Topographic order of retinofugal axons in a marsupial: Implications for map formation in visual nuclei

Abstract

We studied axon order in the primary visual pathway and in nine retinorecipient nuclei of a small marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata) using animals at postnatal day (P) 40 and P80. Dorsal, ventral, nasal, and temporal axons enter the optic nerve true to their retinal origin being respectively dorsal, ventral, medial, and lateral; the arrangement is retained to the chiasm. Dorsal and ventral axons maintain their respective locations within the chiasm but at the base of the contralateral optic tract undergo a 180 degrees axial rotation, thus reversing the dorsoventral axis with respect to the retina. The alignment is conserved along the optic tract with dorsal and ventral axons mapping directly into appropriate quadrants of each retinorecipient nucleus. Nasal and temporal axons remain segregated as they decussate and lie respectively superficially and deep along the optic tract but with some intermingling. Within each retinorecipient nucleus, the nasotemporal axis is clearly demarcated, being represented in either a rostrocaudal (ventral and dorsal lateral geniculate nuclei; lateral posterior, dorsal terminal, and pretectal nuclei) or caudorostral (medial terminal and caudal pretectal nuclei, intergeniculate nucleus and superior colliculus) direction. The results imply that the dorsoventral axis in the retinorecipient nuclei could be due to preordering within the pathway, whereas the nasotemporal axis is determined by target-based cues. Moreover, cues for the orientation of the nasotemporal axis within retinorecipient nuclei must be localised within individual nuclei rather than as a single organiser, as previously envisaged (Chung and Cooke [1978] Proc. R. Soc. Lond. B. 210:335-373).