Axon order in the visual pathway of the quokka wallaby

Abstract

Axon order throughout the visual pathway of the quokka wallaby (Setonix brachyurus) was determined after localised retinal applications of the tracers DiI and/or DiASP. Postnatal days (P) 22-90 were studied to encompass the development and refinement of retinal projections. Order was essentially similar at all stages. Axons entered the optic nerve head true to their sector of retinal origin. In the optic nerve, nasal and temporal axons continued to reflect their retinal origin, dominating, respectively, the medial and lateral halves. By contrast, dorsal and ventral axons exchanged locations between the retrobulbar level and one-third the distance along the nerve; thus, the inversion of the dorsoventral retinal axis, imposed by the lens, was corrected. Decussating axons maintained their relative locations through the chiasm. At the base of the optic tract, nasal and temporal axons underwent an axial rotation to lie on the medial and lateral sides, respectively; thus nasal overlapped with ventral axons and temporal with dorsal axons. Axons maintained their alignments throughout the tract, and as a result, nasal and ventral axons invaded the superior colliculus medially, whereas temporal and dorsal axons invaded laterally. Each retinal quadrant terminated preferentially in its retinotopically appropriate sector of the colliculus. The arrangement of axons in the quokka visual pathway displays several novel features. Axon order is distinct throughout, involving a well-demarcated exchange of dorsal and ventral axons in the nerve and an axial rotation of nasal and temporal axons at the base of the tract; these relocations suggest decision regions for growing axons. The organisation presumably underlies the less extensive searching within the developing superior colliculus to generate retinotopic maps in the quokka and also in tammar wallaby [Marotte, J. Comp Neurol. 293:524-539, 1990] than in the rat [Simon and O'Leary, J. Neurosci. 12:1212-1232, 1992].

Pretarget sorting of retinocollicular axons in the mouse

“…Similar pretarget order has been previously observed in many species, including the rat, ferret, cat, primate, and marsupials, as well as all the submammalian orders for which it has been examined (Bunt and Horder, 1983). In general, pretarget order is stronger in submammalian orders and has been described as weakest in rodents (Chelvanayagam et al, 1998), although we have shown here that it is quite robust. In the human, clinical literature suggests little fiber order in the optic nerve but an increasing degree of order in the ascending optic tract (Miller and Newman, 1998).…”

Pre‐target axon sorting in the avian auditory brainstem

“…Within the optic nerve, axons exiting the retina from dorsal and ventral locations appear to maintain this spatial dimension than axons originating from the nasal and temporal part (Simon and O'Leary, 1991; Chan and Guillery, 1994). A particularly distinct ordering of ventral versus dorsal axons was presented by Dunlop and colleagues in two species of marsupials (Chelvanayagam et al, 1998; Dunlop et al, 2000). Here, dorsal and ventral axons of the optic nerve remain organized in separate partitions throughout the whole fiber tract.…”

“…Examples of topographic pathways include: axon groups spanning the corpus callosum (Hofer and Frahm, 2006), functionally and anatomically differentiated components in the spinothalamic tract (Craig, 2006) and the somatotopic sciatic nerve in rats, with muscular fascicles maintaining the same relative position along the entire nerve (Badia et al, 2010). One axon pathway whose topography has been extensively studied is the retinotectal tract, comprised of the optic nerve axons that will terminate in the superior colliculus or optic tectum (Brouwer and Zeeman, 1926; Hoyt and Luis, 1962; Easter et al, 1981; Aebersold et al, 1981; Torrealba et al, 1982; Bunt and Horder, 1983; Reh et al, 1983; Voigt et al, 1983; Springer and Mednick, 1985; Naito, 1986; Fraley and Sharma, 1986; Naito, 1989; Reese and Baker, 1993; reviewed in Chelvanayagam et al, 1998). Within the optic nerve, axons exiting the retina from dorsal and ventral locations appear to maintain this spatial dimension than axons originating from the nasal and temporal part (Simon and O'Leary, 1991; Chan and Guillery, 1994).…”

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

“…A less stringent visual pathway order has been reported for nasal and temporal axons in a number of species (Torrealba et al, 1982; Naito, 1989; Reese and Cowey, 1990; Simon and O'Leary, 1991; Chan and Guillery, 1994; Chelvanayagam et al, 1998). Furthermore, the mapping of the nasotemporal axis within target tissue is constrained in a way most clearly demonstrated by considering the developing retinocollicular system in the rat (Simon and O'Leary, 1991).…”

“…Moreover, dorsal and ventral axons appear to be more ordered than nasal and temporal ones, resulting in different patterns in which these axons enter and map within target tissue (Simon and O'Leary, 1991; Chan and Guillery, 1994). The preordering of dorsal and ventral axons is most clearly illustrated by the quokka wallaby (Chelvanayagam et al, 1998). These axons respectively exit the eye dorsally and ventrally and exchange positions approximately half way along the optic nerve.…”