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Zebrafish Myology
C H A P T E R
12 Zebrafish Myology Frank J. Tulenko, Peter Currie Australian Regenerative Medicine Institute, Monash University, Clayton, VIC, Australia
Embryonic Origins
Head Muscles
The myofibers that comprise skeletal muscle can vary in their embryonic origin, molecular patterning, and physiology, depending on the location and function. Most craniofacial muscles develop from unsegmented head mesoderm using genetic programs distinct from trunk myomeres, which form from postcranial spheres of cells termed somites (Bryson-Richardson & Currie, 2008). Both head and trunk muscles contain physiologically distinct fast and slow myofibers, the proportions of which can change over time (Hernandez, Patterson, & Devoto, 2005). Slow-twitch muscle fibers are fatigue resistant, metabolically oxidative, heavily vascularized, and are the first fiber type to arise in zebrafish. Fast-twitch fibers function in rapid, powerful actions and are metabolically glycolytic. Studies of postcranial myogenesis have shown that during development, fast and slow fiber types segregate through complex cellular movements within each somite. Slow myofibers arise along the midline and migrate laterally to a superficial position along the myotome. Fast myofibers, in contrast, form from two distinct intrasomitic populations. Cells of the posterior somite differentiate into fast myofibers, whereas cells of the anterior somitic border migrate laterally to form a thin monolayer superficial to the slow fibers. These “external cells” then secondarily ingress between slow myofibers to form additional fast fibers (Bryson-Richardson & Currie, 2008; Stellabotte & Devoto, 2007). Ultimately, the slow muscle fibers form a wedgelike stripe that is positioned lateral to the horizontal septum, running outside and parallel to the fast fibers, which comprise the bulk of the trunk musculature.
The Zebrafish in Biomedical Research https://doi.org/10.1016/B978-0-12-812431-4.00012-9
Extraocular Muscles Similar to other vertebrates, zebrafish rotate their eyes using six extraocular muscles: the superior and inferior obliques, and the medial, lateral, superior, and inferior rectus muscles all of which form by around 72 hpf (Easter & Nicola, 1996) (Fig. 12.1). In 96 hpf fish, both the superior and inferior obliques originate along the rostral orbit and insert on the dorsal and ventral surfaces of the eye, respectively. The superior, inferior, and medial rectus muscles arise from a similar site along the posterior orbit. Whereas the superior and inferior rectus insert just caudal to the superior and inferior obliques, the medial rectus extends between the obliques, inserting on the anteromedial surface of the eye. Unlike the other rectus muscles, the lateral rectus originates outside of the orbit posterior to the diencephalon and inserts on the posterior sclera (Kasprick et al., 2011). Notably, the insertion sites of the superior oblique and rectus muscles overlap in adults (Fig. 12.1B). A similar late overlap has been shown for the inferior oblique and rectus (Kasprick et al., 2011) (Fig. 12.1C). Three cranial nerves (CN) innervate the extraocular muscles: CNIII innervates the inferior oblique, superior rectus, inferior rectus, and medial rectus; CNIV innervates the superior oblique; and CNVI innervates the lateral rectus (Schilling & Kimmel, 1997). Interestingly, a visually evoked startle response develops about 20 h later than the touch startle response, roughly coincident with early maturation of the extraocular muscles (Easter & Nicola, 1996).
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FIGURE 12.1 Extraocular muscles. (A). Ventral view of the six extraocular muscles of a 96 hpf larvae (modified from the camera lucida drawing of Easter and Nicola, 1996:fig11). Dashed lines indicate deeper structures. (B,C). Adult transgenic [Tg(a-actin:EGFP)] with muscle GFP (Kasprick et al., 2011:fig2). Arrowhead marks muscle overlap. ant, anterior; dors, dorsal; IO, inferior oblique; IR, inferior rectus; LR, lateral rectus; MR, medial rectus; post, posterior; SO, superior oblique; SR, superior rectus; vent, ventral.
Arch-associated Muscles In jawed vertebrates, craniofacial muscles develop in association with segmentally arranged arches surrounding the pharynx, an embryological feature reflected in adult patterns of innervation. Zebrafish possess seven pairs of pharyngeal arches: anterior-to-posterior, these are the mandibular arch, hyoid arch, and five gillassociated branchial arches, each with distinct skeletal elements and muscles (Cubbage & Mabee, 1996; Schilling & Kimmel, 1997). Mandibular Arch Muscles Muscles associated with the first arch (mandibular arch) include the intermandibularis, adductor mandibulae, and a dorsal group consisting of the levator arcus palatini and dilatator operculi, all of which are innervated by CNV (Fig.12.2) (Schilling & Kimmel, 1997). The intermandibularis anterior joins the left and right dentary bones (mandible) and remains largely unchanged between larval and adult stages. The intermandibularis posterior becomes associated with the interhyoideus (a second arch muscle) in larvae (Fig.12.2B), forming a continuous muscle, the protractor hyoideus. In adults, the protractor hyoideus is longitudinally split into dorsal and ventral portions connecting the anterior ceratohyal and ventral hypohyal bones with the dentary (Fig.12.2D) (Diogo, Hinits, & Hughes, 2008). The protractor hyoideus depresses the mandible and is innervated by both CNV and VII, reflecting its complex ontogeny (Diogo et al., 2008).
