Neck muscle homology: cucullaris and hypobranchial
As mentioned earlier, the muscles that connect the head with the pectoral girdle can be divided into two main groups of muscles, the dorsal cucullaris and its derivatives, which attach to the back of the skull, the neck vertebrae and to the pectoral girdle (Edgeworth, 1935), and the ventral hypobranchial group (Figs 4–7). These comprise most of the muscles of the tongue and the muscles attaching the branchial or hyoid apparatus and their derivatives to the pectoral girdle (Edgeworth, 1935). The cucullaris muscle is present in all major clades of gnathostome vertebrates, with the exceptions of some Actinopterygii (Winterbottom, 1974; Greenwood & Lauder, 1981), caecilians (Edgeworth, 1935) and snakes (Edgeworth, 1935). Some batoids (skates and rays), sturgeons (Edgeworth, 1935) and coelacanths (Millot & Anthony, 1958) also lack the cucullaris muscle. It is primitively innervated by the ramus accessorius of the Vagus (X) nerve in anamniotes, whereas in amniotes the Accessorius (XI) nerve provides most of the nerve supply (Edgeworth, 1935). The cucullaris is generally considered to be homologous between vertebrates (Edgeworth, 1935; Greenwood & Lauder, 1981; Diogo & Abdala, 2010), based on development, innervation and anatomy; however, the nomenclature is highly variable. It has been described under many different names, e.g. as trapezius in shark (Vetter, 1874; Edgeworth, 1911; Allis, 1917), amphibians (Piatt, 1938) and chick (Noden & Francis-West, 2006), dorsoclavicularis in lungfish (Greil, 1913), protractor pectoralis in osteichthyan fish (Winterbottom, 1974; Greenwood & Lauder, 1981; Diogo & Abdala, 2010) and amphibians (Diogo & Abdala, 2010). In textbooks (e.g. Homberger & Walker, 2004; Kardong, 2009) and studies on cranial muscle development, the term ‘cucullaris’ is commonly used to describe the single muscle of anamniotes such as sharks (Edgeworth, 1935; Kuratani, 2008), amphibians (Edgeworth, 1935; Kesteven, 1944; Piekarski & Olsson, 2007) and the single muscle of amniotes prior to its developmental subdivision into the trapezius and sternocleidomastoideus complex, as in birds (Huang et al. 1997; Noden et al. 1999; Theis et al. 2010). For more extensive reviews on the nomenclature and homology of cranial muscles see Edgeworth (1935) and Diogo & Abdala (2010). In amniotes, the cucullaris commonly develops into two parts: the trapezius and sternocleidomastoideus complex, which may be subdivided further (Diogo & Abdala, 2010). The nomenclature of these muscles is also highly variable (Fürbringer, 1902; Edgeworth, 1935; Diogo & Abdala, 2010).
Figure 5. Muscles of the neck and pectoral region of a salamander, Necturus maculosus. The muscle in blue is derived from the cucullaris and the muscles in green are from the hypobranchial group (modified from Wilder, 1912). oh, omohyoideus; rc, rectus cervicis; rhp, rectus superficialis hypobranchialis posterior; t, trapezius.
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Figure 6. Muscles of the neck and pectoral region of a bird, Cyanocorax cyanopogon. The muscles in blue are derived from the cucullaris and the muscles in green are from the hypobranchial group (modified from Fürbringer, 1902). clhy, cleidohyoideus; cuc, cucullaris and sternocleidomastoideus; cuc.1, cranial part of cucullaris; cuc.2, cervical part of cucullaris; cuc.dc, cucullaris dorsocutaneus; cuc.pt, cucullaris propatagialis.
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Figure 7. Anatomy of the neck and shoulder region of a rabbit. The muscles in blue are derived from the cucullaris and the muscles in green are from the hypobranchial group. Please note that although dsc-i, musculus dorsoscapularis inferior, is also considered to be part of the cucullaris group, there is currently no description of its development (modified from Streissler, 1900). clm, cleidomastoideus; cloc, cleidooccipitalis; dsc-s, dorsoscapularis superior; sh, tendon; stms, sternomastoideus superficialis; sth, sternohyoideus; stth, sternothyroideus.
