The effects of changing retinal ganglion cell (RGC) density and availability of presynaptic sites on the development of RGC dendritic arbor in the developing chick retina were contrasted. Visual form deprivation was used to induce ocular enlargement and expanded retinal area resulting in a 20-30% decrease in RGC density. In these retinas, RGC dendritic arbors increased in a compensatory manner to maintain the inner nuclear layer to RGC convergence ratio in a way that is consistent with simple stretching; RGC dendritic arbors become larger with increased branch lengths, but without change in the total number of branches. In the second manipulation, partial optic nerve section was used to produce areas of RGC depletion of approximately 60% in the central retina. This reduction in density is comparable to the density of locations in the normal peripheral retina. In RGC-depIeted retinas, dendritic arbor areas of RGCs in the central retina grow to match the size of normal peripheral arbors. In contrast to the expanded case, two measures of intrinsic arbor structure are changed in RGC-depleted retinas; the branch density of RGC dendrites is greater, and the relative areas of the two arbors of bistratified cells are altered. We discuss the potential roles of retinal growth, local RGC density, and availability of presynaptic terminals in the developmental control of RGC dendritic arbor.
The ability of pre- and postsynaptic populations to achieve the proper convergence ratios during development is especially critical in topographically mapped systems such as the retinotectal system. The ratio of retinal ganglion cells to their target cells in the optic tectum can be altered experimentally either by early partial tectal ablation, which results in an orderly compression of near-normal numbers of retinal projections into a smaller tectal area, or by early monocular enucleation, which results in the expansion of a reduced number of axons in a near-normal tectal volume. Our previous studies showed that changes in cell death and synaptic density consequent to these manipulations can account for only a minor component of this compensation for the population mismatch. In this study, we examine other mechanisms of population matching in the hamster retinotectal system. We used an in vitro horseradish peroxidase labeling method to trace individual retinal ganglion cell axons in superior colliculi partially ablated on the day of birth, as well as in colliculi contralateral to a monocular enucleation. We found that individual axon arbors within the partially lesioned tectum occupy a smaller area, with fewer branches and fewer terminal boutons, but preserve a normal bouton density. In contrast, ipsilaterally projecting axon arbors in monocularly enucleated animals occupy a greater area than in the normal condition, with a much larger arbor length and greater number of boutons and branches compared with normal ipsilaterally projecting cells. Alteration of axonal arborization of retinal ganglion cells is the main factor responsible for matching the retinal and tectal cell populations within the tectum. This process conserves normal electrophysiological function over a wide range of convergence ratios and may occur through strict selectivity of tectal cells for their normal number of inputs.
The retinal projection to the superior colliculus can be made abnormally dense by inducing a "compressed" retinal projection into a subnormal tectal volume, or abnormally sparse by monocular enucleation early in development. Any or all of the features of cell number, axonal arbor, dendritic arbor, and synaptic density could potentially be adjusted to compensate for such variations in the convergence of one cell population on another. We have examined the consequences of neonatal partial tectal ablation or monocular enucleation for synaptic length, density, and relative numbers of synapse classes in the superficial gray layer of the hamster superior colliculus. Monocular enucleation resulted in a reduction of synaptic density in the superficial gray layer of the colliculus ipsilateral to the remaining eye. This decrease in density was entirely accounted for by a reduction of the number of synapses with round vesicles, large asymmetric terminal specializations, and pale mitochondria characteristic of retinocollicular terminals (RLP synapses). There was no compensatory increase in any other synaptic class. RLP synapses were larger in monocular enucleates. Partial tectal ablation had no effect on synaptic density, nor on the relative proportions of different synaptic types. Synapses of the RLP class were slightly smaller than normal. These results suggest that synaptic density is normally at a maximum that cannot be altered by increases in potential input. However, density may be reduced by decreasing the number of inputs. Terminal classes do not appear to compete with each other within the collicular volume, suggesting that postsynaptic cells controls both the classes and numbers of their potential inputs.
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