Teres major and latissimus dorsi muscles in human embryos: A reconsideration of the so-called brother muscles

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1 Okajimas Folia Anat. Jpn., Fetal 94(3): teres 81 85, major November, muscle Teres major and latissimus dorsi muscles in human embryos: A reconsideration of the so-called brother muscles By Koichiro SAKANAKA 1, Masahito YAMAMOTO 1, Takanori ISHIBASHI 1, Nobuaki YANAGISAWA 2, Jose Francisco RODRÍGUEZ-VÁZQUEZ 3, Gen MURAKAMI 1, 4, Shin-ichi ABE 1 1 Department of Anatomy, Tokyo Dental College, , Misaki-cho, Chiyoda-ku, Tokyo , Japan 2 Division of oral health sciences, department of health sciences school of health and social services, Saitama prefectural university, 820, Sannomiya, Koshigaya, , Japan 3 Department of Anatomy and Human embryology, Institute of Embryology, Faculty of Medicine, Complutense University, Madrid 28040, Spain 4 Division of Internal Medicine, Iwamizawa Asuka Hospital, , Iwamizawa, , Japan Received for Publication, July 10, 2017 Key Words: teres major muscle, latissimus dorsi muscle, brother muscle, human embryo Summary: The teres major and latissimus dorsi muscles (TM, LD) are considered to be the so-called brother muscles. Actually, being similar to the TM, an uppermost part of the LD usually arises from the scapular plate. In embryos of 11 mm CRL, anlagen of the TM and LD appeared to be fused to provide a single mass at an angle between the axillary and radial nerves. However, splitting had already finished in not only the TM and LD but also the other muscles at and around the shoulder in specimens of 14 mm CRL. Thus, muscle splitting at the region appeared to occur simultaneously at a short stage of mm CRL.The TM and LD carried a common tendon still at 6 weeks (14 16 mm CRL), but their muscle bellies were separated clearly. A concept of brother muscles might be applied to the TM and LD according to a bias from the gross and comparative anatomy, not from the embryological view. Introduction The teres major and latissimus dorsi muscles (TM, LD) are considered to originate from a single a single truncozonal muscle in evolution (Frohse and Fränkel, 1908). In the primitive morphology, the TM-LD complex seems to be an antagonist to the anteriorly-located truncozonal muscle, i.e., the serratus anterior muscle. Actually, being similar to the TM, an uppermost part of the LD usually arises from the inferior angle of the scapular plate. Moreover, a band-like tendon of the LD winds around a rod-like TM tendon from the posterior aspect, via the inferior aspect to the anterior aspect. For the human shoulder, however, the TM-LD complex as well as the scapular attachment of LD may interfere with a smooth and wide movement at the thoracoscapular interface (an articulation-like space between the serratus anterior and external intercostal muscles). In this context, conversely, a primary connection or fusion between the TM and LD may be cut secondarily due to active movements at the shoulder. Previous descriptions on the fetal development of the TM and LD was very limited and they suggested a common anlage of them (e.g., Lewis, 1902). There is a well-known example in which a single muscle anlage divides into 2 muscles, i.e., the trapezius and sternocleidomastoid muscle, but this splitting occurs at 5 weeks (Keibel and Mall, 1910; Mekonen et al., 2016). Consequently, the aim of this study was to re-examine the initial development of TM and LD using histological sections of human embryos. Shin-ichi Abe and Koichiro Sakanaka contributed equally to this work. Corresponding author: Masahito Yamamoto, DDS, PhD. Department of Anatomy, Tokyo Dental College, Misaki-cho, Chiyoda-ku, Tokyo , Japan. yamamotomasahito@tdc.ac.jp

2 82 K. Sakanaka et al. Materials and Methods This study was performed in accordance with the provisions of the Declaration of Helsinki 1995 (as revised in 2013). We observed serial horizontal sections of the shoulder and upper extremity from 15 embryos and fetuses at 5 6 weeks (crown-rump length or CRL, mm). These sections were parts of the large collection kept at the Embryology Institute of the Universidad Complutense, Madrid, and were the products of miscarriages and ectopic pregnancies at the Department of Obstetrics of the University. Most sections were stained with hematoxylin and eosin (HE), while a minor part with azan, orange G or silver staining. The study was approved by Complutense university ethics committee (B08/374). Observations and taking photographs were usually performed with Nikon Eclipse 80. Results In embryos of 11 mm CRL (2 specimens), anlagen of the TM and LD appeared to be fused to provide a single mass (Fig. 1). Thus, the identification was based on the location at an angle between the axillary and radial nerves. The common anlage candidate was supplied by multiple nerve twigs from the angle between these 2 major nerves. In the 2 specimens, three heads of the triceps were not discriminated and arm flexors were appeared to be fused. At and around the shoulder, the trapezius, deltoid and pectoralis major were limited muscles to identify. In the other 13 embryos of mm CRL, the scapular origin of the TM was clearly distant from a thick muscle bundle of the LD (Figs. 2 and 3). Likewise, each of muscles on and around the scapula and humerus was able to be identified. Thus, muscle splitting in the arm and shoulder appeared to occur simultaneously at a short stage of mm CRL. Primary muscle tubes started development in most of the muscles although whether the identification was easy or difficult depended on the sectional plane of the muscle. Insertion tendons of the TM and LD joined at an angle between the axillary and radial nerve (Figs. 2E and 3E). Higher magnification views of the combined tendon did not suggest a remnant of fusion or separation, but the entire part was composed of regularly arrayed mesenchymal cells. Therefore, the separation between the TM and LD appeared to start from the scapular or dorsal side. We did not find the scapular origin of the uppermost part of the LD. Fig. 1. Horizontal sections from an embryo of 11 mm (5 weeks). Azan staining (panel A) and HE staining (panels B and C). Panel A (or C) displays the most inferior (or superior) site in the figure. Intervals between panels are 0.05 mm. In panel C, anlagen of the teres major and latissimus dorsi muscles are identified as a single mass (TM+LD) and innervated by multiple nerve twigs from an angle between the axillary and radial nerves (AN, RN). All panels were prepared at the same magnification (scale bar in panel C, 1 mm). Other abbreviations, see the common abbreviation. Discussion According to the present observations, a separation between the TM and LD seemed to be caused by development and topographical change of the scapular plate. Depending on an elongation of the plate and its separation from the humerus, the TM was most likely to be pulled dorsally and inferiorly. In contrast, the LD maintained its bundle-like shape as seen in the early anlage of 11 mm CRL. In the beginning of this study, we speculated that a

