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Central processing of leg proprioception in Drosophila

Central processing of leg proprioception in Drosophila
Central processing of leg proprioception in Drosophila

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.

Animals, Biomechanical Phenomena, Drosophila melanogaster, Feedback, Sensory/physiology, Hindlimb/innervation, Muscle, Skeletal/innervation, Neural Pathways/cytology, Proprioception/physiology, Sensory Receptor Cells/cytology
2050-084X
Agrawal, Sweta
f593de73-fb03-4c0c-88e9-81f87b5cb3e3
Dickinson, Evyn S
fdedff83-0919-42e9-b90a-917e3ddf3514
Sustar, Anne
505e9e21-9868-4e15-83dc-a0912c87b9bf
Gurung, Pralaksha
1bd56922-fa8f-4339-898a-1c1412f9df1c
Shepherd, David
11aa6858-d19c-4450-82ff-11dff9dcd9c4
Truman, James W
558a187a-bf3a-4ffd-a6a4-c1f8449f5938
Tuthill, John C
4f1cc976-9e58-4af9-abc2-a7c0c3689e2a
Agrawal, Sweta
f593de73-fb03-4c0c-88e9-81f87b5cb3e3
Dickinson, Evyn S
fdedff83-0919-42e9-b90a-917e3ddf3514
Sustar, Anne
505e9e21-9868-4e15-83dc-a0912c87b9bf
Gurung, Pralaksha
1bd56922-fa8f-4339-898a-1c1412f9df1c
Shepherd, David
11aa6858-d19c-4450-82ff-11dff9dcd9c4
Truman, James W
558a187a-bf3a-4ffd-a6a4-c1f8449f5938
Tuthill, John C
4f1cc976-9e58-4af9-abc2-a7c0c3689e2a

Agrawal, Sweta, Dickinson, Evyn S, Sustar, Anne, Gurung, Pralaksha, Shepherd, David, Truman, James W and Tuthill, John C (2020) Central processing of leg proprioception in Drosophila. eLife, 9. (doi:10.7554/eLife.60299).

Record type: Article

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.

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More information

Accepted/In Press date: 2 December 2020
Published date: 2 December 2020
Keywords: Animals, Biomechanical Phenomena, Drosophila melanogaster, Feedback, Sensory/physiology, Hindlimb/innervation, Muscle, Skeletal/innervation, Neural Pathways/cytology, Proprioception/physiology, Sensory Receptor Cells/cytology

Identifiers

Local EPrints ID: 455669
URI: http://eprints.soton.ac.uk/id/eprint/455669
ISSN: 2050-084X
PURE UUID: 1e7e83e3-7976-477f-a6a2-e368ffa763db

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Date deposited: 30 Mar 2022 16:43
Last modified: 30 Mar 2022 16:46

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Contributors

Author: Sweta Agrawal
Author: Evyn S Dickinson
Author: Anne Sustar
Author: Pralaksha Gurung
Author: David Shepherd
Author: James W Truman
Author: John C Tuthill

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