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The cucullaris muscle has traditionally been regarded as a part of the posterior branchial arch musculature of the head, based on the innervation and anatomy, e.g. Vetter’s comparative work on the anatomy of the jaw and branchial muscles of fish (Vetter, 1874). Unfortunately, very few early studies on muscle development mention the cucullaris. Greil (1913), in his extensive study of embryos of Australian lungfish (Neoceratodus forsteri), considered it to be derived from the second somite, whereas Edgeworth (1935) described it as derived from the posterior edge of the caudalmost branchial muscle plate in the same species. Piatt (1938) mentioned that apart from being derived from the caudalmost branchial levator muscle, the cucullaris in Ambystoma maculatum potentially also receives a contribution from ‘the dorsolateral spinal muscle primordium’, which would imply a partial somitic origin. McKenzie (1962) noted that in some mammals, the ‘deep’ part (relative to the position of the Accessorius nerve) of the sternomastoideus was likely to have a somitic contribution. This condition was observed in humans and pig but not in rabbit. Edgeworth (1911, 1935), on the other hand, considered the cucullaris to be derived from the caudalmost branchial arch mesoderm in all gnathostomes with exception of sharks, where it was derived from the dorsal edge of all of the five branchial muscle plates; this was contested by Allis (1917). Edgeworth also considered birds to lack a cucullaris, instead having a cranio-cervicalis muscle derived entirely from the first four somites rather than non-segmented cranial mesoderm. Although Edgeworth’s idea of a cranio-cervicalis muscle was not widely accepted, support for a somitic contribution to the cucullaris muscle in birds increased with the discovery of the heterochromatin condensations in quail cells by Le Douarin in 1969; and the quail-to-chick chimaera system for tracing embryonic cell fate. Noden traced both neural crest cells (1983a) and mesoderm (Noden, 1983b, 1986, 1988; Noden et al. 1999) in chicken, showing that the cucullaris received its muscle cells and connective tissue from somitic mesoderm. This was confirmed by an extensive study by Couly et al. (1993), showing that the first six somites provide cells to the cucullaris in chick, and was re-examined in studies by Huang et al. (1997, 2000), who mapped the origin of the cucullaris in chick to mainly the first three somites. Using Wnt1 and Sox10 constructs in mouse to drive expression of GFP in neural crest cells, Matsuoka et al. (2005) showed that the connective tissue of the trapezius and sternocleidomastoideus, and also the cartilage at the attachment points on the pectoral girdle, were derived from neural crest cells. Using another genetic construct, the myofibres were shown to be derived from HoxD4-expressing mesoderm and this was presumed to represent a somitic origin for these muscles. Valasek et al. (2010), also using a Wnt1 transgenic construct, confirmed the presence of neural crest cells in the connective tissue. In anamniotes, the somitic contribution to the cucullaris muscle was confirmed by Piekarski & Olsson (2007), using FITC-dextran injections in Ambystoma mexicanum embryos. In view of this large body of evidence suggesting a somitic origin of the cucullaris, the results from Theis et al. (2010) were surprising. They modified the somite transplantation technique used by Huang et al. (2000), and showed that the cucullaris muscle of chick was primarily derived from the occipital lateral plate mesoderm lateral to somites one to three (Fig. 1) and not from the somites. Added support came from molecular data showing that the development of the cucullaris muscle utilized the same genetic pathways as the other pharyngeal arch muscles (with the exception of the hypobranchial and extra-ocular muscles), rather than pathways associated with the trunk musculature.
