Emergence of complex receptive field properties of ganglion cells in the developing turtle retina

1. Receptive field properties of adult retinal ganglion cells are well documented, but little is known about their development. We made extracellular recordings of activity from turtle retinal ganglion cells during embryogenesis (stages 22-26), during the first 40 days posthatching, and in adults. 2. From stage 22 the cells fired in spontaneous recurring bursts, and from stage 23 they responded to light. Polar plots of the responses to motion were highly anisotropic in early embryonic cells. More than 40% of embryonic cells exhibited multiaxis anisotropy, and only 6% were statistically isotropic. The incidence of anisotropic cells gradually decreased throughout development. The incidence of isotropic cells and the excitatory receptive field diameters of all ganglion cells gradually increased during development and their maturation coincided with the disappearance of the spontaneous bursts (2-4 wk posthatching). 3. Both sensitivities to stimulus orientation and direction of motion were observed at the earliest stages of development. However, orientation selectivity reached a peak incidence at hatching, whereas directional selectivity completely disappeared, only to reappear in adults. 4. These results show that mature spatiotemporal receptive field properties of retinal ganglion cells emerge from initially highly anisotropic properties, which may reflect an immature, polarized dendritic layout. Their maturation might be mediated by dendritic outgrowth and strengthening of excitatory synaptic connections, which could be induced by spontaneous activity and driven to maturation by exposure to light at birth. Mature directional selectivity seems to require visual experience or the late establishment of a specialized inhibitory synaptic drive.