Circuit remodeling during development shapes the human foveal midget connectome for high visual acuity.

In the human fovea, the midget circuitry shows a 'private-line' design, which contributes to the high visual acuity by preserving visual signals at single-cone resolution. Each foveal midget ganglion cell is often contacted by a midget bipolar cell that receives input from a single cone photoreceptor. Developmental strategies creating the private-line are unknown. The connectivity could be rapidly set up with extreme precision as early as synaptogenesis or, by contrast, gradually shaped in concordance with the maturation of foveal architecture and visual sensitivity. To test these hypotheses, we reconstructed the developing midget circuitry in the fetal human fovea using block-face serial electron microscopy. The results suggest that the foveal midget circuitry requires synaptic remodeling to reach the non-divergent connectivity. The circuitry is sculpted from excessive convergent and divergent connections early in fetal life, to each midget bipolar cell contacting a single cone by mid-gestation. The bipolar cell - ganglion cell connectivity undergoes a more protracted period of refinement.