3 Fetal teres major muscle 83 Fig. 2. Horizontal sections from an embryo of 14 mm (6 weeks). HE staining. Panel A (or F) displays the most inferior (or superior) site in the figure. Intervals between panels are 0.2 mm (A B), 0.15 mm (B C), 0.1 mm (C D) and 0.05 mm (D E, E F), respectively. In panels A and B, the scapular origin of the teres major muscle (TM) is distant from the muscle bundle of latissimus dorsi muscle (LD). Insertion tendons of these muscles reach an angle between the axillary and radial nerves (AN, RN) in panel D and both tendons join in panel E. All panels were prepared at the same magnification (scale bar in panel A, 1 mm). Other abbreviations, see the common abbreviation.

4 84 K. Sakanaka et al. Fig. 3. Horizontal sections from an embryo of 15 mm (6 weeks). HE staining. Panel A (or F) displays the most inferior (or superior) site in the figure. Panel C (or E) is the higher magnification view of teres major tendon in panel B (or D). Intervals between panels are 0.3 mm (A B), 0.2 mm (B D) and 0.1 mm (D F), respectively. Scapular origin of the teres major muscle (TM) is distant from the latissimus dorsi muscle (LD) in panel A. Their insertion tendons join at an angle between the axillary and radial nerves (AN, RN) in panel D. Scale bars: 1 mm in panels A, B, D and F; 0.1 mm in panels C and E. Other abbreviations, see the common abbreviation.

5 Fetal teres major muscle 85 primary connection or fusion between the TM and LD is cut secondarily due to active and wide movements at the thoracoscapular interface. Actually, the serratus anterior muscle (a major muscle acting the interface) developed early and its fan-like shape was established at 6 weeks in which the TM and LD carried a common insertion tendon. However, a large loose space between the scapular plate and rib cage suggested no active movement such as wide rotation. Even in embryos, a muscle contraction is liable to provide a fascia from the primitive loose tissue (Miyake et al., 2010). Notably, muscle splitting in the arm and shoulder appeared to occur simultaneously at a very short period corresponding to mm CRL. This is almost consistent with Lewis (1902). Therefore, a common anlagen of the TM and LD was not more evident than the other common anlagen such as flexor muscle anlagen. We expected, in embryos, the so-called brother muscles maintaining the common muscle belly at a period much longer than muscles surrounding them. Indeed, the TM and LD carried a common tendon still at 6 weeks, but their muscle bellies were separated clearly. Moreover, a scapular origin of the LD was likely to develop secondarily because we did not find it. A concept of brother muscles might be applied to the TM and LD according to a bias from the gross and comparative anatomy, not from the embryological view. Although the coracobrachialis and biceps short head are difficult to discriminate in embryos arm (Yamamoto et al., 2016), they might never be called the brother muscles. Likewise, in spite of the common anlagen seen in stages much later than establishment of other flexors (Rodríguez-Vázquez et al., 2017), nobody might consider the flexor pollicis longus and flexor digitorum profundus muscles of the forearm as a pair of brothers. A comparative embryological study of the TM and LD seemed to be necessary using quadrupedal animals in which an active rotation movement is limited in the thoracoscapular interface. References 1) Frohse M, Fränkel M: Die Muskeln des menschlichen Arms. In: Bardeleben K (ed), Handbuch der Anatomie des Menschen. Band II, Abt II, Teil II, Gustav Fischer, Jena, 1908; ) Lewis WH: The development of the arm in man. Am J Anat 1902; 1: ) Keibel F, Mall FP: Manual of Human embryology. vol 1. Lippincott, Philadelphia, 1910; ) Mekonen HK, Hikspoors JPJM, Mommen G, Eleonore Kőhler S, Lamers WH: Development of the epaxial muscles in the human embryo. Clin Anat 2016; 29: ) Miyake N, Hayashi S, Cho BH, Kawase T, Murakami G, Fujimiya M, Kitano H: Fetal anatomy of the human carotid sheath and structures in and around it. Anat Rec 2010; 293: ) Yamamoto M, Takayama T, Takada H, Shiraishi Y, Tomita N, Sakanaka K, Murakami G, Rodríguez-Vázquez JF, Abe SI: Coracobrachialis muscle and the musculocutaneous nerve: A study using human embryonic sections. Okajimas Folia Anat Jpn 2016; 93: ) Rodríguez-Vázquez JF, Jin ZW, Murakami G, Jin Y: Fetal development of digastic muscles in human body: A review and a finding in the flexor digitorum superficialis muscle. Ann Anat 2017 in press. Figure legend Common abbreviation for figures: AA, axillary artery; AN, axillary nerve; ES, esophagus; GHJ, glenohumeral joint; H, humerus; LD, latissimus dorsi muscle; MN, median nerve; R, radius; RN, radial nerve; S, scapula; SA, serratus anterior muscle; SS, subscapularis muscle; TM, teres major muscle; TR, trapezius muscle; UN, ulnar nerve VB, vertebral body; VN, vagus nerve.