A sharp retinal image increases the topographic precision of the goldfish retinotectal projection during optic nerve regeneration in stroboscopic light

Abstract

Locally-correlated neural activity appears to play a key role in refining topographically mapped projections. The retinotectal projection of the goldfish normally regains a high degree of spatial precision after regeneration of a cut optic nerve, but it fails to do so if retinal ganglion cell activity is blocked by tetrodotoxin, or if local correlations in activity are masked by the synchronizing effect of stroboscopic light. A sharp retinal image is not normally needed for a sharp map because local correlation occurs even in darkness or diffuse light, but the possibility that a sharp image might restore local correlation and sharpen the map in stroboscopic light, though taken into account in earlier experiments, has not previously been tested. The precision of the retinotectal map was therefore studied, by retrograde transport of WGA-HRP from a standard tectal injection site and quantitative analysis of the labelled ganglion cell distribution, after regeneration of a cut optic nerve for 83-84 days in either continuous stroboscopic light or normal diurnal light. The lens of the eye was either ablated to blur the retinal image or sham-operated. Two different strobe flash patterns used in previous experiments were also compared. With the lens ablated, stroboscopic light impaired map refinement significantly, confirming previous results. A rapid, irregular flash pattern averaging about 5 Hz was rather more effective than a regular 1 Hz pattern. With the lens intact, however, neither pattern had any detectable effect. The significant gain in precision resulting from a sharp retinal image in these circumstances suggests that common mechanisms could underlie both the internal refinement of the retinotectal map and such directly experience-sensitive processes as the experimental realignment of binocular maps in the frog Xenopus, and of auditory and visual maps in the barn owl.

The development of topography in the visual cortex: a review of models

“…However, these different mechanisms seem likely to operate at different stages of development: initially, topography is probably established by time of outgrowth, selective adhesion, axonal guidance and chemical cues, while in the final stages, a neural-activity-dependent mechanism may lead to a further increase in topographic precision (see e.g. Schmidt and Edwards (1983), Cook (1987), Cook and Becker (1990), Constantine-Paton et al (1990)). …”

Somatic and Dendritic Mosaics Formed by Large Ganglion Cells in the Retina of the Common House Gecko <i>(Hemidactylus frenatus)</i>

“…The HRP was revealed with diaminobenzidine in acetate buffer (pH 6.0) and intensified with cobalt and nickel. The free-floating retina was then dehydrated through alcohols, cleared in methyl salicylate, and flat-mounted in DePeX (Gurr) on standard glass slides bearing photographically generated grids of 0.5 mm squares [Cook, 1987]. Substantial shrinkage occurs in retinae processed in this way, and, in keeping with normal practice, no correction has been made for it in the reported dimensions.…”

“…Standard methods [Cook, 1987] were used to plot and digitize the locations of individual ganglion cells across as much of each specimen as possible, at a total magnification of ×120. The locations of individual photoreceptors and dendritic links were plotted in the same way but with the × 63/1.2 W objective at a magnification of × 600.…”

Spontaneous Activity as a Determinant of Axonal Connections

“…For example, when the optic nerve of a fish is cut, axon regrowth is followed by a slow spatial Rodieck, 1967;Mastronarde, 1983). Moreover, lens ablation, which blurs the retinal image so much that it must abolish any visually evoked local correlation, has no appreciable effect on map refinement in diurnal light Cook, 1987a). This implies that spontaneous activity is capable of providing the necessary spatial information.…”

“…This implies that spontaneous activity is capable of providing the necessary spatial information. On the other hand, stroboscopic light does not block refinement as effectively when the retinal image is sharp as when it is blurred (Cook, 1987a), and it has been claimed that refinement is at least partially impaired in darkness (Schmidt and Eisele, 1985).…”