Ontogeny of architectural complexity in embryonic quail visceral arch muscles

Abstract

Understanding the mechanisms of muscle pattern formation requires that the complete sequence of ontogenetic events be defined, particularly in the emergence of architectural complexity and in the spatial relations between muscles and skeletal elements. This analysis of visceral arch myogenesis in quail (Coturnix coturnix japonica) embryos identifies the location of premuscle condensations and subsequent segregation of individual muscles, documents the initial orientation of myofibers and changes in alignment associated with maturation, and describes the spatial and temporal relations between muscle development and the formation of connective tissues. Premuscle condensations form within the visceral arches on embryonic days 2-4, before skeletal elements make their appearance. Discrete muscles may form from the subdivision of a muscle mass after fiber orientations have been established (e.g., jaw adductor and hyobranchial muscles) or by the segregation of a mesenchymal cluster from the condensation prior to the appearance of oriented fibers (e.g., protractor, muscle of the columella). The rate and pattern of subsequent muscle maturation are closely associated with the development of the hard tissues. Myogenesis in 4-9-day embryos centers around the quadrate cartilage, the retroarticular process of the mandibular (Meckel's) cartilage, and the epibranchial cartilage. Muscles form attachments on these elements and remain without additional attachments until the appropriate elements (e.g., otic capsule, pterygoid bone) develop. No single description of myogenic events applies to all visceral arch muscles, nor is there an arch-specific pattern of ontogeny. Rather, each muscle has distinctive characteristics based on its spatial relations within the developing head.

Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells

“…Previous mapping and gene expression studies have shown that skeletal muscle progenitors form aggregates at or close to their sites of origin within paraxial mesoderm (Noden, 1983b;McClearn and Noden, 1988;Noden et al, 1999). Retroviral injections confirm that progenitors of extraocular muscles first condense, then move as cohorts toward the mesoderm:crest interface, and subsequently enter the crest-derived periocular environment.…”

“…Skeletal muscle fibers, including those within head muscles, are known to develop in two temporally distinct waves, with primary myotubes forming first and acting as scaffolds for later forming secondary myotubes (McClearn and Noden, 1988;Wigmore and Evans, 2002). During our investigation, both primary and secondary myotubes in individual muscles were labeled, indicating that the precursors of these different myotubes arise from the same or overlapping progenitor populations.…”

“…Once established, this partnership with connective tissue primordia is maintained during subsequent stages of muscle individuation, segregation, and the formation of attachments (McClearn and Noden, 1988). Descriptive accounts in avian (Köntges and Lumsden, 1996;Noden and Francis-West, 2006) and mammalian (Matsuoka et al, 2005) embryos indicate that crestmuscle associations are often maintained even when muscles move out of the immediate branchial region.…”

“…During formation of branchial arches, for example, crest cells initially located superficial to mesoderm move inward, circumscribing the muscle primordia (Trainor and Tam, 1994;Trainor et al, 1994;Kimmel et al, 2001). Within the arches, myogenic cells remain segregated until later stages, when crest cells penetrate differentiating muscles to establish endo-, peri-, and epimysial layers (Noden, 1983a;McClearn and Noden, 1988;Trainor and Tam, 1995;Noden and Francis-West, 2006). Köntges and colleagues (Könt-ges and Lumsden, 1996;Matsuoka et al, 2005) have shown that, at later stages, the crest-derived progenitors of connective tissues associated with some branchial muscles will distort the original crest:mesoderm interface to reach distant attachment sites.…”

Developmental relations between sixth nerve motor neurons and their targets in the chick embryo

“…All embryos were fixed prior to the emergence of secondary myocytes (McClearn and Noden, 1988). Labeled angioblasts, identified by their broad dispersal patterns and frequent incorporation into blood vessel walls (Fig.…”