Limited synapse overproduction can speed development but sometimes with long-term energy and discrimination penalties

Neural circuit development requires that synapses be formed between appropriate neurons. In addition, for a hierarchical network, successful development involves a sequencing of developmental events. It has been suggested that one mechanism that helps speed up development of proper connections is an early overproduction of synapses. Using a computational model of synapse development, such as adaptive synaptogenesis, it is possible to study such overproduction and its role in speeding up development; it is also possible to study other outcomes of synapse overproduction that are seemingly new to the literature. With a fixed number of neurons, adaptive synaptogenesis can control the speed of synaptic development in two ways: by altering the rate constants of the adaptive processes or by altering the initial number of rapidly but non-selectively accrued synapses. Using either mechanism, the simulations reveal that synapse overproduction appears as an unavoidable concomitant of rapid adaptive synaptogenesis. However, the shortest development times, which always produces the greatest amount of synapse overproduction, reduce adult performance by three measures: energy use, discrimination error rates, and proportional neuron allocation. Thus, the results here lead to the hypothesis that the observed speed of neural network development represents a particular inter-generational compromise: quick development benefits parental fecundity while slow development benefits offspring fecundity.Author summary: The brain processes information by building and adjusting neural connections, and as an organism learns about the environment, it incorporates associations between features of the environment into these adjustable connections. Organisms, however, are not born with these connections; synapses must develop from a connectionless set of neurons. An important aspect of normal brain development is the timely development of the brain and of hierarchically arranged brain regions. In this paper, we show that an unsupervised algorithm, called adaptive synaptogenesis, builds neurons with stable connections and allows these neurons to appropriately discriminate patterns. Here, we show that larger rates of synaptogenesis and synaptic modification speed up development of stable connections. However, such a speed-up produces larger, steady-state energy-costs. We conjecture that these synaptic modification rates have evolved as a compromise via natural selection. In this regard, the evolution-theoretic idea of parent-offspring conflict arises as a developmental consideration; that is, time to stable connectivity must balance with subsequent neural performance. Importantly, we illustrate that the widely-observed phenomenon of synapse overproduction during development can be understood as a compromise between speedy and efficient development.