Epimere versus Hypomere and the Development of Striated Muscles in the Head

To appreciate the resolution of the problem of head musculature and its innervation, one must consider it in the context of the pattern of development of the muscular components of the body. The body is essentially a tube with three layers—an outer layer of ectoderm that forms the central nervous system, the neural crest, the epidermis, and other tissues; an inner layer of endoderm that forms the lining of the gut and related organs; and an intermediate layer ofmesoderm that forms the bones, muscles, blood vessels, dermis, and other structures of the body. The mesoderm has three dorsal-to-ventral components. The epimere (or paraxial mesoderm), the most dorsal component, forms somites, which are segmental mesodermal masses that give rise to the striated, skeletal muscles of the body wall and the limbs. The intermediate component, mesomere (or nephric ridge), gives rise to the kidneys and gonads, whereas the ventral component, hypomere (or lateral plate mesoderm), gives rise to the smooth, visceral muscles of the gut as well as to the cardiac muscle of the heart.

In the head, the embryological derivation of the various groups of muscles was until recently incorrectly understood, particularly concerning the phar-yngeal region. In addition to giving rise to multiple components of the peripheral nervous system and to most of the skull, neural crest cells give rise to mesenchymal tissue that forms the so-called "visceral" arches of the pharynx. The muscles of this region were long thought to arise from a rostral continuation of hypomeric muscle—the ventral part of the mesoder-mal tissue that in the body gives rise to the smooth muscle of the gut. Muscles derived from the visceral arch region, which in mammals are the muscles of the mandibular arch (lower jaw muscles innervated by the trigeminal nerve), hyoid arch (facial and other muscles innervated by the facial nerve), and the several branchial arches (throat and larynx muscles innervated by the glossopharyngeal and vagus nerves), were thus presumed to be visceral muscles. In conflict with this view was the resemblance of the visceral arch muscles to the striated, skeletal muscle of the body wall and of the tongue and extraocular muscles. The histological structure of the visceral arch muscles and their single-motor neuron innervation pattern are both markedly different from the histological structure and two-neuron chain, parasympathetic innervation pattern of the smooth muscle of the gut. The designation of "special" acknowledged these differences.

Recent work by Gilland, Noden, Northcutt, and others has revealed a different embryological source for the muscles of the visceral arches and has resolved the previous confusion. Rather than being derived from hypomere, the muscles of the visceral arches are in fact derived from the epimeric muscle of the head, the caudal continuation of which gives rise to the striated, skeletal muscles of the body wall. Somites and somitomeres, which are incompletely separated somites, form in the head region and give rise to the extraocular muscles, the muscles of the visceral arches, and the muscles of the tongue. Thus, none of the visceral arch muscles are actually visceral, and there is nothing special about them. They are embryologically derived and innervated in the same manner (by neural tube-derived motor neurons) as the extraocular and tongue muscles. The visceral arch muscles probably evolved before the extraocular muscles were acquired by early vertebrates, however, and long before the muscular tongue was gained by tetrapods, and this difference in history may account for the different position within the brain stem of the two columns of motor neurons that innervate them.

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