In early larvae, the adductor mandibulae initiate as a single mass (Fig.12.2A,B), but in adults subdivides into four bundles: A0, A1, A2, and Au (Fig.12.2B) (Diogo et al. 2008). Collectively, A0, A1, and A2 primarily extend below the eye, connecting the preopercle (A0, A1, A2), quadrate (A0, A1), hyomandibula (A2), and metapterygoid (A2) with the mandible and maxilla (Diogo et al., 2008). Au originates along the medial surface of the mandible (angulo-articular and dentary) and inserts on the tendon of A2. Whereas the adductor mandibulae complex primarily closes the mouth, the maxillary component (specific to A0) functions in mouth protrusion (Diogo et al., 2008). Larval zebrafish possess a single dorsal mandibular premuscle mass, which segments to form the levator arcus palatini and the dilatator operculi in adults (Fig.12.2A,C) (Schilling & Kimmel, 1997). The levator arcus palatini originates along the sphenotic bone of the neurocranium and extends to the metapterygoid and hyomandibula to abduct/elevate the jaw suspensorium. The dilatator operculi neighbors the levator arcus palatini and lies superficial to the adductor hyomandibulae (a second arch muscle), joining the frontal and pterotic bones, hyomandibula, and opercle for opercular abduction (Diogo et al., 2008). Hyoid Arch Muscles Muscles associated with the second arch, the hyoid arch, include the interhyoideus, hyohyoideus, adductor hyomandibulae, adductor operculi, levator operculi, and adductor arcus palatini, all innervated by cranial nerve VII (Schilling & Kimmel, 1997; Diogo et al., 2008) (Fig.12.2). As mentioned above, the interhyoideus together with the intermandibularis posterior comprises the protractor hyoideus. By 4 dpf, the hyohyoideus consists of a wellformed hyohyoideus inferior, as well as posterior myofibers [hyohyoideus superior: Diogo et al. (2008)] that segregate to form the hyohyoideus abductor and adductors following ossification of the branchiostegal rays (Fig.12.2). In adults, the hyohyoideus inferior and abductor originate from the anterior ceratohyals and first branchiostegal ray, respectively, and meet their opposite partner along the jaw medial aponeurosis. The medialmost branchiostegal ray separates the hyohyoideus abductor from the laterally positioned adductors, which extend between the branchiostegal rays, opercle and subopercle. The hyohyoideus abductor and adductors expand and constrict the branchiostegal membranes, respectively (Diogo et al., 2008). The adductor operculi extends from the pterotic bone to the opercle for opercular adduction. The levator operculi originates along the ventrolateral margin of the pterotic, runs lateral to the adductor operculi, and inserts on the
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Head Muscles
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FIGURE 12.2 Cephalic muscles. Arch associated muscles in larval (A,B) and adult (C,D) zebrafish in lateral (A,C) and ventral (B,D) view. (A,B). Confocal maximum projections of 4 dpf Tg(Acta1:EGFP) larvae. Skeletal muscle is green. (C,D). Adult illustrations modified from Diogo et al (2008:fig5). In (D), part of the hyohyoideus adductors (HHAD), as well as the opercle (op), interopercle (iop), subopercle (sop), and preopercle (pop) are removed from the right side. A0, A1, A2, bodies of the adductor mandibulae (ADM); ABD, fin abductor; ABS, abductor superficialis; ADAP, adductor arcus palatini; ADS, adductor superficialis; AH, adductor hyomandibulae; angart, anguloarticular; AOP, adductor operculi; ARRV, arrector ventralis; BL5, fifth branchial levator; brI, branchiostegal ray I; cha, anterior ceratohyal; chp, posterior ceratohyal; cl, cleithrum; den, dentary; DPW, dorsal pharyngeal wall muscle; DOP, dilatator operculi; en, entopterygoid; EP, epaxialis; f, frontal; fr, fin rays; hh, ventral hypohyal; HHAB, hyohyoideus abductor; HHI, hyohyoideus inferior; HYP, hypaxial muscle; INTMA, intermandibularis anterior; LAP, levator arcus palatini; LOP, levator operculi; mnd, mandible; mx, maxilla; osph, orbitosphenoid; pa-exs, parieto-extrascapular; para, parasphenoid; post, posttemporal; PRD, dorsal protractor hyoideus; prmx, premaxilla; PRV, ventral protractor hyoideus; pt, pterotic; rmb, medial branch ramus mandibularis; scl, supracleithrum; SH, sternohyoideus; sph, sphenotic; TV, transversalis ventralis.
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opercle (Fig.12.2C). In zebrafish, as in other teleosts, the levator operculi is thought to function through the opercular series and the interoperculo-mandibular ligament in lower jaw depression (Diogo et al., 2008). The adductor hyomandibulae extends from the neurocranium to the medial margin of the hyomandibula. The adductor arcus palatini extends from the neurocranium to the hyomandibula, metapterygoid, and entopterygoid, antagonizing the function of the levator arcus palatini by adducting the jaw suspensorium (Diogo et al. 2008). Posterior Branchial Arch Muscles At 96 hpf, the muscles associated with the posterior branchial arches include the dorsal pharyngeal wall muscles [branchial levatores: Hernandez et al. (2005)], rectus ventralis, transversus ventralis, and rectus communis [Schilling & Kimmel, 1997; see also Winterbottom (1974) for review] (Fig.12.2A,B). The dorsal pharyngeal wall muscles are positioned between the dorsal branchial cartilages and neurocranium (Hernandez et al., 2005). In both larvae and adults, the anterior-most levatores are relatively small, whereas the fifth is larger for its role in feeding and consists exclusively of fast fibers (Hernandez et al., 2005). The transversus ventralis muscles function in respiration and extend from the ceratobranchials to the median raphe of the ventral midline (Schilling & Kimmel, 1997). The rectus ventralis muscles are positioned between the aforementioned branchial arch muscles, joining adjacent ceratobranchials. In contrast, the rectus communis forms a band that extends across the third through fifth branchial arches (Schilling & Kimmel, 1997). Branches of CNIX and X innervate the muscles of the posterior branchial arches (Schilling & Kimmel, 1997). Hypobranchial Muscles Zebrafish possess a single hypobranchial muscle, the sternohyoideus. Unlike the cranial mesoderm-derived pharyngeal muscles described above, the sternohyoideus arises from postcranial somitic mesoderm that becomes secondarily anteriorized during development, a process likely mediated by the growth dynamics of the circumpharyngeal tissues (Lours-Calet et al., 2014). Interestingly, the anterior somites that give rise to the sternohyoideus also contribute striated myofibers to the esophagus for ingestion (Minchin et al., 2013). Whereas the sternohyoideus muscles are paired in larvae (Fig.12.2A,B), they form a single sheet in adults, extending from the cleithrum to the urohyal (Fig.12.2C,D). Anterior branches of the occipito-spinal nerves innervate the sternohyoideus, which functions in hyoid depression, suspensorium abduction, and mouth opening (Diogo et al., 2008).
