Regulation of retinal ganglion cell axon arbor size by target availability: Mechanisms of compression and expansion of the retinotectal projection

Abstract

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.

Development and matching of binocular orientation preference in mouse V1

“…The LGN axons compete for neurotrophic factors released by the post-synaptic cells. Such fixed pre- and post-synaptic resources in the RGCs of gold fish (Hayes and Meyer, 1988) and optic tectum cells (Xiong et al, 1994) are reported in the literature.…”

Compensatory and transneuronal plasticity after early collicular ablation

“…Volume measurements of HRPlabeled terminal fields are an overall measure that do not necessarily equate to equal densities of terminal connections. Measurements of individual arbors and terminal bouton numbers would be necessary to examine RGC arbors at the single cell level (Xiong et al, 1994).…”

“…vLGN, ventral lateral geniculate nucleus; dLGN, dorsal lateral geniculate nucleus; PT/LP, pretectal/lateral posterior nucleus complex; SC, superior colliculus. mal bouton density (Xiong et al, 1994). As a result, normal electrophysiological function can be maintained over a wide range of convergence ratios such as would occur after orderly compression of the retino-collicular projection (Finlay et al, 1979a;Xiong et al, 1994).…”

Large Developing Receptive Fields Using a Distributed and Locally Reprogrammable Address–Event Receiver

“…More commonly however neurons make connections to many other neurons (i.e., they have a large axonal "fan-out") and receive large numbers of incoming connections (dendritic "fan-in"). As two examples, Xiong et al [10] found an average fan-out of 167 for retinal ganglion cells in the tectum of the hamster, while Palkovits et al [11] found an average fan-in of 85 000 onto the Purkinje cells of the cat. In order to implement arbitrary many-to-many network connectivity, address-events are commonly received not directly by a neural array chip but rather by a microcontroller, and are then compared to a lookup table in memory in order to find out the addresses of the neurons or synapses which should be targeted.…”