The sensory peripheral nervous system in the tail of a cephalochordate studied by serial blockface scanning electron microscopy

Abstract

Serial blockface scanning electron microscopy (SBSEM) is used to describe the sensory peripheral nervous system (PNS) in the tail of a cephalochordate, Asymmetron lucayanum. The reconstructed region extends from the tail tip to the origin of the most posterior peripheral nerves from the dorsal nerve cord. As peripheral nerves ramify within the dermis, all the nuclei along their course belong to glial cells. Invaginations in the glial cell cytoplasm house the neurites, an association reminiscent of the nonmyelinated Schwann cells of vertebrates. Peripheral nerves pass from the dermis to the epidermis via small fenestrae in the sub-epidermal collagen fibril layer; most nerves exit abruptly, but a few run obliquely within the collagen fibril layer for many micrometers before exiting. Within the epidermis, each nerve begins ramifying repeatedly, but the branches are too small to be followed to their tips with SBSEM at low magnification (previous studies on other cephalochordates indicate that the branches end freely or in association with epidermal sensory cells). In Asymmetron, two morphological kinds of sensory cells are scattered in the epidermis, usually singly, but sometimes in pairs, evidently the recent progeny of a single precursor cell. The discussion considers the evolution of the sensory PNS in the phylum Chordata. In cephalochordates, Retzius bipolar neurons with intramedullary perikarya likely correspond to the Rohon-Beard cells of vertebrates. However, extramedullary neurons originating from ventral epidermis in cephalochordates (and presumably in ancestral chordates) contrast with vertebrate sensory neurons, which arise from placodes and neural crest.

Tail regeneration in a cephalochordate, the Bahamas lancelet,Asymmetron lucayanum

“…In Asymmetron lucayanum (Figure 1), the body region posterior to the anus is the tail, which narrows to a slender caudal process posteriorly (Figure 2). Like the rest of the body, the tail is covered by a single‐layered epidermis consisting mostly of non‐ciliated cuboidal cells and a few ciliated sensory cells (Holland & Somorjai, 2020a). Frontal sections through the tail region (Figures 3–5) show the central nervous system (CNS).…”

“…Toward the posterior of the CNS, the nerve cell bodies and neurites drop out, leaving only the ependymal cells in the wall of the neural tube, which curls ventrally around the tip of the notochord and then terminates (at CNS* in Figure 14). Small peripheral sensory nerves (Figure 12, arrowhead) run in the long axis of the tail; these were described in detail by Holland and Somorjai (2020a); many of them are too small to detect in light micrographs so they are not included in the present study.…”

“…At this, and at all subsequent regeneration stages, the wound epidermis remains single‐layered. The subepidermal collagen fibril layer (Holland & Somorjai, 2020a) stops abruptly at the edge of the wound (Figures 16 and 17, single arrows) and is undetectable beneath the wound epidermis.…”

Amphioxus neuroglia: Molecular characterization and evidence for early compartmentalization of the developing nerve cord

“…In the amphioxus peripheral nervous system, small cells, called Müller glia, are associated with dorsal nerves and motor neurons contacting the muscles (Bone, 1960). Glial cells are also said to ensheathe sensory neurites that innervate the adult tail, similar to vertebrate nonmyelinating Schwann cells (Holland & Somorjai, 2020). Given that amphioxus lacks a definite neural crest, the peripheral glia‐like cell populations are likely of intramedullary origin.…”

Serial blockface SEM suggests that stem cells may participate in adult notochord growth in an invertebrate chordate, the Bahamas lancelet

“…1 b) because it is a close neighbor of the notochord and a likely candidate for providing at least part of the microenvironment influencing the maintenance and differentiation of notochordal stem cells. The CNS cells in the reconstructed region are mostly, and possibly entirely, neuroglia [ 16 ]. Low-magnification SBSEM could not resolve cytoplasmic boundaries between these cells, but their distribution is adequately shown by depictions of their nuclei alone.…”