Trunk Muscles The trunk musculature of zebrafish consists of approximately 32 muscle blocks (myomeres), which reflect somitic segmentation. Vertical connective tissue myosepta separate the myomeres and transmit their contractions to the skeleton for locomotion. In addition to vertical myosepta, zebrafish possess horizontal myosepta that split each myomere into dorsal epaxial and ventral hypaxial regions (Figs.12.2C and 12.3A). In adult teleosts, the epaxial myomeres collectively comprise the epaxialis muscle (Fig.12.2C). In addition to the epaxial and hypaxial myomeres, a transient muscle, the hypaxialis posterior, contributes to the ventral body wall of early larvae (Fig. 12.3A) and is thought to function with the sternohyoideus in suction feeding (Hernandez, Barresi, & Devoto, 2002). The hypaxialis posterior arises using a developmental program similar to the appendicular muscles (Haines et al., 2004), and in adult pearlfish, it is incorporated into the obliquus inferior (hypaxial body wall muscle) (Windner et al., 2011).
Pectoral Fin Muscles In zebrafish, the pectoral fins develop in two continuous phases. The first starts with the onset of fin bud outgrowth around 26 hpf and is marked by the formation of a fin skeleton consisting of an endoskeletal disc proximally and actinotrichia distally. The second phase begins during the third week of development and involves fin rotation, remodeling of the endoskeleton to form distinct radials, and differentiation of lepidotrichia distally (Grandel & Schulte-Merker, 1998). The myofibers of the pectoral fins appear early during the first phase of fin development, forming two simple muscle groups, an abductor and an adductor, each positioned on opposite sides of the endoskeletal disk (Fig. 12.3A,B). Like tetrapod limbs, the fin muscles of zebrafish derive from migratory somitic myoblasts (Neyt et al., 2000), and therefore, can be classified as abaxial using the terminology of Burke and Nowicki (2003). During the juvenile stage, the abductors and adductors increase in thickness and split to form superficial and deep groups (the abductor superficialis; abductor profundus; adductor superficialis and adductor profundus), plus two ventral arrectors (arrector ventralis, arrector 3) and one dorsal arrector (arrector dorsalis) along the leading margin of the fin (Thorsen & Hale, 2005; Siomava & Diogo, 2017) (Fig.12.3BeD). The pectoral fin muscles originate from the shoulder girdle and extend toward the fin rays. Whereas the arrectors insert exclusively on the first ray, the abductor profundus, adductor superficialis, and adductor profundus insert
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Pelvic Fin Muscles
FIGURE 12.3 Appendicular muscles. (A). Lateral view of a 5 dpf Tg(Acta1:EGFP) larvae. Muscle is green. (B,C). Confocal cross-sections through the pectoral fin of a 5 dpf larvae (B) and 8.9 mm juvenile (C) Tg(a-actin:EGFP) from Thorsen and Hale (2005:figs2 and 6). In larvae, the endoskeletal disk (ED) separates the abductor (ABD) and adductor (ADD) muscles. By 8.9 mm, the abductor superficialis (ABS), abductor profundus (ABP), and arrector ventralis (ARRV) are segmented. (D). Illustrated medial view of adult pectoral fin muscles modified from Diogo and Abdala (2007:fig8). (EeG). Pelvic fin muscles shown by fluorescence [Tg(Acta1:EGFP] (E) and gross dissection (FeG) in ventral (E,F) and dorsal (G) views. (F) and (G) are modified from Siomava and Diogo (2017:fig2) with pseudocoloring based on original tracings and personal communications (N.S.). ABPPLV, abductor profundus pelvicus; ABSPLV, abductor superficialis pelvicus; ADP, adductor profundus; ADPPLV, adductor profundus pelvicus; ADS, adductor superficialis; ADSPLV, adductor superficialis pelvicus; ARD, arrector dorsalis; ARDPLV, arrector dorsalis pelvicus; ARRV, arrector ventralis; ARVPLV, arrector ventralis pelvicus; cor, coracoid; EP, epaxialis; fr1, first fin ray; HYP, hypaxial muscle; mscora, mesocoracoid arch; PHY, posterior hypaxial muscle; PI, pit, protractor ischii and tendon; pplvg, posterior process pelvic girdle.
distally on all rays except the first (Siomava & Diogo, 2017). In addition to splitting, the majority of the muscles of the pectoral fin secondarily shift into the body wall, such that in adults, only a small portion remains within the fin. Pectoral nerves 1e4 (the spino-occipital nerve and spinal nerves 1e3) innervate the pectoral fin muscles (Thorsen & Hale, 2007). Based on studies of teleosts, the arrector ventralis is thought to initiate downstroke of the fin’s leading edge, which is further powered by the superficial and deep abductors. The arrector dorsalis contracts following peak down-stroke, and along with the superficial and deep adductors antagonize abduction to retract the fins (Thorsen & Hale, 2005). Notably, zebrafish are reported to possess a transient protractor pectoralis muscle connecting the skull and pectoral girdle. This muscle derives from the cardiopharyngeal field and is branchiomeric rather than intrinsically appendicular (Siomava & Diogo, 2017).
Pelvic Fin Muscles In zebrafish, the pelvic fins form approximately 4 weeks after initiation of the pectoral fins (and are present by 8 mm standard length) (Parichy, Elizondo, Mills, Gordon, & Engeszer, 2009). Two muscles anchor the pelvic girdle to the trunk. The protractor ischii extends from the cleithrum and ventral trunk myomeres on either side of the body, forming a single tendon that attaches to the posterior process of the pelvic girdle (Fig. 12.3E,F). Caudally, the retractor ischii extends from the pelvic girdle to the anal fin. Like the pectoral musculature, the muscles of the pelvic fin are organized into superficial and deep layers of abductors (abductor superficialis pelvicus and abductor profundus pelvicus) and adductors (adductor superficialis pelvicus and adductor profundus pelvicus) that extend to most rays, as well as arrectors (arrector ventralis pelvicus and arrector dorsalis pelvicus)
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that insert on the first ray (Siomava & Diogo, 2017) (Fig. 12.3F,G). Whereas pectoral myoblasts migrate long distances, pelvic myoblasts reach the base of the fin via direct epithelial extension before delaminating to form the dorsal and ventral muscle groups (Cole et al., 2011).
