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

PLoS Comput Biol. 2017 Sep 22;13(9):e1005750. doi: 10.1371/journal.pcbi.1005750. eCollection 2017 Sep.

Abstract

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.

MeSH terms

  • Computational Biology
  • Computer Simulation*
  • Models, Neurological*
  • Nerve Net / physiology*
  • Neurons / physiology*
  • Synapses / physiology*

Grants and funding

Funded by the National Science Foundation (www.nsf.gov), grant number 1162449 to Toby Berger & William B Levy. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.