep (widely) + cumstances of the student dissection. st lower shallow, lateral By putting the findings of these nine cases in order, it 5 R mh upper unclear + was clarified that they invariably had the following three st lower c o m m o n characteristics: ( 1 ) t h e twig originating from the 6 R mh upper medial facial nerve appears as the twig of the stylohyoid branch st lower lateral in all cases except one case supplied by the twig of the 7 R mh upper unclear unclear marginal mandibular branch; (2) the twig originating from mm lower lateral the facial nerve, whether it issues from the stylohyoid or 8 R mh upper deep, medial + marginal mandibular branch, always enters the anterior st lower shallow belly on its lower (shallow) surface and the twig of the (widely) mylohyoid nerve on its upper (deep) surface; (3) the twig 9 L mh upper deep, medial + of the mylohyoid nerve, a branch of the trigeminal nerve st lower shallow, cenderived from the first branchial arch is distributed to the tral, lateral deep region and the twig of the stylohyoid branch, a branch of the facial nerve derived from the second branR = right side, L = left side, mh = twig of the mylohyoid nerve, st = twig of the stylohyoid branch, mm = twig of the marginal chial arch is distributed to the shallow region of the anterior belly. mandibular branch
the stylohyoid branch was distributed to the shallow (lower) and lateral region (Fig. 4 a). In No. 8, the twig of the mylohyoid nerve was distributed to the deep region near the medial margin (Fig. 5 b) and the twig of the stylohyoid branch was spread widely in the shallow layer
Fig. 2. Case No. 3. The twig (asterisk) issuing from the stylohyoid branch (st) of the facial nerve (VII) descended along the stylohyoid muscle and entered the anterior belly (AD) on its lower surface across its intermediate tendon. The anterior belly also received the twig of the mylohyoid nerve (mh) on its upper surface as usual.
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Fig. 3. Case No. 3. Illustration of the intramuscular distribution of the twigs of the mylohyoid and facial nerves. The anterior belly (AD) is reflected laterally. The twig of the mylohyoid nerve (mh) was distributed to the deep (upper) region widely and the twig of the stylohyoid branch (asterisk) was distributed to the shallow (lower) and central region of the anterior belly. There were a few communications (white circles) between the two twigs. form premuscle mass receiving the branches of the facial nerve. During its later development, the branch of the facial nerve to the anterior part of the mass, which would b e c o m e the anterior belly, was intercepted by the newly formed intermediate tendon while the anterior part secondarily received the branch of the mylohyoid nerve instead of the facial nerve. In other words, the change of nerve supply to the anterior belly occurs during the development and in the end the anterior and posterior bellies of the digastric muscle are supplied by different nerves. Before the new detailed reports on the development of the digastric muscle were presented, on the basis of Futamura' s report, it was explained that the anterior belly receiving two twigs from the mylohyoid and facial nerves was an instance which maintained the twig from the facial nerve which usually disappeared by the formation of the
Discussion The anterior belly of the digastric muscle sometimes receives a twig originating from the facial nerve in addition to the mylohyoid nerve. Such cases have been reported by Yoshizaki (1961), Mizukami (1973) and Shigemasa et al. (1982) in Japan. In all cases reported by them, the twig issuing from the stylohyoid branch of the facial nerve descended along the stylohyoid muscle and entered the anterior belly on its lower surface across its intermediate tendon. The findings of these previous reports are much the same as those in this paper. A l t h o u g h the anterior belly of the digastric muscle innervated by the mylohyoid and facial nerves is very rare as shown by low frequency (0.83%), it shows c o m m o n characteristics as mentioned above. We recognized some invariable rules in those characteristics and attempted to consider what their morphological significance could mean. As regards the development of the digastric muscle, F u t a m u r a (1906) described it as follows. In the h u m a n embryo, the digastric muscle appeared at first as a uni-
m'h--%,~ ~ \\~..-~-._
"~.~"'~ ~---:-. /
a) mh
b) Fig. 5. Case No. 8. a: Lower (shallow) surface of the anterior belly (AD). The twig of the stylohyoid branch (asterisk) spread widely in the shallow layer from medial to lateral margin, b: Upper (deep) surface. The twig of the mylohyoid nerve (mh) was distributed to the deep region near the medial margin. Some communications (white circles) were found between these two twigs.
Fig. 4. Case No. 4. a: Lower (shallow) surface of the anterior belly. The twig of the stylohyoid branch (asterisk) was distributed to the shallow and lateral region, b: Upper (deep) surface. The twig of the mylohyoid nerve (mh) was distributed to the deep region of the anterior belly widely. These two twigs communicated with each other at some peripheral points (white circles).
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intermediate tendon during the development. Gasser (1967) showed the double derivation of the digastric muscle in that its posterior belly was derived from the second branchial arch, and that its anterior belly developed caudal to the mylohyoid muscle in the ventral region of the first branchial arch. He also described that the primordium of the stylohyoid muscle was situated rostral to the primordium of the posterior belly and near the original primordium of the anterior belly. According to Ballard
~ m h
b)~ ~ 2 ~ Fig. 6. Case No. 9. a: Lower (shallow) surface of the anterior belly (AD). The twig (asterisk) of the stylohyoid branch (st) was distributed to the region from central to near lateral margin in the shallow layer, b: Upper (deep) surface. The twig of the mylohyoid nerve (mh) was distributed to the deep medial region. It communicated with the twig of the stylohyoid branch at a few peripheral parts (white circles).
