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Chromatic neuronal jamming in a primitive brain

Nature Physics volume 16, pages 553–557 (2020)Cite this article

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Abstract

Jamming models developed in inanimate matter have been widely used to describe cell packing in tissues1,2,3,4,5,6,7, but predominantly neglect cell diversity, despite its prevalence in biology. Most tissues, animal brains in particular, comprise a mix of many cell types, with mounting evidence suggesting that neurons can recognize their respective types as they organize in space8,9,10,11. How cell diversity revises the current jamming paradigm is unknown. Here, in the brain of the flatworm planarian Schmidtea mediterranea, which exhibits remarkable tissue plasticity within a simple, quantifiable nervous system12,13,14,15,16, we identify a distinct packing state, ‘chromatic’ jamming. Combining experiments with computational modelling, we show that neurons of distinct types form independent percolating networks barring any physical contact. This jammed state emerges as cell packing configurations become constrained by cell type-specific interactions and therefore may extend to describe cell packing in similarly complex tissues composed of multiple cell types.

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Fig. 1: The planarian brain allows quantification of neuronal packing with single-neuron resolution.
Fig. 2: Neuronal packing exhibits geometric hallmarks of jamming.
Fig. 3: A chromatic jamming model for neuronal packing.

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Data availability

The datasets generated and analysed within this study can be downloaded from https://github.com/xianshine/cJamming or are available from the corresponding authors on request.

Code availability

Analysis and simulation codes are available for public access on GitHub (https://github.com/xianshine/cJamming).

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Acknowledgements

We thank Kejia Chen and Ke Chen for help with data analysis, R.H. Roberts-Galbraith and J.J. Collins III for experimental assistance during the early phase of this study and S. Granick, I. Riedel-Kruse, D.M. Sussman and P.N. Newmark for discussions. Plasmids that contain the planarian neuropeptide genes were provided by J.J. Collins III. This work is supported by the Burroughs Wellcome Fund through the CASI programme to B.W.

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Author notes

  1. These authors contributed equally: Margarita Khariton, Xian Kong.

Authors and Affiliations

  1. Department of Bioengineering, Stanford University, Stanford, CA, USA

    Margarita Khariton & Bo Wang

  2. Department of Chemical Engineering, Stanford University, Stanford, CA, USA

    Xian Kong & Jian Qin

  3. Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA, USA

    Bo Wang

Authors
  1. Margarita Khariton
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  2. Xian Kong
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  3. Jian Qin
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Contributions

J.Q. and B.W. designed the research, M.K. and B.W. performed the experiments, M.K., X.K. and B.W. analysed the data, X.K. performed the simulation, X.K. and J.Q. analysed the simulation results and all authors wrote the paper.

Corresponding authors

Correspondence to Jian Qin or Bo Wang.

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The authors declare no competing interests.

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Peer review information Nature Physics thanks Corey O’Hern and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Figs. 1–9, note and references.

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Khariton, M., Kong, X., Qin, J. et al. Chromatic neuronal jamming in a primitive brain. Nat. Phys. 16, 553–557 (2020). https://doi.org/10.1038/s41567-020-0809-9

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