The sensory peripheral nervous system in the tail of a cephalochordate studied by serial blockface scanning electron microscopy. Issue 15 (4th May 2020)

• Record Type: Journal Article
• Authors: Holland, Nicholas D.; Somorjai, Ildiko M. L.
• Is Part Of: Journal of comparative neurology. Volume 528:Issue 15(2020)
• Page Start: 2569
• Page End: 2582
• Publication Date: 2020-05-04
• Subjects: amphioxus -- Cephalochordata -- glia -- lancelet -- peripheral nervous system -- SBSEM; Comparative neurobiology -- Periodicals; Neurology -- Periodicals; 616
• DOI: 10.1002/cne.24913
• Languages: English
• ISSNs: 0021-9967

Abstract

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. Abstract : Cephalochordates (amphioxus or lancelets) are basal in the phylum Chiordata and can exemplify the relatively simple developmental and anatomical starting conditions likely to have evolved into more complex vertebrate features. Here we use serial blockface scanning electron microscopy to reconstruct the sensory peripheral nervous system in the tail of a lancelet. The nerves (glial cell/neurite complexes) branch within the dermis and then exit to the epidermis to associate with the perikarya of two kinds of ciliated sensory neurons. The results indicate that cephalochordate neuroglia have an intramedullary origin. Moreover, we suggest that the peripheral nerves in the dermis are, at least in part, comparable to Rohon‐Beard cells of vertebrates, whereas, in contrast, the placode‐ and neural crest‐derived peripheral neurons of vertebrates are evolutionary novelties that appear to have supplanted the epidermal sensory receptors of cephalochordates.