Influence of spontaneous activity and visual experience on developing retinal receptive fields

BACKGROUND The role played by early neural activity in shaping retinal functions has not yet been established. In the developing vertebrate retina, ganglion cells fire spontaneous bursts of action potentials before the onset of visual experience. This spontaneous bursting disappears shortly after birth or eye opening. In the present study, we have investigated whether the outgrowth of receptive fields in turtle retinal ganglion cells is affected by early spontaneous bursting or by early visual experience. RESULTS Ganglion cells normally stop bursting spontaneously 2-4 weeks post-hatching, the time when receptive-field areas reach adult size. When turtles are reared in the dark, the spontaneous bursting persists. Concomitantly, receptive-field areas expand to more than twice those observed in normal adults. To test whether chronic blockade of spontaneous bursting inhibits the expansion of developing receptive-field areas, we have exposed the retina to curare, a nicotinic cholinergic antagonist, because spontaneous bursting by ganglion cells requires acetylcholine. Curare was released from Elvax, a slow-release polymer that was implanted in the eye. When spontaneous bursting was chronically blocked with curare in hatchlings, dark-induced expansion of receptive fields was abolished. Moreover, receptive fields of ganglion cells exposed to curare in hatchlings reared in normal light and dark cycles were smaller than normal. CONCLUSIONS These results strongly suggest that early, acetylcholine-dependent spontaneous bursts of activity control the outgrowth of receptive-field areas in retinal ganglion cells. The onset of visual experience induces the disappearance of the immature spontaneous bursts, resulting in the stabilization of receptive-field areas to their mature size.