A stochastic neuronal model predicts random search behaviors at multiple spatial scales in C. elegans
Abstract
Random search is a behavioral strategy used by organisms from bacteria to humans to locate food that is randomly distributed and undetectable at a distance. We investigated this behavior in the nematode Caenorhabditis elegans, an organism with a small, well-described nervous system. Here we formulate a mathematical model of random search abstracted from the C. elegans connectome and fit to a large-scale kinematic analysis of C. elegans behavior at submicron resolution. The model predicts behavioral effects of neuronal ablations and genetic perturbations, as well as unexpected aspects of wild type behavior. The predictive success of the model indicates that random search in C. elegans can be understood in terms of a neuronal flip-flop circuit involving reciprocal inhibition between two populations of stochastic neurons. Our findings establish a unified theoretical framework for understanding C. elegans locomotion and a testable neuronal model of random search that can be applied to other organisms.
Additional Information
© 2016 Roberts et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 26 October 2015. Accepted: 19 January 2016. Published: 29 January 2016. This research was supported by a grant MH051383 from the National Institute of Mental Health to SRL. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Author contributions: WMR, Modeling, Conception and design, Analysis and interpretation of data, Drafting or revising the article; SBA, Design and construction of tracking system, Acquisition of data; KJL, RAL, MCB, Behavior, Acquisition of data; THL, Electrophysiology, Acquisition of data; TRT, Neuronal ablations, Acquisition of data; EJI, Chemotaxis simulations, Analysis and interpretation of data; SF, Spotted worm tracking method, Acquisition of data; NP, CIB, Molecular biology, Contributed unpublished essential data or reagents; SRL, Modeling, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article.Attached Files
Published - elife-12572-v2.pdf
Accepted Version - eLife.12572.full.pdf
Supplemental Material - elife-12572-fig1-v2-download.jpg
Supplemental Material - elife-12572-fig2-v2-download.jpg
Supplemental Material - elife-12572-fig3-v2-download.jpg
Supplemental Material - elife-12572-fig4-v2-download.jpg
Supplemental Material - elife-12572-fig5-v2-download.jpg
Supplemental Material - elife-12572-fig6-v2-download.jpg
Supplemental Material - elife-12572-fig7-v2-download.jpg
Supplemental Material - elife-12572-fig8-v2-download.jpg
Supplemental Material - elife-12572-fig9-v2-download.jpg
Supplemental Material - elife-12572-media1.mp4
Supplemental Material - elife-12572-media2.mp4
Supplemental Material - elife-12572-media3.mp4
Supplemental Material - elife-12572-media4.mp4
Files
Name | Size | Download all |
---|---|---|
md5:35e03dbfc57e438f3e046a33dcad7353
|
4.4 MB | Preview Download |
md5:1f26f1fbe42bdb5b1c9ca82cd610a3d4
|
267.5 kB | Preview Download |
md5:eaf37a119c6856ceb141c5526724005d
|
384.8 kB | Preview Download |
md5:67e2c4f05e29c7e47b37683998b7120e
|
232.0 kB | Preview Download |
md5:4527601a95611cdb39054176b105d20f
|
1.5 MB | Download |
md5:8a455a6bf5a326bb2ac74261751f899b
|
1.6 MB | Download |
md5:a6be76ed537bbddd5ed1812de6e68967
|
1.4 MB | Download |
md5:a5d9ef5ebe8acd80e74d68148a4e0f77
|
1.4 MB | Download |
md5:84f2c8238ca3c34ed1228a6af6b0dfd3
|
8.6 MB | Preview Download |
md5:d877ea32c3c3210d34b25724553dd3e9
|
409.0 kB | Preview Download |
md5:d0b5308337dfe028e9c4f6f5b2c70d81
|
513.7 kB | Preview Download |
md5:4b83d590870101ba6fa2aaa3902c615b
|
70.5 kB | Preview Download |
md5:4d0f557a9cd8f15e5acf5ae59659cf3d
|
239.1 kB | Preview Download |
md5:0fc1ba0a2abe3cb59506122f9e731779
|
300.5 kB | Preview Download |
md5:0a03f3f23ada1479a4e4f47f44010287
|
292.2 kB | Preview Download |
Additional details
- Eprint ID
- 64302
- Resolver ID
- CaltechAUTHORS:20160208-110258933
- MH051383
- National Institute of Mental Health (NIMH)
- Created
-
2016-02-08Created from EPrint's datestamp field
- Updated
-
2023-06-02Created from EPrint's last_modified field