Peculiar and typical oligodendrocytes are involved in an uneven myelination pattern during the ontogeny of the lizard visual pathway

Abstract

We studied the myelination of the visual pathway during the ontogeny of the lizard Gallotia galloti using immunohistochemical methods to stain the myelin basic protein (MBP) and proteolipid protein (PLP/DM20), and electron microscopy. The staining pattern for the PLP/DM20 and MBP overlapped during the lizard ontogeny and was first observed at E39 in cell bodies and fibers located in the temporal optic nerve, optic chiasm, middle optic tract, and in the stratum album centrale of the optic tectum (OT). The expression of these proteins extended to the nerve fiber layer (NFL) of the temporal retina and to the outer strata of the OT at E40. From hatching onwards, the labeling became stronger and extended to the entire visual pathway. Our ultrastructural data in postnatal and adult animals revealed the presence of both myelinated and unmyelinated retinal ganglion cell axons in all visual areas, with a tendency for the larger axons to show the thicker myelin sheaths. Moreover, two kinds of oligodendrocytes were described: peculiar oligodendrocytes displaying loose myelin sheaths were only observed in the NFL, whereas typical medium electron-dense oligodendrocytes displaying compact myelin sheaths were observed in the rest of the visual areas. The weakest expression of the PLP/DM20 in the NFL of the retina appears to be linked to the loose appearance of its myelin sheaths. We conclude that typical and peculiar oligodendrocytes are involved in an uneven myelination process, which follows a temporo-nasal and rostro-caudal gradient in the retina and ON, and a ventro-dorsal gradient in the OT.

Development of astroglia heterogeneously expressing Pax2, vimentin and GFAP during the ontogeny of the optic pathway of the lizard (Gallotia galloti): an immunohistochemical and ultrastructural study

“…microtubules, nestin) might be sufficient to preserve the cell morphology under normal physiological conditions, although not after retinal insults (Lundkvist et al 2004). The proximity of loose myelin and Müller processes in the PR and the apparent absence of glial cells in this region indicate they cooperate in myelination as suggested previously (Santos et al 2006) Interestingly, in G. galloti, Müller glia express Pax2 only in the CR, as reported in zebrafish and chick (Boije et al 2010;Stanke et al 2010). However, retinal astrocytes are the only astroglia expressing Pax2 in mammals.…”

Expression of BDNF and NT‐3 during the ontogeny and regeneration of the lacertidian (Gallotia galloti) visual system

“…Because newly hatched lizards require a functional visual system to survive in their natural environment, abundant BDNF staining at this stage may be a key factor mediating experience-dependent effects on RGCs (Landi et al, 2007). In this respect, the temporo-spatial staining pattern of fibers is reminiscent of that of the myelination process (Santos et al, 2006) although BDNF staining in putative myelinating cells was undetected during development. As BDNF is essential for myelination and remyelination by Schwann cells (Zhang et al, 2000;Chan et al, 2001) and BDNF KO mice have hypomyelinated RGCs axons (Cellerino et al, 1997), we hypothesize that RGCs expressing BDNF might also regulate myelination of lizard RGC axons by local influence on oligodendrocytes.…”

Extraocular Source of Oligodendrocytes Contribute to Retinal Myelination and Optokinetic Responses in Zebrafish

“…25 Previous studies have shown that axons are myelinated in some lower vertebrate retinas, such as in chickens, lizards, and goldfish. [2][3][4][5] Despite a lack of transgenic lines, they simply described myelination and the different developmental states of OLs by immunohistochemistry and TEM evidence. Using olig2 zebrafish, 12 we can quantitatively observe the temporal dynamics of myelination in zebrafish retinas.…”

“…5). 22 Although retinal myelination has been reported in some lower vertebrates, such as chickens, lizards, turtles, and fish, [2][3][4][5] no study has related the functional characterization of myelin in retinas. Lysophosphatidylcholine can induce rapid and highly reproducible demyelination in the CNS without producing much damage to the axons.…”

“…[2][3][4][5] By immunohistochemistry and transmission electron microscopy (TEM), previous studies described myelination and different developmental states of oligodendrocytes (OLs) in the above animals' retinas. [2][3][4][5] Through an injection of fluorescent dye DiI into the third ventricle, previous studies have also shown that some OLs can migrate into chick retinas from external to the eye. 3 However, whether all OLs in retinas are from external to the eye was not yet clearly demonstrated.…”