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Nature. 2017 Oct 26;550(7677):519-523. doi: 10.1038/nature24056. Epub 2017 Oct 18.

Network control principles predict neuron function in the Caenorhabditis elegans connectome.

Author information

1
Center for Complex Network Research and Department of Physics, Northeastern University, Boston, Massachusetts 02115, USA.
2
School of Physics Science and Engineering, Tongji University, Shanghai 200092, China.
3
Department of Psychiatry, Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge CB2 0SZ, UK.
4
Division of Neurobiology, MRC Laboratory of Molecular Biology, Cambridge Biomedical Campus, Francis Crick Avenue, Cambridge CB2 0QH, UK.
5
Center for Cancer Systems Biology, Dana Farber Cancer Institute, Boston, Massachusetts 02115, USA.
6
Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA.
7
Center for Network Science, Central European University, H-1051 Budapest, Hungary.

Abstract

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.

PMID:
29045391
PMCID:
PMC5710776
DOI:
10.1038/nature24056
[Indexed for MEDLINE]
Free PMC Article

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