Self-organized emergence of modularity, hierarchy, and mirror reversals from competitive synaptic growth in a developmental model of the visual pathway

Abstract

A hallmark of the primate visual system is its architectural organization consisting of multiple distinct (modular) areas that connect hierarchically. These areas exhibit specific spatial organization on the cortical sheet, with primary visual cortex at the center and subsequent regions in the hierarchy encircling the earlier one, and detailed topological organization, with retinotopy in each area but striking mirror reversals across area boundaries. The developmental rules that drive the simultaneous formation of these architectural, spatial, and topographic aspects of organization are unknown. Here we demonstrate that a simple synaptic growth rule driven by spontaneous activity and heterosynaptic competition generates a detailed connectome of the visual pathway, with emergence of all three types of organization. We identify a theoretical principle -- local greedy wiring minimization via spontaneous drive (GWM-S) -- implemented by the mechanism, and use this insight to propose biologically distinct growth rules that predict similar endpoints but testably distinguishable developmental trajectories. The same rules predict how input geometry and cortical geometry together drive emergence of hierarchical, convolution-like, spatially and topographically organized sensory processing pathways for different modalities and species, providing a possible explanation for the observed pluripotency of cortical structure formation. We find that the few parameters governing structure emergence in the growth rule constitute simple knobs for rich control, that could (potentially genetically) encode a projection neuron-like connectivity patterns and interneuron-like ones. In all, the presented rules provide a parsimonious mechanistic model for the organization of sensory cortical hierarchies even without detailed genetic cues for features like map reversal, and provide numerous predictions for experiment during normal and perturbed development.