Abstract
The vertebrate spinal accessory nerve (SAN) innervates the cucullaris muscle, the major muscle of the neck, and is recognized as a synapomorphy that defines living jawed vertebrates. Morphologically, the cucullaris muscle exists between the branchiomeric series of muscles innervated by special visceral efferent neurons and the rostral somitic muscles innervated by general somatic efferent neurons. The category to which the SAN belongs to both developmentally and evolutionarily has long been controversial. To clarify this, we assessed the innervation and cytoarchitecture of the spinal nerve plexus in the lamprey and reviewed studies of SAN in various species of vertebrates and their embryos. We then reconstructed an evolutionary sequence in which phylogenetic changes in developmental neuronal patterning led towards the gnathostome-specific SAN. We hypothesize that the SAN arose as part of a lamprey-like spinal nerve plexus that innervates the cyclostome-type infraoptic muscle, a candidate cucullaris precursor.
Highlights
The head of the embryonic vertebrate has a mesodermal component that consists of pharyngeal arch mesoderm ventrally and paraxial head mesoderm dorsally, giving rise to the branchial muscles and somatic muscles, respectively
The paraxial part of the head mesoderm differentiates into extrinsic eye muscles innervated by cranial nerves III, IV, and VI (Figure 1B), which are classified as general somatic efferent (GSE) nerves, as are the spinal nerves in the trunk, which is defined as the domain that develops segmented somitic mesoderm from which myotomes will arise
The current review focuses on the evolution of the spinal accessory nerve (SAN) and in particular on the question of whether it belongs to special visceral efferent (SVE), GSE or another category of efferent nerves in the comparative anatomical, embryological, and evolutionary developmental contexts
Summary
The head of the embryonic vertebrate has a mesodermal component that consists of pharyngeal arch (visceral) mesoderm ventrally and paraxial (somatic) head mesoderm dorsally, giving rise to the branchial muscles and somatic muscles, respectively (reviewed by [1]). Extrapolating from this, it is plausible that the lamprey SNP corresponds to the position expected for the hypothetical ancestral SAN, thereby suggesting that the SAN was ancestrally positioned at the levels of the Xth and XIIth nuclei (Figure 3) This speculation is consistent with the evidence that the gnathostome SAN has many somatic spinal nerve cytoarchitectural features, and as Sperry and Boord [35] have described, the SNP is located in the rostral spinal cord, unrelated to any of the components of the vagus or the branchial arches. The GSE axonal pattern depends on its specific developmental mechanism because the cervical spinal motor neurons have SAN-like morphological properties, as seen in the phenotype of the mouse lacking the Lim-HD–family genes Lhx and Lhx4 [89].
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