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The Musculature of the Mouse Tail Is Characterized by Metameric Arrarmements of Bicipital Muscles

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The Musculature of the Mouse Tail Is Characterized by Metameric Arrarmements of Bicipital Muscles Okajimas Folia Anat. Jpn.. 76(4): 157-170, October. 1999 The Musculature of the Mouse Tail is Characterized by Metameric Arrarmements of Bicipital Muscles By Harumichi SHINOHARA Division of Human Sciences, Toyama Medical and Pharmaceutical University, Toyama 930-0194, Japan —Received for Publication, March 18, 1999 — Key Words: Mouse tail, Muscular system, Bicipital muscle, Metameric arrangement Summary: This is the first report, to our knowledge, of the full characterization of the musculature of the mouse tail. Bicipital muscles form a major part of the tail musculature. The tail tendons originate with fusiform muscle from the dorsal and ventral lumbo-sacro-coxal regions and are inserted into the coccygeal vertebrae (extrinsic muscles of the tail). Each coccygeal vertebra has short muscles that terminate on the adjacent vertebrae (intrinsic muscles of the tail). The short muscle and its corresponding tail tendon are joined, thereby forming a bicipital muscle that is inserted into the coccygeal process. A geographical correspondence is strictly maintained between the origin of the tendon in the lumbo-sacro-coxal region and the insertion of the bicipital muscle in the coccygeal vertebrae. In other words, the or- ganization of the tail musculature is based upon repetitions of fusion between the extrinsic and intrinsic muscles at each coccygeal vertebral level. This design is referred to as the metameric arrangement of the bicipital musdes. The organi- zation, arrangement and function of muscles in the tail have features in common with those muscles in the digits of the human extremities. The tail occupies a special position in develop- mel et al., 1966). Cook (1983) stated that the muscle ment (Holmdahl, 1925; Griffith et al., 1992). A mass arrangements of the mouse and rat are very similar of pluripotent mesenchymal cells, the tail bud, is and that descriptions of the muscular system of the believed to give rise to the ectodermal, mesodermal rat are applicable to the mouse. There are two and endodermal tissues of the tail (see the discus- standard texbooks of rat anatomy: Anatomy of the sion section). Genetic approaches have been made Rat (Greene, 1968) and Anatomy and Embryology to define the role of the tail bud in organogenesis of of the Laboratory Rat (Hebei and Stromberg, the tail (Takeda et al., 1994; Matsuura et al., 1998). 1986). A description of the tail musculature is in- Recently, Gofflot et aL (1997) examined the genetic cluded only in the latter textbook. Strocchi et al. patterning of the developing mouse tail at the time (1985) examined histologically organization of the of closure of the posterior neuropore. They ob- tail tendons and their connective tissue investments served continuity of the expression of several genes but did not clarified the gross anatomical aspects of from the primitive streak and node into sub- the tail musculature, e.g., where do the tendons populations of the tail bud and caudal axial struc- originate from and terminate. The present study tures prior to their histological differentiation of was performed to clarify the muscular organization these structures. However, these attempts have of the mouse tail. been hampered by the fact that the anatomical or- ganization of the mouse tail has not yet been fully characterized. Materials and Methods Useful descriptions of the musculature of the mouse are largely lacking. There are several text- Six mice, C57BL/6 strain, of 20-25 weeks of age, books of mouse anatomy, but they do not contain were used without regard to male or female for descriptions of the musculature (Cook, 1965; Hum- dissection and examination of tail muscles. Mice Part of this work was supported by a Grant-in-Aid for Scientific Research no. 0167-0010 and a Grant from Yokota Foundation in Toyama Medical and Pharmaceutical University. 157 158 H. Shinohara were killed by inhalation of ethyl ether vapor. They Overall View were skinned, fixed in 10% formalin for one week The tail is defined osteologically as the coccygeal and rinsed in tap water for a day or two. Tails were region that extends from the lumbo-sacro-coxal re- removed from two animals and kept in a 0.5 M so- gion. It consists of a base and a body but the border lution of EDTA sodium salt (4Na), pH 7.4, for between them is not clearly defined (Figs. 1, 2 and three months. Each tail was cut, perpendicularly to 3). Muscles are distributed in the lumbo-sacro-coxal the long axis, into slices of 1-2 mm in thickness region. The region can be divided roughly into with a pair of razor blades and each slice was de- three portions: medial, intermediate and lateral fatted in absolute ethanol for one day. The slices (Figs. 4, 