Right and left eye bands in frogs with unilateral tectal ablations.

Abstract

ASBSTRACTSurgical ablation of a single tectal lobe in Rana pipiens can cause regenerating retinal ganglion cell axons to cross to the remaining tectum. These synaptically deprived fibers can obtain termination space in a retinotopic and highly stereotyped manner. Each of the two eyes can share the undisturbed tectum by terminating in mutually exclusive, eye-specific stripes that alternate across the medial-lateral extent of the tectal lobe. Invading axons from the ipsilateral eye must actively displace establish synapses from the contralateral eye in order to form these exclusive termination zones because the normal projection to the intact tectum is not severed in these experiments. In animals in which a large proportion of anomalous fibers do not reach the undisturbed tectum, only a few ipsilateral eye bands are observed. Nevertheless, these bands have the same width, periodicity, and orientation as those observed in fully banded preparations. When ipsilateral eye terminal density is extremely low, banding is absent. The completely striped termination pattern of unitectal animals is identical to the pattern previously reported in the dually innervated tecta of three-eyed R. pipiens. We theorize that this pattern results from a compromise between two synaptogenic forces that are active in regeneration as well as in development. Axons originating from different presynaptic sources often segregate during termination within a single synaptic region. These input segregation patterns can appear as ellipses, annulae, or patches (1-7). However, the most widely known example is the system of interdigitating left and right eye stripes, the ocular dominance columns, produced by alternating layers of the dorsal lateral geniculate in layer IV of cat and monkey visual cortex (3,4,(8)(9)(10).Recently we reported (11) that similar stripes of visual input can be produced experimentally in the optic tectum of developing Rana pipiens. Normally, the optic tectum in these frogs receives direct retinal ganglion innervation from the contralateral eye. However, when a supernumerary eye primordium is implanted in early embryonic stages, the third eye will frequently innervate one of the two tecta along with retinal axons from one of the host's eyes. The presence of a supernumerary optic projection disrupts the normally continuous ganglion cell termination pattern within the superficial tectal neuropil. In these three-eyed frogs the fibers from the supernumerary and normal eyes form approximately 200-,m-wide eye-specific bands of neuropil that alternate across the medial-lateral extent of the doubly innervated optic lobe (11).We report here that the striped pattern also can be produced in regeneration after the unilateral ablation of one of the two tectal lobes. During regeneration the segregation develops in differentiated nervous tissue between inputs from the left and right eyes of the same animal. Moreover, the segregation involves a period in which surgically undisturbed retinotectal synapses are displaced by axons that invade the...

Insights into activity‐dependent map formation from the retinotectal system: A middle‐of‐the‐brain perspective

“…In general, manipulations that cause RGC axons expressing common molecular cues to have different patterns of activity will result in afferent segregation. For example, if axons from both eyes in an animal are made to project to a single tectal lobe by rerouting axons from one eye to innervate the ipsilateral tectum, ocular dominance bands form as well (Straznicky and Glastonbury, 1979;Law and Constantine-Paton, 1980). Surgically manipulating a single eye to create a bilaterally symmetric double nasal or double temporal retina similarly produces segregation of axons from the two halves of the eye (Ide et al, 1983;Coletti et al, 1990).…”

Analysis of mouse EphA knockins and knockouts suggests that retinal axons programme target cells to form ordered retinotopic maps

“…Its primary role would be to prune away the axonal arbor so as to reduce the overlap between adjacent axonal projections (Johnson et al, 1999;Ruthazer and Cline, 2004). In the special case of the double innervation of the target, in either the three-eyed frog (Constantine-Paton and Law, 1978), Xenopus compound eye (Fawcett and Willshaw, 1982) paradigms or by allowing optic nerve fibres to reinnervate both contralateral and ipsilateral tecta (Law and Constantine-Paton, 1980;Meyer, 1982), this will result in the formation of striped patterns of ocular dominance. On this interpretation, it would be expected that, in the three heterozygous EphA3 knockin cases discussed here, eventually discontinuous projections would develop on the rostrocaudal region of colliculus where coalescence of the projections from EphA3 + cells and EphA3 -cells was observed.…”

Emergence of binocular functional properties in a monocular neural circuit

“…Specifically, we artificially induced a second retinal projection to the otherwise monocular larval zebrafish optic tectum and carried out in vivo two-photon calcium imaging of recipient neuronal populations11,12. Although several seminal studies have used similar retinotectal rewiring techniques to provide important anatomical insights into developmental plasticity13-15, we present, to the best of our knowledge, the first functional analysis of these circuits to test the sufficiency of retinotectal rewiring for the emergence of binocular receptive-field properties.…”