Research report
Survival of isthmo-optic neurons after early removal of one eye

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Abstract

In a series of normal 12- or 13-day-old chick embryos in which the neuroanatomical tracer wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) was injected into one eye, about 25,000 neurons were found to be retrogradely labeled in the isthmic region of the brain. Of these, about 100 were found on the side of the injection, whereas about 22,000 were found in the contralateral isthmo-optic nucleus (ION, the nucleus of origin of centrifugal fibers to the retina) and a further 3000 ectopic cells were present on this side but lay outside the borders of the ION. After comparable injections on the 18th day of incubation or later, no more than 40 retrogradely labeled neurons were seen on the side of the injection, and on the contralateral side the numbers of neurons in the ION and in the ectopic ION population were reduced by about 60% to approximately 9500 and 1500 cells, respectively. In the present study we have re-examined the effects of removing one optic vesicle or optic cup on the survival and distribution of isthmo-optic neurons in two further series of chick embryos: in the first series the animals were injected intraocularly with WGA-HRP on the 12th day of incubation; in the other the eye injections were done on day 18, 19 or 20.

In animals in which the eye rudiment was removed on or before stage 13 of the Hamburger and Hamilton series23, essentially all of the centrifugally projecting neurons on both sides of the brain could be labeled from the surviving eye at day 12; however, in chicks operated upon after stage 13 the distribution of the labeled ION neurons was indistinguishable from that in a normal 12 day embryo. In monocular chicks that were allowed to survive beyond the period of naturally occurring cell death in the ION (i.e. beyond day 17) a variety of labeling patterns was seen in the ION and the surrounding region. In nearly all of the animals in which the eye was removed after stage 13, the number of labeled neurons on the side contralateral to the surviving eye was comparable to that seen in a normal, unoperated embryo, whereas virtually no cells were labeled in the isthmic region of the opposite (ipsilateral) side. In animals in which the eye removal was done on or before stage 13 the ION and ectopic ION populations on both sides were frequently labeled, but in no case did the total number of labeled neurons on the two sides exceed the number found on one side in a normal chick. In other animals operated on at these stages, very few labeled cells were found on the side of the surviving eye, but the number on the contralateral side was again only about half that found in a normal animal. Analysis of the anterogradely labeled retinofugal projection in these brains suggests that there is a close correlation between the number of surviving isthmo-optic neurons on each side and the magnitude of the crossed and uncrossed retinal projections to the optic tectum.

Taken together the present findings provide further evidence in support of the notion that during development the axons of the centrifugal neurons compete with each other within the retina, for a trophic agent that is available in only limited supply. In addition, they indicate that the availability of the trophic agent is not regulated by the magnitude of the centrifugal input to the retina, since even in animals in which the retina was innervated by twice the normal number of centrifugal fibers, the surviving eye was never able to support more than the normal number of isthmo-optic neurons. Several possible factors that may be involved in determining the laterality of the centrifugal projection in monocular chicks are discussed.

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