Abstract
The functional organization of the mammalian retina is not spatially uniform. These functional inhomogenities presumably represent adaptations to specific visual needs associated with particular ecological benefits. However, how such asymmetries develop has not been documented yet. Here we present the ontogeny of light responses in mouse RGCs from eye opening to adulthood. Using a large-scale, high-density multielectrode array, we were able to record simultaneously from hundreds to thousands of dorsal and ventral RGCs, documenting light response properties (firing peak amplitude, time to peak and response duration) for the three major RGC types (ON, OFF, ON-OFF). Responses to different contrasts not only revealed a complex developmental profile for all three RGC types, but also unveiled differences between RGCs located in the dorsal versus ventral retina. At eye-opening, dorsal RGCs of all types were significantly more responsive to light, perhaps indicating an ecological advantage to nest viewing for young, pre-weaning pups. At the same time, the developmental profile of ON and OFF RGCs exhibited antagonistic behavior, with the strongest ON responses shortly after eye-opening, followed by an increase in the strength of OFF responses at later stages. We estimated RGC receptive field sizes and polarity across development using a novel super-resolution approach based on white noise and spike-triggered average (STA) responses and found that receptive field centers decrease but STA strength increases with maturation. These results show for the first time that the refinement of developing RGC responses to light is also not spatially uniform across the retina.
Significance Statement (120 maximum) Using a large-scale, high-density multielectrode array, we have investigated the ontogeny of light responses in retinal ganglion cells (RGCs) in the developing mouse retina. We were able to record from hundreds to thousands of RGCs simultaneously at pan-retinal level, and found that the refinement of receptive field properties strikingly differs between RGCs in the dorsal and ventral retina, with stronger ON and generally more prominent responses in the dorsal retina immediately after eye opening, followed by an increase in OFF responses. These findings suggest that retinal functionality is not spatially uniform and that there might be an ecological advantage to favoring the development of dorsal light responses before the rest of the retina reaches functional maturity.
Conflict of Interest The authors declare no competing financial interests.