5 and 6). The body of the tail has eight were then hydrated in distilled water and stained stripes along its long axis. These stripes consist of faintly in a weak solution of alizarin red (i.e., a few four fasciculi of tendons and four stripes of non- drops of 0.01% alizarin red in 100 ml of distilled tendinous tissue that are arranged alternately. water). The bodies of the remaining four animals The non-tendinous tissue is composed princi- were cut into the cranial and caudal halves at the pally of muscles. These muscles are short muscles thoraco-lumbar border and the caudal half was that span two or three coccygeal vertebrae. The placed in a weak solution of alizarin red in order to dorsal short muscles originate from the midsagittal stain bone tissues. They were dissected under a fascia and cranial articular process and they are in- dissecting microscope. serted into the cranial articular process at more distal vertebrae. The lateral short muscles originate from the caudal transverse process and they termi- Results nate on the transverse process at more distal verte- brae. The medial short muscles originate from the Preliminary Results cranial hemal process and they are inserted into the Some aspects of the skeletal organization of the cranial hemal process of the next vertebra. Some mouse tail are included in this report because they muscle fibers of the proximal short muscle usually are important for considerations of the functions of extend beyond the insertions and participate in the the tail muscles in movements of the tail (see Shi- formation of the short muscles at more distal ver- nohara, 1999 for details). The tail usually consists of tebrae. Thus, a long stripe, composed of continuous 29 coccygeal vertebrae (Col—Co29). Each coccy- short muscles, is formed. geal vertebra consists of a body, cranial and caudal There are two fasciculi of tendons on each (left articular processes, cranial and caudal transverse or right) side, and the transverse process divides processes and cranial and caudal hemal processes. them into the dorsal and ventral fasciculi (Figs. 1, 2 The vertebral arch is formed from Col to Co4 but and 3). The dorsal fasciculus (Fig. 7) consists of is not formed at Co5. Thus, a spinous process is tendons that are inserted into the cranial articular present from Col to Co4 but is not at vertebrae process. The most proximal insertion of the dorsal caudal to Co5. Adjacent vertebrae are connected tendons is at Co5. The ventral fasciculus includes by two joints, one that involves the articular proc- two categories of tendons, the lateral and medial esses and the other that involves the intervertebral tendons. The lateral tendons (Fig. 8) are inserted discs. The second and third coccygeal vertebrae are into the cranial transverse process at Co6 and more connected by both joints but the third and fourth distal levels. The medial tendons (Fig. 9) converge coccygeal vertebrae lack the former connection. on the ipsilateral sesamoid bones and are inserted Thus, the vertebrae distal to Co4 are connected into the cranial hemal processes. The most proxi- end-to-end only via intervertebral discs. The con- mal insertion of the medial tendon is at Co6. nection via the articular processes limits the direc- Clearly, Co5 (or Co6) is the landmark coccygeal tion and extent of skeletal movements. Loss of this vertebra for the attachment of the tail tendons. The articulation between Co3 and Co4 and distal to Co4 region proximal to this landmark is tentatively de- gurantees the freedom of tail movements. One pair fined as the tail base and the region distal to it is the of sesamoid bones is found at each intervertebral tail body. All vertebrae distal to Co6 are attached level. The first pair appears between Col and Co2 to the three (dorsal, lateral and medial) tendons. and at least 25 paris can be distinguished under Therefore, when a tail consists of 29 coccygeal ver- a dissecting microscope. The second pair usually tebrae, 73 tendons (25 dorsal tendons, 24 lateral fuses and forms a single, wing-nut-shaped (ses- tendons and 24 medial tendons) pass on one (left or amoid) bone. thus, there are usually 49 sesamoid right) side of the fifth coccygeal vertebra, 70 ten- bones in the tail. The sesamoid bones are sites of dons on one side of the sixth coccygeal vertebra insertion of the ventral tendons of the tail. and 67 tendons on one side of the seventh vertebra. Musculature of the Mouse Tail 159 Cross Sections of the Tail vertebrae. The dorsal tendons are the extrinsic Cross sections perpendicular to the long axis of muscles of the tail. The dorsal tendons join with the tail revealed that the dorsal midsagittal fascia, corresponding dorsal short muscles (intrinsic tail vertebral body and ventral connective-tissue sep- muscles) to form bicipital muscles (see below, next tum divide the tail into left and right hemispheres paragraph). The dorsal tendons might be involved (Figs.
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