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Network control principles predict neuron function in the Caenorhabditis elegans connectome

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Yan, Gang 
Vértes, Petra E 
Towlson, Emma K 
Chew, Yee Lian 
Walker, Denise S 


Recent studies on the controllability of complex systems offer a powerful mathematical framework to systematically explore the structure-function relationship in biological, social, and technological networks. Despite theoretical advances, we lack direct experimental proof of the validity of these widely used control principles. Here we fill this gap by applying a control framework to the connectome of the nematode Caenorhabditis elegans, allowing us to predict the involvement of each C. elegans neuron in locomotor behaviours. We predict that control of the muscles or motor neurons requires 12 neuronal classes, which include neuronal groups previously implicated in locomotion by laser ablation, as well as one previously uncharacterized neuron, PDB. We validate this prediction experimentally, finding that the ablation of PDB leads to a significant loss of dorsoventral polarity in large body bends. Importantly, control principles also allow us to investigate the involvement of individual neurons within each neuronal class. For example, we predict that, within the class of DD motor neurons, only three (DD04, DD05, or DD06) should affect locomotion when ablated individually. This prediction is also confirmed; single cell ablations of DD04 or DD05 specifically affect posterior body movements, whereas ablations of DD02 or DD03 do not. Our predictions are robust to deletions of weak connections, missing connections, and rewired connections in the current connectome, indicating the potential applicability of this analytical framework to larger and less well-characterized connectomes.



Animals, Caenorhabditis elegans, Connectome, Lasers, Locomotion, Motor Neurons, Nerve Net, Neurons

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Medical Research Council (MR/K020706/1)
We thank M. Angulo, J. Gao, Y.-Y. Liu, J.-J. Slotine, K. Albrecht, S. P. Cornelius and A. Li for valuable discussions and L. Grundy, A. Brown and E. Yemini for help with analysis of tracking data. We are grateful to V. Butler and the Caenorhabditis Genetics Center, which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440), for C. elegans strains. This work is supported by the John Templeton Foundation: Mathematical and Physical Sciences grant number PFI-777; European Commission grant number 641191 (CIMPLEX); MRC grant number MC-A023-5PB91; Wellcome Trust grant number WT103784MA. P.E.V. is supported by the Medical Research Council grant number MR/K020706/1. Y.L.C. is supported by an EMBO Long Term Fellowship.