Median Fin Muscles Zebrafish have three median fins: the dorsal, anal, and caudal fins. The dorsal fin bears paired sets of inclinator, erector, and depressor dorsalis muscles arranged in series on either side of the fin blade (Fig.12.4A) (Schneider and Sulner, 2006; Siomava and Diogo, 2017). The erector and depressor muscles connect the proximal fin radials with the base of individual fin rays to raise and lower the fins, respectively. The inclinator muscles extend from the skin and epaxial musculature to the lateral edge of each ray to bend the fin sideways. In addition to the muscles described above, two longitudinal muscles, the protractor and the retractor dorsalis, raise and lower the fin, respectively. Muscles associated with the dorsal fin are innervated by a nerve plexus formed by the dorsal rami of spinal nerves between the ninth and 17th vertebrae (Schneider & Sulner, 2006). The musculature of the anal fin is similar to that of the dorsal fin (Siomava & Diogo, 2017). The musculature of the caudal fin consists of superficial and deep sets of muscles on either side of the lateral midline (Fig.12.4B,C). The superficial muscles include dorsal and ventral bodies of three primary groups, the lateralis profundus, lateralis superficialis, and the interfilamenti caudalis. The lateralis profundus dorsalis and ventralis extend from the caudal vertical myosepta and proximal caudal fin bones to the base of several dorsally and ventrally positioned fin rays (6e8 and 21e24, respectively) (Schneider & Sulner, 2006; Siomava & Diogo, 2017). The lateralis superficalis dorsalis and ventralis lie between the lateralis profundus muscles. These triangular muscles have a broad base of attachment along the lateral midline and narrow distally at their single ray insertion sites. The interfilamenti caudalis dorsalis and ventralis neighbor the lateralis superficialis. These muscles arise from a narrow base (along the proximal dorsomedial and ventromedial fin rays), and fan out to insert along several medially positioned rays (Siomava & Diogo, 2017). Notably, an interradialis caudalis primarily extends along the fifth ray and is unique to the dorsal side of the fin. Deeper within the caudal fin, a series of flexors (flexor caudalis dorsalis inferioris and ventralis inferioris; flexor caudalis dorsalis superioris and ventralis superioris) and an adductor (adductor caudalis ventralis) originate from the posterior-most vertebrae and proximal caudal fin bones and insert along the proximal caudal fin rays (Siomava & Diogo, 2017). The nerve roots
FIGURE 12.4
Median fin muscles. Left-lateral view of the muscles of the dorsal (A) and caudal (B,C) fins. (A). Dorsal fin illustration modified from Schneider and Sulner (2006:fig1a). Skin and axial muscles are removed. (B,C). Illustrations of superficial (A) and deep (B) caudal fin muscles modified from Schneider and Sulner (2006:fig6). In (C) the axial muscles and superficial caudal fin muscles have been removed. ACV, adductor caudalis ventralis; DPD, depressor dorsalis; EP, epaxialis; ERD, erector dorsalis; FCDI, flexor caudalis dorsalis inferioris; FCDS, flexor caudalis dorsalis superioris; FCVI, flexor caudalis ventralis inferior; FCVS, flexor caudalis ventralis superior; ICD, interfilamenti caudalis dorsalis; ICV, interfilamenti caudalis ventralis; IND, inclinator dorsalis; IRC, Interradialis caudalis; LPD, lateralis profundus dorsalis; LPV, lateralis profundus ventralis; LSD, lateralis superficialis dorsalis; LSV, lateralis superficialis ventralis; PROD, protractor dorsalis; RD, retractor dorsalis.
of spinal segments 27e31 innervate the muscles of the caudal fin (Schneider & Sulner, 2006).
Conclusions Zebrafish provide an excellent model for investigating the genetic basis of form and are particularly amenable to imaging morphogenesis in vivo. Moreover, as representative actinopterygians, zebrafish occupy a key phylogenetic position for anchoring comparisons with amniotes. Here, we have summarized aspects of
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References
zebrafish myology, including descriptions of the muscles of the head, trunk, and appendages. These descriptions, together with the excellent works by the authors summarized above, provide anatomical context for studies of muscle development, regeneration, physiology, disease modeling, and evolution.
References Bryson-Richardson, R. J., & Currie, P. D. (2008). The genetics of vertebrate myogenesis. Nature Reviews Genetics, 9, 632e646. Burke, A. C., & Nowicki, J. L. (2003). A new view of patterning domains in the vertebrate mesoderm. Developmental Cell, 4, 159e165. Cole, N. J., Hall, T. E., Don, E. K., Berger, S., Boisvert, C. A., Neyt, C., et al. (2011). Development and evolution of the muscles of the pelvic fin. PLoS Biology, 9(10), e1001168. Cubbage, C. C., & Mabee, P. M. (1996). Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). Journal of Morphology, 229, 121e160. Diogo, R., & Abdala, V. (2007). Comparative anatomy, homologies and evolution of the pectoral muscles of bony fish and tetrapods: A new insight. Journal of Morphology, 268, 504e517. Diogo, R., Hinits, Y., & Hughes, S. M. (2008). Development of mandibular, hyoid and hypobranchial muscles in the zebrafish: Homologies and evolution of these muscles within bony fishes and tetrapods. BMC Developmental Biology, 8, 24. https://doi.org/ 10.1186/1471-213X-8-24. Easter, S. S., & Nicola, G. N. (1996). The development of vision in the zebrafish (Danio rerio). Developmental Biology, 180, 646e663. Grandel, H., & Schulte-Merker, S. (1998). The development of the paired fins in the zebrafish (Danio rerio). Mechanisms of Development, 79, 99e120. Haines, L., Neyt, C., Gautier, P., Keenan, D. G., BrysonRichardson, R. J., Hollway, G. E., et al. (2004). Met and Hgf signaling controls hypaxial muscle and lateral line development in the zebrafish. Development, 131, 4857e4869. Hernandez, L. P., Barresi, M. J. F., & Devoto, S. H. (2002). Functional morphology and developmental biology of zebrafish: Reciprocal illumination from an unlikely couple. Integrative and Comparative Biology, 42, 222e231. Hernandez, L. P., Patterson, S. E., & Devoto, S. H. (2005). The development of muscle fiber type identity in zebrafish cranial muscles. Anatomy and Embryology, 209, 323e334.
