Abstract
The nematode Caenorhabditis elegans, with information on neural connectivity, three-dimensional position and cell linage, provides a unique system for understanding the development of neural networks. Although C. elegans has been widely studied in the past, we present the first statistical study from a developmental perspective, with findings that raise interesting suggestions on the establishment of long-distance connections and network hubs. Here, we analyze the neuro-development for temporal and spatial features, using birth times of neurons and their three-dimensional positions. Comparisons of growth in C. elegans with random spatial network growth highlight two findings relevant to neural network development. First, most neurons which are linked by long-distance connections are born around the same time and early on, suggesting the possibility of early contact or interaction between connected neurons during development. Second, early-born neurons are more highly connected (tendency to form hubs) than later-born neurons. This indicates that the longer time frame available to them might underlie high connectivity. Both outcomes are not observed for random connection formation. The study finds that around one-third of electrically coupled long-range connections are late forming, raising the question of what mechanisms are involved in ensuring their accuracy, particularly in light of the extremely invariant connectivity observed in C. elegans. In conclusion, the sequence of neural network development highlights the possibility of early contact or interaction in securing long-distance and high-degree connectivity.
Highlights
The complexity of the nervous system continues to protract efforts to understand its development
The relatively simple invertebrate neural systems have been the subject of intense study in the last few decades [1], helping to shed light on mechanisms involved in development like axon guidance and molecular cues
We looked at spatial network features in particular focusing on the onset of short, medium, and long distance connection-pairs
Summary
The complexity of the nervous system continues to protract efforts to understand its development. We looked at the development of the neuronal network of C. elegans using information from 279 of the 302 neurons (see methods and [2]). Our work marks the first attempt to computationally and statistically represent the neural development of C. elegans based on available biological data, enabling a spatio-temporal analysis of the developing neuronal network. Graph theory [7] is increasingly being applied to elucidate the function based on the structures of complex networks like the brain [8,9] and here we carry out a structural analysis of neuronal networks during different stages of C. elegans development. We observe neuronal growth (see Video S1), development times of different classes of neurons, and the time windows for establishing short- and long-distance connectivity
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