Addition of new neurons and the emergence of a local neural circuit for precise timing

During development, neurons arrive at local brain areas in extended period of time, but how they form local neural circuits is unknown. Here we computationally model the emergence of a network for precise timing in the premotor nucleus HVC in songbird. We show that new motor projection neurons, mostly added to HVC before and during song learning, are recruited to the end of a growing feedforward network. High spontaneous activity of new neurons makes them the prime targets for recruitment in a self-organized process via synaptic plasticity. Once recruited, the new neurons fire readily at precise times, and they become mature. Neurons that are not recruited become silent and replaced by new immature neurons. Our model incorporates realistic HVC features such as interneurons, spatial distributions of neurons, and distributed axonal delays. The model predicts that the birth order of the projection neurons correlates with their burst timing during the song. Significance StatementFunctions of local neural circuits depend on their specific network structures, but how the networks are wired is unknown. We show that such structures can emerge during development through a self-organized process, during which the network is wired by neuron-by-neuron recruitment. This growth is facilitated by steady supply of immature neurons, which are highly excitable and plastic. We suggest that neuron maturation dynamics is an integral part of constructing local neural circuits.