5
~
D
Fig. 7. Scheme to show the relative position and the movement of the primordium of each muscle in the branchial arches. The primordia of the mylohyoid muscle (Mh) and the anterior belly (AD) are situated in the most ventral region of the first branchial arch (I) and arranged in rostro-caudal direction, holding the mylohyoid nerve (mh) between them. In the second branchial arch (II), the primordium of the stylohyoid muscle (St) is situated relatively ventral and rostral to that of the posterior belly (PD). The anterior belly receiving the twigs of the mylohyoid and facial nerves is formed secondarily combining the most ventral and rostral part of the primordium of the stylohyoid muscle with the caudal part of the primordium of the anterior belly.
(1964), the primordia of the mylohyoid and the anterior belly are situated at the ventral region in the first branchial arch. At the present time, the theory that the anterior and posterior bellies of the digastric muscle have different derivations is generally accepted. With regard to the derivation of the muscle, a theory was presented by Fiirbringer at the end of 19th century and supported by Nishi (1938) in Japan, called the theory of nerve-muscle specificity. That theory explains that the relationship between the muscle and its nerve supply is maintained through out the entire phylogenetic process, and which nerve supplies the muscle is an important clue to decide the derivation of the muscle and the homology between it and other muscles. In other words, the derivation of the muscle is shown by its nerve supply. When the three common characteristics mentioned in the result section were examined, being based on these two theories, it was possible and logical to conjecture that the anterior belly receiving the twigs from the mylohyoid and the facial nerves was formed by combining the premuscle mass of the first branchial arch with that of the second branchial arch. In addition, the first characteristic meant that the premuscle mass participating in the formation of the anterior belly had been derived from the primordium of the stylohyoid muscle in the second branchial arch. The second and third characteristics show that the part derived from the primordium of the stylohyoid muscle is combined with the primordium of the anterior belly from its caudal and somewhat dorsal position. These characteristics apply to the fact that the primordium of the anterior belly separates caudally from that of the mylohyoid muscle in the first branchial arch and the second branchial arch is situated caudal to the first branchial arch, and the findings reported by Gasser (1967) and Ballard (1964). As a result, it is supposed that the primordium of each muscle is situated in the first and second branchial arches and moves as shown in Figure 7. The primordia of the mylohyoid muscle and the anterior belly are situated in the most ventral region of the first branchial arch and arranged in a rost-caudal direction, holding the mylohyoid nerve between them. In the second branchial arch, the primordium of the stylohyoid muscle is situated relatively ventral and rostral to that of the posterior belly. The anterior belly in question, receiving the twigs of the mylohyoid and facial nerves, is formed by combining secondarily the most ventral and rostral part of the primordium of the stylohyoid muscle in the second branchial arch with the caudal part of the primordium of the anterior belly in the first branchial arch. It seems that the extent of the area to which the twig of the stylohyoid branch is distributed reflects the size of the premuscle mass which was separated from the primordium of the stylohyoid muscle and combined secondarily with that of the anterior belly. The fact that these two twigs communicate with each other at a peripheral point seems to suggest that the combination of these two premuscle masses derived from the first and second branchial arches occurred at an early point in its development.
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The p h e n o m e n o n that one muscle at first glance is formed by the combination of plural primordia having different derivations in fact is not limited to the head and cervical regions of the h u m a n body. K o d a m a (1986) reported similar p h e n o m e n a in the muscles of trunk such as the supracostal muscle. K o d a m a described that the form of muscle was determined by the place where it existed rather than its derivation, and called it the local factor to the muscle morphogenesis. The anterior belly having two derivations in this paper is the same as the usual anterior belly derived from one derivation in appearance. In this case, it is thought that the local factor to the muscle morphogenesis reflects the formation of the anterior belly of the digastric muscle.
References Ballard WW (1964) Comparative Anatomy and Embryology. Ronald Press Company, New York EislerP (1912) Die Muskeln des Stammes. In: BardelebenK (Ed) Handbuch der Anatomie des Menschen, vol 2, Teil 2. Fischer, Jena, pp 274-284 Futamura R (1906) Uber die Entwickelung der Facialismuskulatur des Menschen. Anat Hefte 30:435-516 Gasser RF (1967) The Development of the Facial Muscles in Man. Am J Anat 120:357-376
Hollinshead WH (1974) Textbook of Anatomy, 3rd ed. Harper Row Publishers, Hagerstown, p 769 Kodama K (1986) Morphological Significance of the Supracostal Muscles, and the Superficial Intercostal Nerve - A New Definition. Kaibogaku Zasshi 61:107-129 (in Japanese) Mizukami S (1973) Innervation of the anterior belly of the digastric muscle. Kaibogaku Zasshi 48:24 (in Japanese) Nishi S (1938) Muskelsystem, Muskel und Nerv. In: Bolk L e t al. (Eds) Handbuch der vergleichenden Anatomie der Wirbeltiere, Bd5. Urban & Schwarzenberg, Berlin und Wien, pp 344-346 Shigemasa K, Kobayashi M, Nomoto A, Koyano T, Kinoshita T, Kitagawa T, Tezuka M, Takemoto R (1982) Double Innervation of the Anterior Belly of the Digastric Muscle. Nihon Univ Dent J 56:636-641 (in Japanese) Sinclair DC (1981) Muscles and fasciae. In: Romanes GJ (Ed) Cunningham's Textbook of Anatomy, 12th ed. Oxford University Press, Oxford, pp 284, 756-757 Warwick R, Williams PL, Dyson M, Bannister LH (1989) Gray's Anatomy, 37th ed. Churchill Livingstone, Edinburgh, pp 11071113 Woodburne RT, Burkel WE (1988) Essentials of Human Anatomy, 8th ed. Oxford University Press, New York, p 205 Yoshizaki F (1961) A case of double innervation of the anterior belly of the digastric muscle by the mylohyoid and facial nerves. Journal of Okayama Medical Association 73:173-175 (in Japanese)
Accepted July 8, 2002
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