Novel organization and development of copepod myelin. ii. nonglial origin

Abstract

Nerve-impulse conduction is greatly speeded by myelin sheaths in vertebrates, oligochaete annelids, penaeid and caridean shrimp, and calanoid copepods. In the first three invertebrate cases, myelin arises from glial cells, as it does in vertebrates. The contribution of the glial cells to the layered structure of the myelin is clear: their nuclei are either embedded in the layers or reside in contiguous cytoplasmic compartments, and their cell membranes are seen to be continuous with those of the myelin layers. However, with calanoids, the association with glial cells presumed necessary to generate the myelin has never been satisfactorily identified. We have conducted a systematic examination of thin sections through different parts of the copepod nervous system to identify the structural organization of copepod myelin and the likely mechanism for its formation. We find that myelination appears to commence by laying down and compacting a cisternal tongue against the inside of the axolemma. This is followed by the successive layering and compaction of additional tongues to create a stack of tongues. The margins of the tongues then expand to encircle the interior of a neurite, meeting and fusing to form complete concentric myelin. No sign of glial involvement could be detected at any stage. Unlike glially derived myelin, the extracellular tracer lanthanum did not penetrate between the myelin layers in copepods, further evidence against a glial source. We believe this to be the first demonstration of a nonglial origin for myelin in any species.

Novel organization and development of copepod myelin. i. ontogeny

“…For caridean shrimp, no developmental studies have been carried out, but adult myelin is again different, with alternating glia overlapping to form seams on alternate sides in successive layers (Heuser and Doggenweiler, 1966). Functional, fenestrated nodes have been described in other invertebrates (Günther 1976;Xu and Terakawa, 1999), but the node structure is very different, with myelin obviously outside the axolemma in those cases, whereas in the copepod it appears to be internal to the axolemma (see also Wilson and Hartline, 2011). Thus, in all cases of crustacean myelin, the end result is the formation of complete concentric layers surrounding the axon, but the underlying structures are so different that it must be considered an example of convergent evolution.…”

“…The myelin also changes from complete to partial where DGF contacts the giant motor neuron (MoG) in a functional node (white arrow); the myelin appears to retract to the partial state to form a marginal ''cliff'' within the confines of the axolemma (black arrow on one side of node; see Fig. 6, Wilson and Hartline, 2011). Electron-dense cytoplasm is also observed in the sheath cells (sc) near the myelinated axon in D,E,H.…”

“…Through its development, we gain an understanding for what the functional adult structure represents and how and where it is attained. In a companion paper (Wilson and Hartline, 2011), we address the issue of the cell type from which the myelin is derived.…”

Adaptive evolution of voltage-gated sodium channels: The first 800 million years

“…+ Channel Clustering at the Axon Initial Segment and the Nodes of Ranvier Myelination and saltatory conduction are key innovations of the vertebrate nervous system that markedly increase axonal conduction velocity [myelination evolved multiple times in some invertebrate lineages as well despite a widespread and persistent belief to the contrary (25,26)]. Myelination is not present in agnathans but occurs in all gnathostomes, likely appearing first in a placoderm ancestor (27).…”

The Evolution of Myelin: Theories and Application to Human Disease

“…Intriguingly copepod myelin seems to be neurally, rather than glially derived, developing by sequential laying down of membrane layers on the inside of the axon membrane [47,48]. This explains the continuous structure; one possible application of this discovery is discussed in Section 3.…”