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

The map of the retina onto the optic tectum is a highly conserved feature of the vertebrate visual system; the mechanism by which this mapping is accomplished during development is a long-standing problem of neurobiology. The early suggestion by Roger Sperry that the map is formed through interactions between retinal ganglion cell axons and target cells within the tectum has gained significant experimental support and widespread acceptance. Nonetheless, reports in a variety of species indicate that some aspects of retinotopic order exist within the optic tract, leading to the suggestion that this "preordering" of retinal axons may play a role in the formation of the mature tectal map. A satisfactory account of pretarget order must provide the mechanism by which such axon order develops. Insofar as this mechanism must ultimately be determined genetically, the mouse suggests itself as the natural species in which to pursue these studies. Quantitative and repeatable methods are required to assess the contribution of candidate genes in mouse models. For these reasons, we have undertaken a quantitative study of the degree of retinotopic order within the optic tract and nerve of wild-type mice both before and after the development of the retinotectal map. Our methods are based on tract tracing using lipophilic dyes, and our results indicate that there is a reestablishment of dorsoventral but not nasotemporal retinal order when the axons pass through the chiasm and that this order is maintained throughout the subsequent tract. Furthermore, this dorsoventral retinotopic order is well established by the day after birth, long before the final target zone is discernible within the tectum. We conclude that pretarget sorting of axons according to origin along the dorsoventral axis of the retina is both spatially and chronologically appropriate to contribute to the formation of the retinotectal map, and we suggest that these methods be used to search for the molecular basis of such order by using available mouse genetic models.

mentioning

confidence: 99%

Pretarget sorting of retinocollicular axons in the mouse

Plas

Lopez

Crair

2005

“…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.…”

Section: Discussionmentioning

confidence: 89%

“…However, pre-target axon sorting seems to play an important role in establishing and/or maintaining topographic organization of axons. It has been speculated that the pre-ordering of the dorsal and ventral axons in the optic nerve might deliver axons to their appropriate region of the target nucleus (Dunlop et al, 2000). Imai and colleagues provided showed that normal map formation fails when axons did not undergo pre-target axon sorting (Imai et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Pre‐target axon sorting in the avian auditory brainstem

Kashima

Rubel

Seidl

2013

Topographic organization of neurons is a hallmark of brain structure. The establishment of the connections between topographically organized brain regions has attracted much experimental attention and it is widely accepted that molecular cues guide outgrowing axons to their targets in order to construct topographic maps. In a number of systems afferent axons are organized topographically along their trajectory as well and it has been suggested that this pre-target sorting contributes to map formation. Neurons in auditory regions of the brain are arranged according to their best frequency (BF), the sound frequency they respond to optimally. This BF changes predictably with position along the so-called tonotopic axis. In the avian auditory brainstem, the tonotopic organization of the second- and third-order auditory neurons in nucleus magnocellularis (NM) and nucleus laminaris (NL) has been well described. In this study we examine whether the decussating NM axons forming the crossed dorsal cochlear tract (XDCT) and innervating the contralateral NL are arranged in a systematic manner. We electroporated dye into cells in different frequency regions of NM to anterogradely label their axons in the XDCT. The placement of dye in NM was compared to the location of labeled axons in XDCT. Our results show that NM axons in XDCT are organized in a precise tonotopic manner along the rostrocaudal axis, spanning over the entire rostrocaudal extent of both the origin and target nuclei. We propose that in the avian auditory brainstem, this pre-target axon sorting contributes to tonotopic map formation in NL.

“…In addition, retinal specialisations, such as the area centralis, develop after metamorphosis in concert with continuing cell division (Dunlop and Beazley, 1981, 1984; Coleman et al, 1984; Nguyen and Straznicky, 1989). By contrast, in birds and mammals, generation of retinal ganglion cells, development of the fovea and area centralis, axon outgrowth, formation of visual centres, and synaptogenesis are restricted to early developmental stages and are largely complete by the time of eye opening (Kahn, 1973; Lund and Bunt, 1976; Beazley and Dunlop, 1983; Provis et al, 1983; Cooper and Rakic, 1983; Campbell et al, 1984; Young, 1985; Walsh and Polley, 1985; Dunlop et al, 1987, 2000a; Lia et al, 1987; Harman and Beazley, 1989; Warton and McCart, 1989; Rapaport et al, 1996).…”

mentioning

confidence: 99%

Development of visual projections follows an avian/mammalian‐like sequence in the lizard Ctenophorus ornatus

Dunlop¹,

Tee

Rodger

et al. 2002

Self Cite

Development of primary visual projections was examined in a lizard Ctenophorus ornatus by anterograde and retrograde tracing with DiI and by GAP-43 immunohistochemistry. Visual pathway development was essentially similar to that in birds and mammals and thus differed from patterns in fish or amphibians. A number of features characterised the development as mammalian-like. Three phases occurred in rapid succession after laying: outgrowth (2-3 weeks, early), exuberance (4-5 weeks, intermediate), and retraction to the adult pattern (6-8 weeks, late) at about the time of hatching and eye opening. Furthermore, ipsilateral projections developed with only a slight lag relative to the contralateral ones. The dorsally located fovea could be identified from early stages. Optic axons formed transient exuberant projections to the ipsilateral optic tectum, to the opposite optic nerve, and to nonvisual regions. The pattern resembled that formed in the long term by regenerating optic axons in C. ornatus (Dunlop et al. [2000b] J. Comp. Neurol. 416:188-200), suggesting that axons recognise molecular signals associated with the initial exuberant innervation but not those associated with subsequent refinement.