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New Research, Sensory and Motor Systems

A gate-and-switch model for head orientation behaviors in C. elegans

Marie-Hélène Ouellette, Melanie J. Desrochers, Ioana Gheta, Ryan Ramos and Michael Hendricks
eNeuro 20 November 2018, ENEURO.0121-18.2018; DOI: https://doi.org/10.1523/ENEURO.0121-18.2018
Marie-Hélène Ouellette
1Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada
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Melanie J. Desrochers
1Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada
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Ioana Gheta
1Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada
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Ryan Ramos
1Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada
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Michael Hendricks
1Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada
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Abstract

The nervous system seamlessly integrates perception and action. This ability is essential for stable representation of and appropriate responses to the external environment. How the sensorimotor integration underlying this ability occurs at the level of individual neurons is of keen interest. In C. elegans, RIA interneurons receive input from sensory pathways and have reciprocal connections with head motor neurons. RIA simultaneously encodes both head orientation and sensory stimuli, which may allow it to integrate these two signals to detect the spatial distribution of stimuli across head sweeps and generate directional head responses. Here, we show that blocking synaptic release from RIA disrupts head orientation behaviors in response to unilaterally presented stimuli. We found that sensory encoding in RIA is gated according to head orientation. This dependence on head orientation is independent of motor encoding in RIA, suggesting a second, posture-dependent pathway upstream of RIA. This gating mechanism may allow RIA to selectively attend to stimuli that are asymmetric across head sweeps. Attractive odor removal during head bends triggers rapid head withdrawal in the opposite direction. Unlike sensory encoding, this directional response is dependent on motor inputs to and synaptic output from RIA. Together, these results suggest that RIA is part of a sensorimotor pathway that is dynamically regulated according to head orientation at two levels: the first is a gate that filters sensory representations in RIA, and the second is a switch that routes RIA synaptic output to dorsal or ventral head motor neurons.

Significance statement Simple head orientation behaviors in C. elegans provide an opportunity to dissect sensorimotor integration at the cellular and subcellular levels. We describe a single interneuron that coordinates posture, sensation, and movement to detect the spatial distribution of stimuli and direct motor output to guide navigation behavior. Our findings underscore the fundamental role of neural mechanisms for integrating sensory input into ongoing behavior.

  • behaviour
  • C. elegans
  • calcium signalling
  • sensorimotor integration

Footnotes

  • Authors report no conflict of interest.

  • M.H., M-H.O., and M.J.D. designed the research. All authors performed research and analyzed data. M.H. and M-H.O. wrote the paper.

  • Funding sources This work was supported by funding from McGill University to M.H. and M-H.O., the National Science and Engineering Research Council (NSERC) to M.H. (RGPIN/05117-2014), the Canadian Foundation for Innovation (CFI) to M.H. (32581), and the Canada Research Chairs Program to M.H. (950-231541).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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A gate-and-switch model for head orientation behaviors in C. elegans
Marie-Hélène Ouellette, Melanie J. Desrochers, Ioana Gheta, Ryan Ramos, Michael Hendricks
eNeuro 20 November 2018, ENEURO.0121-18.2018; DOI: 10.1523/ENEURO.0121-18.2018

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A gate-and-switch model for head orientation behaviors in C. elegans
Marie-Hélène Ouellette, Melanie J. Desrochers, Ioana Gheta, Ryan Ramos, Michael Hendricks
eNeuro 20 November 2018, ENEURO.0121-18.2018; DOI: 10.1523/ENEURO.0121-18.2018
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Keywords

  • behaviour
  • C. elegans
  • calcium signalling
  • sensorimotor integration

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