Corollary discharge promotes a sustained motor state in a neural circuit for navigation
- Harvard University, United States
- Mount Sinai Hospital, Canada
- University of Massachusetts Medical School, United States
Abstract
Animals exhibit behavioral and neural responses that persist on longer time scales than transient or fluctuating stimulus inputs. Here, we report that C. elegans uses feedback from the motor circuit to a sensory processing interneuron to sustain its motor state during thermotactic navigation. By imaging circuit activity in behaving animals, we show that a principal postsynaptic partner of the AFD thermosensory neuron, the AIY interneuron, encodes both temperature and motor state information. By optogenetic and genetic manipulation of this circuit, we demonstrate that the motor state representation in AIY is a corollary discharge signal. RIM, an interneuron that is connected with premotor interneurons, is required for this corollary discharge. Ablation of RIM eliminates the motor representation in AIY, allows thermosensory representations to reach downstream premotor interneurons, and reduces the animal's ability to sustain forward movements during thermotaxis. We propose that feedback from the motor circuit to the sensory processing circuit underlies a positive feedback mechanism to generate persistent neural activity and sustained behavioral patterns in a sensorimotor transformation.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1-6. Source code has been provided for Figure 7.
Article and author information
Author details
Vivek Venkatachalam
Hillary Denise Rodgers
Aravinthan DT Samuel
Funding
National Institute of Neurological Disorders and Stroke (NS082525-01A1)
- Aravinthan DT Samuel
National Institute of General Medical Sciences (PO1 GM103770)
- Aravinthan DT Samuel
National Institute of General Medical Sciences (RO1 GM084491)
- Mark J Alkema
Burroughs Wellcome Fund
- Vivek Venkatachalam
Canadian Institutes of Health Research (154274)
- Mei Zhen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Manuel Zimmer, Research Institute of Molecular Pathology, Vienna Biocenter and University of Vienna, Austria
Version history
- Received: March 27, 2021
- Accepted: April 8, 2021
- Accepted Manuscript published: April 21, 2021 (version 1)
- Accepted Manuscript updated: April 22, 2021 (version 2)
- Version of Record published: May 21, 2021 (version 3)
Copyright
© 2021, Ji et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Corollary discharge promotes a sustained motor state in a neural circuit for navigation
eLife 10:e68848.
https://doi.org/10.7554/eLife.68848
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