Retinal ganglion cell terminals change their projection sites during larval development of Rana pipiens

Abstract

Interconnecting neuronal populations in the vertebrate CNS are typically not well matched in their overall topographic patterns of histogenesis and differentiation during development. One striking example of this mismatch is the retinotectal system of the frog, where the retina grows in concentric annuli, while the optic tectum, a major retinal target, adds new neurons at only the caudo-medial border. The retinal ganglion cell (RGC) terminals nevertheless form an organized map in the tectum during the period when the two structures are undergoing such disparate modes of growth. This led Gaze et al. (Gaze, R. M., M. J. Keating, and S. H. Chung (1974) Proc. R. Soc. Lond. (Biol.) 185: 301-330) to propose that the terminals must shift caudally during development. In the present study, we have directly tested the hypothesis of "shifting connections" by selectively labeling an identified population of RGC terminals, those at the optic nerve head (ONH), and determining their tectal projection site relative to a particular group of [3H]thymidine-labeled tectal neurons. With this double-label technique, we have found that RGC terminals from cells at the ONH move from a position rostral to the [3H]thymidine-labeled tectal cells to a position caudal to these same cells during the latter half of larval development. This represents a movement of approximately 1.4 mm across the tectal surface between stages T&K XII and T&K XXV. In addition, we have used electron microscopy and electrophysiology to demonstrate that the RGC terminals make functional synaptic connections during this period. This indicates that RGC terminals continually change the tectal neurons with which they form functional synapses during the development of the retinotectal system. We propose that such moving, but highly ordered connections can best be explained by a two stage mechanism for map formation, in which graded selective adhesions between cells in appropriate regions of retina and tectum provide the overall gross retinotopy of the projection, while competitive interactions between RGC terminals are responsible for the refinement of the precision in this system.

Stabilization of Axon Branch Dynamics by Synaptic Maturation

“…The retinotopic projection in frogs and fish remains plastic throughout life, because retinal axons continually shift their positions in the tectum to maintain retinotopy despite asymmetric patterns of neurogenesis in the retina and tectum (Easter and Stuermer, 1984;Reh and Constantine-Paton, 1984). In addition to continually updating the retinotopic map, retinotectal axons must also convey useful visual information to the brain of the tadpole.…”

Ion Channel Development, Spontaneous Activity, and Activity-Dependent Development in Nerve and Muscle Cells

“…543, 615 for review). In cold-blooded vertebrates, the retinotopic map of initial RGC projections is fairly accurate, although there is substantial remodeling and refinement of that map, partly to compensate for retinal and tectal growth (494). This period of refinement occurs after the establishment of patterned vision, and thus the activity dependence of refinement in these animals could reflect activity driven by visual input, although the relative roles of visually driven and spontaneous activity are not entirely clear (see Ref.…”

Growth behavior of retinotectal axons in live zebrafish embryos under TTX‐induced neural impulse blockade

“…As demonstrated recently by Schmidt and Buzzard (1993), the receptive fields in 1.5-to 2-year-old goldfish raised under strobe light were enlarged, and small and large arbors-but not medium sized ones-bore ectopic side branches. Terminal arbors in fish constantly move , while the retina and the tectum grow to maintain retinotopia, a process called shifting of terminal arbors (Reh and Constantine-Paton, 1984;Easter and Stuermer, 1984). It appears that normal activity patterns may be required during the process of retinotectal arbor shifting for the elimination of side branches (Schmidt and Buzzard, 1993).…”