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Kasprick, D. S., Kish, P. E., Junttila, T. L., Ward, L. A., Bohnsack, B. L., & Kahana, A. (2011). Microanatomy of adult zebrafish extraocular muscles. PLoS One, 6, e27095. Lours-Calet, C., Alvares, L. E., El-Hanfy, A. S., Gandesha, S., Walters, E. H., Sobreira, D. R., et al. (2014). Evolutionarily conserved morphogenetic movements at the vertebrate head-trunk interface coordinate the transport and assembly of hypopharyngeal structures. Developmental Biology, 390, 231e246. Minchin, J. E. N., Williams, V. C., Hinits, Y., Low, S., Tandon, P., Fan, C. M., et al. (2013). Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion. Development, 140, 2972e2984. Neyt, C., Jagla, K., Thisse, C., Thisse, B., Haines, L., & Currie, P. D. (2000). Evolutionary origins of vertebrate appendicular muscle. Nature, 408, 82e86. Parichy, D. M., Elizondo, M. R., Mills, M. G., Gordon, T. N., & Engeszer, R. E. (2009). Normal table of post-embryonic zebrafish development: Staging by externally visible anatomy of the living fish. Developmental Dynamics, 238, 2975e3015. Schilling, T. F., & Kimmel, C. B. (1997). Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development, 124, 2945e2960. Schneider, H., & Sulner, B. (2006). Innervation of dorsal and caudal fin muscles in adult zebrafish Danio rerio. Journal of Comparative Neurology, 497, 702e716. Siomava, N., & Diogo, R. (2017). Comparative anatomy of zebrafish paired and median fin muscles: Basis for functional, developmental, and macroevolutionary studies. Journal of Anatomy. https://doi.org/10.1111/joa.12728. Stellabotte, F., & Devoto, S. H. (2007). The teleost dermomyotome. Developmental Dynamics, 236, 2432e2443. Thorsen, D. H., & Hale, M. E. (2005). Development of zebrafish (Danio rerio) pectoral fin musculature. Journal of Morphology, 266, 241e255. Thorsen, D. H., & Hale, M. E. (2007). Neural development of the zebrafish (Danio rerio) pectoral fin. Journal of Comparative Neurology, 504, 168e184. Windner, S. E., Steinbacher, P., Obermayer, A., Kasiba, B., ZweimuellerMayer, J., & Stoiber, W. (2011). Distinct modes of vertebrate hypaxial muscle formation contribute to the teleost body wall musculature. Development Genes and Evolution, 221, 167e178. Winterbottom, R. (1974). A descriptive synonymy of the striated muscles of the Teleostei. Proceedings of the Academy of Natural Sciences of Philadelphia, 125, 225e317.
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12 Zebrafish Myology Frank J. Tulenko, Peter Currie Australian Regenerative Medicine Institute, Monash University, Clayton, VIC, Australia
Embryonic Origins
Head Muscles
The myofibers that comprise skeletal muscle can vary in their embryonic origin, molecular patterning, and physiology, depending on the location and function. Most craniofacial muscles develop from unsegmented head mesoderm using genetic programs distinct from trunk myomeres, which form from postcranial spheres of cells termed somites (Bryson-Richardson & Currie, 2008). Both head and trunk muscles contain physiologically distinct fast and slow myofibers, the proportions of which can change over time (Hernandez, Patterson, & Devoto, 2005). Slow-twitch muscle fibers are fatigue resistant, metabolically oxidative, heavily vascularized, and are the first fiber type to arise in zebrafish. Fast-twitch fibers function in rapid, powerful actions and are metabolically glycolytic. Studies of postcranial myogenesis have shown that during development, fast and slow fiber types segregate through complex cellular movements within each somite. Slow myofibers arise along the midline and migrate laterally to a superficial position along the myotome. Fast myofibers, in contrast, form from two distinct intrasomitic populations. Cells of the posterior somite differentiate into fast myofibers, whereas cells of the anterior somitic border migrate laterally to form a thin monolayer superficial to the slow fibers. These “external cells” then secondarily ingress between slow myofibers to form additional fast fibers (Bryson-Richardson & Currie, 2008; Stellabotte & Devoto, 2007). Ultimately, the slow muscle fibers form a wedgelike stripe that is positioned lateral to the horizontal septum, running outside and parallel to the fast fibers, which comprise the bulk of the trunk musculature.
The Zebrafish in Biomedical Research https://doi.org/10.1016/B978-0-12-812431-4.00012-9
Extraocular Muscles Similar to other vertebrates, zebrafish rotate their eyes using six extraocular muscles: the superior and inferior obliques, and the medial, lateral, superior, and inferior rectus muscles all of which form by around 72 hpf (Easter & Nicola, 1996) (Fig. 12.1). In 96 hpf fish, both the superior and inferior obliques originate along the rostral orbit and insert on the dorsal and ventral surfaces of the eye, respectively. The superior, inferior, and medial rectus muscles arise from a similar site along the posterior orbit. Whereas the superior and inferior rectus insert just caudal to the superior and inferior obliques, the medial rectus extends between the obliques, inserting on the anteromedial surface of the eye. Unlike the other rectus muscles, the lateral rectus originates outside of the orbit posterior to the diencephalon and inserts on the posterior sclera (Kasprick et al., 2011). Notably, the insertion sites of the superior oblique and rectus muscles overlap in adults (Fig. 12.1B). A similar late overlap has been shown for the inferior oblique and rectus (Kasprick et al., 2011) (Fig. 12.1C). Three cranial nerves (CN) innervate the extraocular muscles: CNIII innervates the inferior oblique, superior rectus, inferior rectus, and medial rectus; CNIV innervates the superior oblique; and CNVI innervates the lateral rectus (Schilling & Kimmel, 1997). Interestingly, a visually evoked startle response develops about 20 h later than the touch startle response, roughly coincident with early maturation of the extraocular muscles (Easter & Nicola, 1996).
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FIGURE 12.1 Extraocular muscles. (A). Ventral view of the six extraocular muscles of a 96 hpf larvae (modified from the camera lucida drawing of Easter and Nicola, 1996:fig11). Dashed lines indicate deeper structures. (B,C). Adult transgenic [Tg(a-actin:EGFP)] with muscle GFP (Kasprick et al., 2011:fig2). Arrowhead marks muscle overlap. ant, anterior; dors, dorsal; IO, inferior oblique; IR, inferior rectus; LR, lateral rectus; MR, medial rectus; post, posterior; SO, superior oblique; SR, superior rectus; vent, ventral.
