Central processing of leg proprioception in Drosophila
- University of Washington, United States
- Bangor University, United Kingdom
- Janelia Research Campus, Howard Hughes Medical Institute, United States
Abstract
Proprioception, the sense of self-movement and position, is mediated by mechanosensory neurons that detect diverse features of body kinematics. Although proprioceptive feedback is crucial for accurate motor control, little is known about how downstream circuits transform limb sensory information to guide motor output. Here, we investigate neural circuits in Drosophila that process proprioceptive information from the fly leg. We identify three cell-types from distinct developmental lineages that are positioned to receive input from proprioceptor subtypes encoding tibia position, movement, and vibration. 13Bα neurons encode femur-tibia joint angle and mediate postural changes in tibia position. 9Aα neurons also drive changes in leg posture, but encode a combination of directional movement, high frequency vibration, and joint angle. Activating 10Bα neurons, which encode tibia vibration at specific joint angles, elicits pausing in walking flies. Altogether, our results reveal that central circuits integrate information across proprioceptor subtypes to construct complex sensorimotor representations that mediate diverse behaviors, including reflexive control of limb posture and detection of leg vibration.
Data availability
Data made freely available on Dryad (doi:10.5061/dryad.k3j9kd55t).
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Central processing of leg proprioception in Drosophila: physiology and behavior dataDryad Digital Repository, doi:10.5061/dryad.k3j9kd55t.
Article and author information
Author details
Funding
National Institutes of Health (R01NS102333)
- Sweta Agrawal
- Evyn S Dickinson
- Anne Sustar
- Pralaksha Gurung
- John C Tuthill
Howard Hughes Medical Institute
- David Shepherd
- James W Truman
Pew Charitable Trusts (Scholar Award)
- Sweta Agrawal
- Evyn S Dickinson
- Anne Sustar
- Pralaksha Gurung
- John C Tuthill
Searle Scholars Program (Scholar Award)
- Sweta Agrawal
- Evyn S Dickinson
- Anne Sustar
- Pralaksha Gurung
- John C Tuthill
Alfred P. Sloan Foundation (Scholar Award)
- Sweta Agrawal
- Evyn S Dickinson
- Anne Sustar
- Pralaksha Gurung
- John C Tuthill
McKnight Endowment Fund for Neuroscience (Scholar Award)
- Sweta Agrawal
- Evyn S Dickinson
- Anne Sustar
- Pralaksha Gurung
- John C Tuthill
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Ronald L Calabrese, Emory University, United States
Version history
- Received: June 22, 2020
- Accepted: December 1, 2020
- Accepted Manuscript published: December 2, 2020 (version 1)
- Version of Record published: December 21, 2020 (version 2)
Copyright
© 2020, Agrawal 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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Central processing of leg proprioception in Drosophila
eLife 9:e60299.
https://doi.org/10.7554/eLife.60299
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