Retinal waves in adaptive rewiring networks orchestrate convergence and divergence in the visual system.

Abstract

Spontaneous retinal wave activity shaping the visual system is a complex neurodevelopmental phenomenon. Retinal ganglion cells are the hubs through which activity diverges throughout the visual system. We consider how these divergent hubs emerge, using an adaptively rewiring neural network model. Adaptive rewiring models show in a principled way how brains could achieve their complex topologies. Modular small-world structures with rich-club effects and circuits of convergent-divergent units emerge as networks evolve, driven by their own spontaneous activity. Arbitrary nodes of an initially random model network were designated as retinal ganglion cells. They were intermittently exposed to the retinal waveform, as the network evolved through adaptive rewiring. A significant proportion of these nodes developed into divergent hubs within the characteristic complex network architecture. The proportion depends parametrically on the wave incidence rate. Higher rates increase the likelihood of hub formation, while increasing the potential of ganglion cell death. In addition, direct neighbors of designated ganglion cells differentiate like amacrine cells. The divergence observed in ganglion cells resulted in enhanced convergence downstream, suggesting that retinal waves control the formation of convergence in the lateral geniculate nuclei. We conclude that retinal waves stochastically control the distribution of converging and diverging activity in evolving complex networks.