Arch-associated Muscles In jawed vertebrates, craniofacial muscles develop in association with segmentally arranged arches surrounding the pharynx, an embryological feature reflected in adult patterns of innervation. Zebrafish possess seven pairs of pharyngeal arches: anterior-to-posterior, these are the mandibular arch, hyoid arch, and five gillassociated branchial arches, each with distinct skeletal elements and muscles (Cubbage & Mabee, 1996; Schilling & Kimmel, 1997). Mandibular Arch Muscles Muscles associated with the first arch (mandibular arch) include the intermandibularis, adductor mandibulae, and a dorsal group consisting of the levator arcus palatini and dilatator operculi, all of which are innervated by CNV (Fig.12.2) (Schilling & Kimmel, 1997). The intermandibularis anterior joins the left and right dentary bones (mandible) and remains largely unchanged between larval and adult stages. The intermandibularis posterior becomes associated with the interhyoideus (a second arch muscle) in larvae (Fig.12.2B), forming a continuous muscle, the protractor hyoideus. In adults, the protractor hyoideus is longitudinally split into dorsal and ventral portions connecting the anterior ceratohyal and ventral hypohyal bones with the dentary (Fig.12.2D) (Diogo, Hinits, & Hughes, 2008). The protractor hyoideus depresses the mandible and is innervated by both CNV and VII, reflecting its complex ontogeny (Diogo et al., 2008).
In early larvae, the adductor mandibulae initiate as a single mass (Fig.12.2A,B), but in adults subdivides into four bundles: A0, A1, A2, and Au (Fig.12.2B) (Diogo et al. 2008). Collectively, A0, A1, and A2 primarily extend below the eye, connecting the preopercle (A0, A1, A2), quadrate (A0, A1), hyomandibula (A2), and metapterygoid (A2) with the mandible and maxilla (Diogo et al., 2008). Au originates along the medial surface of the mandible (angulo-articular and dentary) and inserts on the tendon of A2. Whereas the adductor mandibulae complex primarily closes the mouth, the maxillary component (specific to A0) functions in mouth protrusion (Diogo et al., 2008). Larval zebrafish possess a single dorsal mandibular premuscle mass, which segments to form the levator arcus palatini and the dilatator operculi in adults (Fig.12.2A,C) (Schilling & Kimmel, 1997). The levator arcus palatini originates along the sphenotic bone of the neurocranium and extends to the metapterygoid and hyomandibula to abduct/elevate the jaw suspensorium. The dilatator operculi neighbors the levator arcus palatini and lies superficial to the adductor hyomandibulae (a second arch muscle), joining the frontal and pterotic bones, hyomandibula, and opercle for opercular abduction (Diogo et al., 2008). Hyoid Arch Muscles Muscles associated with the second arch, the hyoid arch, include the interhyoideus, hyohyoideus, adductor hyomandibulae, adductor operculi, levator operculi, and adductor arcus palatini, all innervated by cranial nerve VII (Schilling & Kimmel, 1997; Diogo et al., 2008) (Fig.12.2). As mentioned above, the interhyoideus together with the intermandibularis posterior comprises the protractor hyoideus. By 4 dpf, the hyohyoideus consists of a wellformed hyohyoideus inferior, as well as posterior myofibers [hyohyoideus superior: Diogo et al. (2008)] that segregate to form the hyohyoideus abductor and adductors following ossification of the branchiostegal rays (Fig.12.2). In adults, the hyohyoideus inferior and abductor originate from the anterior ceratohyals and first branchiostegal ray, respectively, and meet their opposite partner along the jaw medial aponeurosis. The medialmost branchiostegal ray separates the hyohyoideus abductor from the laterally positioned adductors, which extend between the branchiostegal rays, opercle and subopercle. The hyohyoideus abductor and adductors expand and constrict the branchiostegal membranes, respectively (Diogo et al., 2008). The adductor operculi extends from the pterotic bone to the opercle for opercular adduction. The levator operculi originates along the ventrolateral margin of the pterotic, runs lateral to the adductor operculi, and inserts on the
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FIGURE 12.2 Cephalic muscles. Arch associated muscles in larval (A,B) and adult (C,D) zebrafish in lateral (A,C) and ventral (B,D) view. (A,B). Confocal maximum projections of 4 dpf Tg(Acta1:EGFP) larvae. Skeletal muscle is green. (C,D). Adult illustrations modified from Diogo et al (2008:fig5). In (D), part of the hyohyoideus adductors (HHAD), as well as the opercle (op), interopercle (iop), subopercle (sop), and preopercle (pop) are removed from the right side. A0, A1, A2, bodies of the adductor mandibulae (ADM); ABD, fin abductor; ABS, abductor superficialis; ADAP, adductor arcus palatini; ADS, adductor superficialis; AH, adductor hyomandibulae; angart, anguloarticular; AOP, adductor operculi; ARRV, arrector ventralis; BL5, fifth branchial levator; brI, branchiostegal ray I; cha, anterior ceratohyal; chp, posterior ceratohyal; cl, cleithrum; den, dentary; DPW, dorsal pharyngeal wall muscle; DOP, dilatator operculi; en, entopterygoid; EP, epaxialis; f, frontal; fr, fin rays; hh, ventral hypohyal; HHAB, hyohyoideus abductor; HHI, hyohyoideus inferior; HYP, hypaxial muscle; INTMA, intermandibularis anterior; LAP, levator arcus palatini; LOP, levator operculi; mnd, mandible; mx, maxilla; osph, orbitosphenoid; pa-exs, parieto-extrascapular; para, parasphenoid; post, posttemporal; PRD, dorsal protractor hyoideus; prmx, premaxilla; PRV, ventral protractor hyoideus; pt, pterotic; rmb, medial branch ramus mandibularis; scl, supracleithrum; SH, sternohyoideus; sph, sphenotic; TV, transversalis ventralis.