In contrast to the cucullaris muscle and its derivatives, the study of the hypobranchial group of muscles has been less controversial. They are innervated by the spinal Hypobranchialis nerve in anamniotes and the Hypoglossus nerve (XII) in amniotes, and fall into two main groups, the rostral geniohyoideus and the caudal rectus cervicis muscles (Edgeworth, 1935). It should be noted that there are a number of other muscles in the same area but those are derived from unsegmented paraxial head mesoderm and are innervated by Trigeminus (V), Facialis (VII), Glossopharyngeus (IX), Vagus (X) or spinal nerves (Edgeworth, 1935). In gnathostomes, cells from the ventro-lateral part of a varying number of anterior somites migrate ventral to the pharyngeal arches in a structure called the hypoglossal chord (Fig. 8; Hunter, 1935). The geniohyoideus gives rise to most of the muscles of the tongue in tetrapods, whereas the rectus cervicis gives rise to muscles connecting the branchial and hyoid apparatus to the ventral pectoral girdle and sternum (Edgeworth, 1935). In the shark, geniohyoideus and rectus cervicis are derived from several of the more caudal somites and give rise to the geniocoracoideus (van Wijhe, 1882; Dohrn, 1884; Edgeworth, 1935; Allis, 1917 called this muscle coracomandibularis) and rectus cervicis (Edgeworth, 1935; Allis, 1917 called this muscle coracohyoideus; Diogo & Abdala, 2010 described it as sternohyoideus). The somitic contribution to these was confirmed in Australian lungfish (Greil, 1913; Edgeworth, 1935) and amphibians (Platt, 1897; Lewis, 1910; Edgeworth, 1935; Piatt, 1938; Martin & Harland, 2006; Piekarski & Olsson, 2007). However, most of the available data on the development of the hypobranchial muscles is, as in the case of the cucullaris, derived from studies of birds. Edgeworth (1935) considered that only one somite contributed cells to the hypobranchial muscles in chick, but most other studies list a varying number of somites. Hunter (1935) described the tongue muscles as derived from the first seven somites based on histology, which was partly confirmed by Deuchar’s (1958) study of the fate of the first three somites using carbon particles, and Hazelton’s (1970) study using tritium-labelled thymidine in the first four somites. Noden (1983b, 1986) found a contribution from somites two to five, using quail-chick chimaeras. Couly et al. (1993), using the same method, showed that the hypobranchial muscles were derived from the first five somites. Huang et al. (1999) re-examined the developmental fate of single somites in the neck region and found that somites two to six give rise to all the hypobranchial tongue muscles in chick. The connective tissue component of the rostral hypobranchial muscles was shown by Le Lièvre & Le Douarin (1975) to be neural crest cell-derived in chick. This was later confirmed and expanded by Noden (1983a) and Kontges & Lumsden (1996). The first description of neural crest cell contribution to the caudal attachment of the hypobranchial muscles to the pectoral girdle was provided by McGonnell et al. (2001), tracing a population of neural crest cells to the attachment of the cleidohyoid muscle (derived from rectus cervicis; Edgeworth, 1935) to the clavicle in chick. This was confirmed in all the hypobranchial muscles of the mouse by the study of Matsuoka et al. (2005). In summary, the major neck muscles are all connected by neural crest-derived connective tissues; the hypobranchial muscles are clearly somatic-derived and controversy exists whether the cucullaris anlagen is of somitic or cranial origin.
Figure 8. Diagram of stage 19 chick embryo, showing the cells migrating from the ventral somites into the hypoglossal chord (grey) and further anterior into the head region (modified from Hunter, 1935). H, hypoglossal chord; O, otic vesicle; p1–p3, pharyngeal pouches; s2–s4, somites two to four.
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Neck musculature: skeletal attachments
The skeletal elements involved in the neck region include the skull or braincase, branchial arches, and the pectoral or shoulder girdle. The latter girdles have changed substantially through vertebrate evolution with a reduction in the dermally derived elements and increase in the endochondral structures, including the scapula and coracoid, which also change through evolution (Kardong, 2009). The dermally derived bones include the cleithrum, clavicle and interclavicle, as well as a series of small bones that connect the skull to the pectoral girdle in many fish: anocleithrum, supracleithrum, post-temporal. As dermal bones, these structures develop in the dermis via epithelial–mesenchymal interactions, whereas endochondral bones form from a mesodermally derived cartilaginous precursor. Neural crest contributes to most cranial dermal bones and postcranially, as far as is currently known, to the turtle plastron, alligator gastralia and zebrafish dermal caudal fin rays (Couly et al. 1993; Smith et al. 1994; Gilbert et al. 2007). However, given the predominance of dermal bone in the head and trunk skeletons of early fossil vertebrates, Smith & Hall (1990, 1993) suggested that neural crest also contributed to these bony skeletons. Dermal and endochondral ossifications were considered developmentally separate until work by Matsuoka et al. (2005) which indicated that the mouse scapula had a dual origin, based on the attached musculature and, more specifically, the muscle connective tissue. In this study, it was observed that most of the scapula was mesodermally derived but neural crest-derived muscle connective tissue attached to the scapular spine, and the anterior part of the spine itself was said to be neural crest-derived, rather than from mesoderm. Thus it is muscle connectivity that determined developmental origin of these bones. However, this was questioned in a subsequent paper by Valasek et al. (2010: p. 487), who observed that neural crest cells were only ‘scattered on the surface’ of the scapular spine. Other researchers have demonstrated that the dorsal part of the tetrapod scapula is derived from anterior somites rather than lateral plate mesoderm, including the region where the cucullaris muscle would attach (summarized by Piekarski & Olsson, 2011; Fig. 6; Shearman et al. 2011).