Following the Ontogeny of Retinal Waves: Pan-Retinal Recordings of Population Dynamics in the Neonatal Mouse

Abstract The immature retina generates spontaneous waves of spiking activity that sweep across the ganglion cell layer during a limited developmental period, before the onset of visual experience. The spatiotemporal patterns encoded in the waves are believed to be instructive for the wiring of functional connections throughout the visual system. However, the ontogeny of retinal waves is still poorly documented due to relatively low resolution of conventional recording techniques. Here, we have characterized the spatiotemporal features of mouse retinal waves from birth until eye opening with unprecedented detail using a large-scale, dense 4,096-channel multielectrode array that allowed us to record from the entire neonatal retina at near cellular resolution. We found that early cholinergic waves propagate with random trajectories over large areas with low ganglion cell recruitment. They become slower, smaller and denser when GABAA signalling matures, beyond postnatal day (P) 7. Glutamatergic influences dominate from P10, coinciding with profound changes in activity dynamics. At that time waves cease to be random, beginning to show repetitive trajectories confined to a few localised hotspots. These hotspots gradually tile the retina with time, and disappear after eye opening. Our observations demonstrate that retinal waves undergo major spatiotemporal changes during ontogeny. Our results support the hypothesis that cholinergic waves guide the refinement of retinal targets while glutamatergic waves may also support the wiring of retinal receptive fields.