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opercle (Fig.12.2C). In zebrafish, as in other teleosts, the levator operculi is thought to function through the opercular series and the interoperculo-mandibular ligament in lower jaw depression (Diogo et al., 2008). The adductor hyomandibulae extends from the neurocranium to the medial margin of the hyomandibula. The adductor arcus palatini extends from the neurocranium to the hyomandibula, metapterygoid, and entopterygoid, antagonizing the function of the levator arcus palatini by adducting the jaw suspensorium (Diogo et al. 2008). Posterior Branchial Arch Muscles At 96 hpf, the muscles associated with the posterior branchial arches include the dorsal pharyngeal wall muscles [branchial levatores: Hernandez et al. (2005)], rectus ventralis, transversus ventralis, and rectus communis [Schilling & Kimmel, 1997; see also Winterbottom (1974) for review] (Fig.12.2A,B). The dorsal pharyngeal wall muscles are positioned between the dorsal branchial cartilages and neurocranium (Hernandez et al., 2005). In both larvae and adults, the anterior-most levatores are relatively small, whereas the fifth is larger for its role in feeding and consists exclusively of fast fibers (Hernandez et al., 2005). The transversus ventralis muscles function in respiration and extend from the ceratobranchials to the median raphe of the ventral midline (Schilling & Kimmel, 1997). The rectus ventralis muscles are positioned between the aforementioned branchial arch muscles, joining adjacent ceratobranchials. In contrast, the rectus communis forms a band that extends across the third through fifth branchial arches (Schilling & Kimmel, 1997). Branches of CNIX and X innervate the muscles of the posterior branchial arches (Schilling & Kimmel, 1997). Hypobranchial Muscles Zebrafish possess a single hypobranchial muscle, the sternohyoideus. Unlike the cranial mesoderm-derived pharyngeal muscles described above, the sternohyoideus arises from postcranial somitic mesoderm that becomes secondarily anteriorized during development, a process likely mediated by the growth dynamics of the circumpharyngeal tissues (Lours-Calet et al., 2014). Interestingly, the anterior somites that give rise to the sternohyoideus also contribute striated myofibers to the esophagus for ingestion (Minchin et al., 2013). Whereas the sternohyoideus muscles are paired in larvae (Fig.12.2A,B), they form a single sheet in adults, extending from the cleithrum to the urohyal (Fig.12.2C,D). Anterior branches of the occipito-spinal nerves innervate the sternohyoideus, which functions in hyoid depression, suspensorium abduction, and mouth opening (Diogo et al., 2008).
Trunk Muscles The trunk musculature of zebrafish consists of approximately 32 muscle blocks (myomeres), which reflect somitic segmentation. Vertical connective tissue myosepta separate the myomeres and transmit their contractions to the skeleton for locomotion. In addition to vertical myosepta, zebrafish possess horizontal myosepta that split each myomere into dorsal epaxial and ventral hypaxial regions (Figs.12.2C and 12.3A). In adult teleosts, the epaxial myomeres collectively comprise the epaxialis muscle (Fig.12.2C). In addition to the epaxial and hypaxial myomeres, a transient muscle, the hypaxialis posterior, contributes to the ventral body wall of early larvae (Fig. 12.3A) and is thought to function with the sternohyoideus in suction feeding (Hernandez, Barresi, & Devoto, 2002). The hypaxialis posterior arises using a developmental program similar to the appendicular muscles (Haines et al., 2004), and in adult pearlfish, it is incorporated into the obliquus inferior (hypaxial body wall muscle) (Windner et al., 2011).
Pectoral Fin Muscles In zebrafish, the pectoral fins develop in two continuous phases. The first starts with the onset of fin bud outgrowth around 26 hpf and is marked by the formation of a fin skeleton consisting of an endoskeletal disc proximally and actinotrichia distally. The second phase begins during the third week of development and involves fin rotation, remodeling of the endoskeleton to form distinct radials, and differentiation of lepidotrichia distally (Grandel & Schulte-Merker, 1998). The myofibers of the pectoral fins appear early during the first phase of fin development, forming two simple muscle groups, an abductor and an adductor, each positioned on opposite sides of the endoskeletal disk (Fig. 12.3A,B). Like tetrapod limbs, the fin muscles of zebrafish derive from migratory somitic myoblasts (Neyt et al., 2000), and therefore, can be classified as abaxial using the terminology of Burke and Nowicki (2003). During the juvenile stage, the abductors and adductors increase in thickness and split to form superficial and deep groups (the abductor superficialis; abductor profundus; adductor superficialis and adductor profundus), plus two ventral arrectors (arrector ventralis, arrector 3) and one dorsal arrector (arrector dorsalis) along the leading margin of the fin (Thorsen & Hale, 2005; Siomava & Diogo, 2017) (Fig.12.3BeD). The pectoral fin muscles originate from the shoulder girdle and extend toward the fin rays. Whereas the arrectors insert exclusively on the first ray, the abductor profundus, adductor superficialis, and adductor profundus insert
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Pelvic Fin Muscles
FIGURE 12.3 Appendicular muscles. (A). Lateral view of a 5 dpf Tg(Acta1:EGFP) larvae. Muscle is green. (B,C). Confocal cross-sections through the pectoral fin of a 5 dpf larvae (B) and 8.9 mm juvenile (C) Tg(a-actin:EGFP) from Thorsen and Hale (2005:figs2 and 6). In larvae, the endoskeletal disk (ED) separates the abductor (ABD) and adductor (ADD) muscles. By 8.9 mm, the abductor superficialis (ABS), abductor profundus (ABP), and arrector ventralis (ARRV) are segmented. (D). Illustrated medial view of adult pectoral fin muscles modified from Diogo and Abdala (2007:fig8). (EeG). Pelvic fin muscles shown by fluorescence [Tg(Acta1:EGFP] (E) and gross dissection (FeG) in ventral (E,F) and dorsal (G) views. (F) and (G) are modified from Siomava and Diogo (2017:fig2) with pseudocoloring based on original tracings and personal communications (N.S.). ABPPLV, abductor profundus pelvicus; ABSPLV, abductor superficialis pelvicus; ADP, adductor profundus; ADPPLV, adductor profundus pelvicus; ADS, adductor superficialis; ADSPLV, adductor superficialis pelvicus; ARD, arrector dorsalis; ARDPLV, arrector dorsalis pelvicus; ARRV, arrector ventralis; ARVPLV, arrector ventralis pelvicus; cor, coracoid; EP, epaxialis; fr1, first fin ray; HYP, hypaxial muscle; mscora, mesocoracoid arch; PHY, posterior hypaxial muscle; PI, pit, protractor ischii and tendon; pplvg, posterior process pelvic girdle.
distally on all rays except the first (Siomava & Diogo, 2017). In addition to splitting, the majority of the muscles of the pectoral fin secondarily shift into the body wall, such that in adults, only a small portion remains within the fin. Pectoral nerves 1e4 (the spino-occipital nerve and spinal nerves 1e3) innervate the pectoral fin muscles (Thorsen & Hale, 2007). Based on studies of teleosts, the arrector ventralis is thought to initiate downstroke of the fin’s leading edge, which is further powered by the superficial and deep abductors. The arrector dorsalis contracts following peak down-stroke, and along with the superficial and deep adductors antagonize abduction to retract the fins (Thorsen & Hale, 2005). Notably, zebrafish are reported to possess a transient protractor pectoralis muscle connecting the skull and pectoral girdle. This muscle derives from the cardiopharyngeal field and is branchiomeric rather than intrinsically appendicular (Siomava & Diogo, 2017).
