Developmental switch in excitability, Ca(2+) and K(+) currents of retinal ganglion cells and their dendritic structure.

ABSTRACT

In the retina of teleost fish, continuous neuronal development occurs at the margin, in the peripheral growth zone (PGZ). We prepared tissue slices from the retina of rainbow trout that include the PGZ and that comprise a time line of retinal development, in which cells at progressive stages of differentiation are present side by side. We studied the changes in dendritic structure and voltage-dependent Ca(2+), Na(+), and K(+) currents that occur as ganglion cells mature. The youngest ganglion cells form a distinct bulge. Cells in the bulge have spare and short dendritic trees. Only half express Ca(2+) currents and then only high-voltage-activated currents with slow inactivation (HVAslow). Bulge cells are rarely electrically excitable. They express a mixture of rapidly inactivating and noninactivating K(+) currents (IKA and IKdr). The ganglion cells next organize into a transition zone, consisting of a layered structure two to three nuclei thick, before forming the single layered structure characteristic of the mature retina. In the transition zone, the dendritic arbor is elaborately branched and extends over multiple laminae in the inner plexiform layer, without apparent stratification. The arbor of the mature cells is stratified, and the span of the dendritic arbor is well over five times the cell body's diameter. The electrical properties of cells in the transition and mature zones differ significantly from those in the bulge cells. Correlated with the more elaborate dendritic structures are the expression of both rapidly inactivating HVA (HVAfast) and of low-voltage-activated (LVA) Ca(2+) currents and of a high density of Na(+) currents that renders the cells electrically excitable. The older ganglion cells also express a slowly activating K(+) current (IKsa).