First evidence of diversity in eutherian chiasmatic architecture: Tree shrews, like marsupials, have spatially segregated crossed and uncrossed chiasmatic pathways

Abstract

In the optic chiasm of mammals, axons either cross the midline to the opposite side of the brain or remain uncrossed. In the eutherian species studied to date, uncrossed axons in the caudal nerve are found in all regions. In the chiasm, they are dispersed through the hemichiasm, with many axons approaching the midline and then turning back to enter the same side of the brain as the originating eye. In marsupials, by contrast, uncrossed axons never approach the midline; instead, they remain grouped in the lateral nerve and chiasm. The impression gained from these data is that there is a major difference in chiasmatic architecture between eutherian and marsupial mammals. Therefore, the mechanisms by which axons choose their route through the chiasm was also thought to differ between the two major groups of mammals. However, the present study shows that the chiasm of a highly visual eutherian mammal, the tree shrew, is similar to that found in marsupials, with uncrossed axons confined to lateral regions and not approaching the midline. However, unlike marsupials, in the tree shrew, optic fascicles in the chiasm are often separated by thick collagen bundles. It is probable that the chiasmatic structure described to date for eutherian mammals is not ubiquitous, as was previously thought, and theories explaining the mechanisms by which axons chose their route through the chiasm during development will have to be expanded.

Early midline interactions are important in mouse optic chiasm formation but are not critical in man: a significant distinction between man and mouse

“…Here there is no change in axon order prechiasmatically and uncrossed axons remain confined laterally through the chiasm segregated by astrocytic processes both at maturity and during development (Jeffery & Harman, 1992). Similar patterns are found in the tree shrew (Jeffery et al. , 1998).…”

Early development of the nervous system of the eutherian <i>Tupaia belangeri</i>

“…In the studied embryos of Tupaia belangeri, ipsilateral axons turn back towards their site of origin already in prechiasmatic parts of the optic nerve (Fig. 7a, b, Knabe et al, 2008; for adult Tupaia also see Jeffery et al, 1998), thus resembling marsupials (Taylor and Guillery, 1994;Harman and Jeffery, 1995; MacLaren, 1998). Consequently, it seemed to us rather improbable that axonal pathfinding in the optic chiasm of Tupaia should be primarily attributable to midline signalling.…”

Segregated hemispheric pathways through the optic chiasm distinguish primates from rodents

“…In the marmoset, extra-fascicular collagen was present deep into the chiasm and was continuous with that found around fascicles in the proximal nerve. These patterns were reminiscent of patterns seen in the tree shrew (Jeffery et al, 1998). At the interface between the nerve and the chiasm, there was no indication of any fibres coursing across the width of the nerve that might correspond to the anterior knee of Wilbrand, which was supposed to represent fibres coursing from the contralateral nerve that had already crossed the midline and partially obscured fibres from the other eye as they enter the chiasm.…”

“…The eutherian (placental) line of mammalian evolution did not develop until after the marsupials were an established group (Novacek, 1992). Interestingly, tree shrews are like marsupials in lacking any change in fibre order in the prechiasmatic region of the optic nerve and have segregated hemispheric pathways through the chiasm (Jeffery et al, 1998). Hence, it is possible that rodents and carnivores may form a separate and distinct group in terms of this feature.…”

“…Ipsilaterally projecting ganglion cells are spatially mixed with contralaterally projecting cells in the temporal retina in rodents and ferrets (Jeffery et al, 1981; Thompson and Morgan, 1993), while in primates the two populations are segregated (Fukuda et al, 1989). While this notion is initially appealing, it is undermined by the fact that in both marsupials and tree shrews, that have segregated hemispheric pathways through the chiasm, ipsilaterally and contralaterally projecting ganglion cell populations are mixed in the temporal retina (Harman and Jeffery 1992; Jeffery et al, 1998). Hence, the organisation of the naso-temporal division is independent of the configuration of the hemispherical pathways at the chiasm.…”