Pelvic Fin Muscles In zebrafish, the pelvic fins form approximately 4 weeks after initiation of the pectoral fins (and are present by 8 mm standard length) (Parichy, Elizondo, Mills, Gordon, & Engeszer, 2009). Two muscles anchor the pelvic girdle to the trunk. The protractor ischii extends from the cleithrum and ventral trunk myomeres on either side of the body, forming a single tendon that attaches to the posterior process of the pelvic girdle (Fig. 12.3E,F). Caudally, the retractor ischii extends from the pelvic girdle to the anal fin. Like the pectoral musculature, the muscles of the pelvic fin are organized into superficial and deep layers of abductors (abductor superficialis pelvicus and abductor profundus pelvicus) and adductors (adductor superficialis pelvicus and adductor profundus pelvicus) that extend to most rays, as well as arrectors (arrector ventralis pelvicus and arrector dorsalis pelvicus)
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that insert on the first ray (Siomava & Diogo, 2017) (Fig. 12.3F,G). Whereas pectoral myoblasts migrate long distances, pelvic myoblasts reach the base of the fin via direct epithelial extension before delaminating to form the dorsal and ventral muscle groups (Cole et al., 2011).
Median Fin Muscles Zebrafish have three median fins: the dorsal, anal, and caudal fins. The dorsal fin bears paired sets of inclinator, erector, and depressor dorsalis muscles arranged in series on either side of the fin blade (Fig.12.4A) (Schneider and Sulner, 2006; Siomava and Diogo, 2017). The erector and depressor muscles connect the proximal fin radials with the base of individual fin rays to raise and lower the fins, respectively. The inclinator muscles extend from the skin and epaxial musculature to the lateral edge of each ray to bend the fin sideways. In addition to the muscles described above, two longitudinal muscles, the protractor and the retractor dorsalis, raise and lower the fin, respectively. Muscles associated with the dorsal fin are innervated by a nerve plexus formed by the dorsal rami of spinal nerves between the ninth and 17th vertebrae (Schneider & Sulner, 2006). The musculature of the anal fin is similar to that of the dorsal fin (Siomava & Diogo, 2017). The musculature of the caudal fin consists of superficial and deep sets of muscles on either side of the lateral midline (Fig.12.4B,C). The superficial muscles include dorsal and ventral bodies of three primary groups, the lateralis profundus, lateralis superficialis, and the interfilamenti caudalis. The lateralis profundus dorsalis and ventralis extend from the caudal vertical myosepta and proximal caudal fin bones to the base of several dorsally and ventrally positioned fin rays (6e8 and 21e24, respectively) (Schneider & Sulner, 2006; Siomava & Diogo, 2017). The lateralis superficalis dorsalis and ventralis lie between the lateralis profundus muscles. These triangular muscles have a broad base of attachment along the lateral midline and narrow distally at their single ray insertion sites. The interfilamenti caudalis dorsalis and ventralis neighbor the lateralis superficialis. These muscles arise from a narrow base (along the proximal dorsomedial and ventromedial fin rays), and fan out to insert along several medially positioned rays (Siomava & Diogo, 2017). Notably, an interradialis caudalis primarily extends along the fifth ray and is unique to the dorsal side of the fin. Deeper within the caudal fin, a series of flexors (flexor caudalis dorsalis inferioris and ventralis inferioris; flexor caudalis dorsalis superioris and ventralis superioris) and an adductor (adductor caudalis ventralis) originate from the posterior-most vertebrae and proximal caudal fin bones and insert along the proximal caudal fin rays (Siomava & Diogo, 2017). The nerve roots
FIGURE 12.4
Median fin muscles. Left-lateral view of the muscles of the dorsal (A) and caudal (B,C) fins. (A). Dorsal fin illustration modified from Schneider and Sulner (2006:fig1a). Skin and axial muscles are removed. (B,C). Illustrations of superficial (A) and deep (B) caudal fin muscles modified from Schneider and Sulner (2006:fig6). In (C) the axial muscles and superficial caudal fin muscles have been removed. ACV, adductor caudalis ventralis; DPD, depressor dorsalis; EP, epaxialis; ERD, erector dorsalis; FCDI, flexor caudalis dorsalis inferioris; FCDS, flexor caudalis dorsalis superioris; FCVI, flexor caudalis ventralis inferior; FCVS, flexor caudalis ventralis superior; ICD, interfilamenti caudalis dorsalis; ICV, interfilamenti caudalis ventralis; IND, inclinator dorsalis; IRC, Interradialis caudalis; LPD, lateralis profundus dorsalis; LPV, lateralis profundus ventralis; LSD, lateralis superficialis dorsalis; LSV, lateralis superficialis ventralis; PROD, protractor dorsalis; RD, retractor dorsalis.
of spinal segments 27e31 innervate the muscles of the caudal fin (Schneider & Sulner, 2006).
Conclusions Zebrafish provide an excellent model for investigating the genetic basis of form and are particularly amenable to imaging morphogenesis in vivo. Moreover, as representative actinopterygians, zebrafish occupy a key phylogenetic position for anchoring comparisons with amniotes. Here, we have summarized aspects of
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References
zebrafish myology, including descriptions of the muscles of the head, trunk, and appendages. These descriptions, together with the excellent works by the authors summarized above, provide anatomical context for studies of muscle development, regeneration, physiology, disease modeling, and evolution.
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