Development of primary visual projections occurs entirely postnatally in the fat-tailed dunnart, a marsupial mouse,Sminthopsis crassicaudata

Abstract

We have examined the development of retinal projections in a diminutive polyprotodont marsupial, the fat-tailed dunnart, Sminthopsis crassicaudata. Here, we document the most immature mammalian visual system at birth described to date. At postnatal day (P) 0, the retinal ganglion cell layer has yet to form, and axons have not entered the optic stalk. By P4, the retinal ganglion cell layer could be distinguished at the posterior pole, and the front of growing axons extended one-third the length of the optic stalk, a distance of approximately 150 microm; a few pioneer growth cones had grown beyond the main axon group but had still to reach the midline. Axons had decussated at the optic chiasm by P10 to penetrate the base of the contralateral optic tract and, by P15, had reached the dorsal lateral geniculate nucleus (dLGN), superior colliculus (SC), and accessory optic system (AOS); ipsilaterally projecting axons matured slightly later. From P20, axons had reached the caudal SC both contralaterally and ipsilaterally and terminated throughout the depth of the retinorecipient layers. After P30, the projections gradually refined. Within the rostral dLGN, segregation into four contralateral and four ipsilateral bands occurred by P50, approximately 5 days after eye opening. The projection to the ipsilateral SC underwent refinement by P50, becoming restricted to its rostral pole, and presented as discrete patches within the stratum opticum. At birth, the dunnart visual system is comparable to early to midembryonic stages [embryonic day (E) 12, E14, E19, E24, and E30, respectively] in the mouse, rat, ferret, cat, and monkey. The extreme immaturity of the neonatal dunnart together with the observation that the entire development of the primary optic pathway occurs postnatally over a protracted period make this marsupial especially valuable for investigating factors that control pathway formation in the early developing mammalian primary visual system.

Translating developmental time across mammalian species

“…No additional animals were killed. Data were obtained from Tables 1^5 of Robinson and Dreher (1990), Table 2 from Finlay and Darlington (1995), Tables 1^3 of Ashwell et al (1996), data reported in Dunlop et al (1997), Table 1 of Darlington et al (1999), as well as from the general literature where noted. Data for the cortical events in this study refer to posterior (presumptive visual) cortex.…”

The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function

“…In grey squirrels the AOS nuclei are already innervated at birth (Cusick and Kaas, 1982), although these retinal projections undergo redistribution during postnatal development. Studies in the marsupial fat-tailed dunnart (Dunlop et al, 1997) have shown that the development of visual pathways in general and of accessory optic projections in particular, occurs entirely postnatally in this species: retinal projections don't reach the accessory optic nuclei until P15. This makes the dunnart a suitable species for studies on the development of the visual system.…”

Differentiation and Morphological Integration of Neural Progenitor Cells Transplanted into the Developing Mammalian Eye

“…Their lack of a pouch and their fetal‐like nature at birth circumvents the need for in utero experimental procedures that would be required on more conventional mammalian model systems such as mice, rats, rabbits, ferrets, or cats. Thus, their immaturity at birth and their protracted period of postnatal development make marsupials, like Monodelphis , excellent models for the study of visual system development and plasticity 17–22…”