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Mechanosensory stimulation triggers sustained local motor activity in Drosophila melanogaster

View ORCID ProfileAlexandra M. Medeiros, View ORCID ProfileAnna F. Hobbiss, Gonçalo Borges, View ORCID ProfileMarta Moita, View ORCID ProfileCésar S. Mendes
doi: https://doi.org/10.1101/2022.07.19.500315
Alexandra M. Medeiros
1iNOVA4Health, NOVA Medical School|Faculdade de Ciências Médicas, NMS|FCM, Universidade Nova de Lisboa; Lisbon, Portugal
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  • ORCID record for Alexandra M. Medeiros
Anna F. Hobbiss
1iNOVA4Health, NOVA Medical School|Faculdade de Ciências Médicas, NMS|FCM, Universidade Nova de Lisboa; Lisbon, Portugal
2Champalimaud Research, Champalimaud Center for the Unknown, Lisbon, Portugal
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Gonçalo Borges
1iNOVA4Health, NOVA Medical School|Faculdade de Ciências Médicas, NMS|FCM, Universidade Nova de Lisboa; Lisbon, Portugal
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Marta Moita
2Champalimaud Research, Champalimaud Center for the Unknown, Lisbon, Portugal
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César S. Mendes
1iNOVA4Health, NOVA Medical School|Faculdade de Ciências Médicas, NMS|FCM, Universidade Nova de Lisboa; Lisbon, Portugal
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  • For correspondence: cesar.mendes@nms.unl.pt
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Abstract

Most vertebrates and invertebrates such as Drosophila melanogaster are able to move in complex environments due to their ability to integrate sensory information along with motor commands. Mechanosensory structures exist along each leg to assist in motor coordination by transmitting external cues or proprioceptive information to motor centers in the central nervous system. Nevertheless, how different mechanosensory structures engage these locomotor centers and their underlying circuits remains poorly understood.

Here, we tested the role of mechanosensory structures in movement initiation by optogenetically stimulating specific classes of leg sensory structures. We found that stimulation of leg Mechanosensory Bristles (MsB) and femoral Chordotonal Organ (ChO) is sufficient to initiate forward movement in immobile animals. While the stimulation of the ChO required brain centers to induce forward movement, unexpectedly, brief stimulation of leg MsB triggered sustained cyclic motor activity dependent only on circuits within the Ventral Nerve Cord (VNC). The duration of the MsB-induced movement was dependent on the number of excited cells and specific to leg afferents, since stimulation of MsB in other segments lead to different motor outcomes. MsB-mediated movement lacked inter and intra-leg coordination, but preserved antagonistic muscle activity within joints. Our data shows that sensory stimulation can act in combination with descending commands in order to elicit a faster response to mechanical stimulation. In addition, it sheds light on the ability of specific sensory circuits to modulate motor control, including initiation of movement, presenting a new system to better understand how different levels of coordination are controlled by VNC and central brain locomotor circuits.

Significance Statement Sensory feedback is critical to allow smooth and stable locomotion. Proprioceptors interact directly with pre-motor centers optimizing and sustaining coordinated movement. However, initiation of moment is considered to be triggered by higher-order centers in the brain. Here we took advantage of the genetic toolkit provided by the fruit fly Drosophila melanogaster to optogenetically activate different classes of leg sensory cells in immobile animals. We found that leg mechanosensory bristles can specifically trigger sustained leg activity independently of higher-order centers as headless flies could sustain prolonged leg movement upon mechanosensory stimulation. Moreover, while this sensory-evoked movement lacks intra- and inter-leg coordination, it still preserved basic antagonistic muscle activity. These findings suggest a parallel mechanism to trigger fast movement upon sensory stimulation. In addition, it provides a new model for movement initiation and a point–of-entry to define pre-motor circuits.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵3 Lead contact

  • The updated manuscript has been revised and subjected to some minor alterations. We corrected some errors or inaccuracies that were identified during the initial review. We conducted some additional analysis, that provided us with new insights and strengthened our conclusions. Furthermore, we updated the title of our manuscript to better reflect the focus of our research. The new title is "Mechanosensory stimulation triggers sustained local motor activity in Drosophila melanogaster", which we believe more accurately captures the scope and implication or our study. Overall, these updates improved the readability and quality of the manuscript.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 08, 2023.
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Mechanosensory stimulation triggers sustained local motor activity in Drosophila melanogaster
Alexandra M. Medeiros, Anna F. Hobbiss, Gonçalo Borges, Marta Moita, César S. Mendes
bioRxiv 2022.07.19.500315; doi: https://doi.org/10.1101/2022.07.19.500315
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Mechanosensory stimulation triggers sustained local motor activity in Drosophila melanogaster
Alexandra M. Medeiros, Anna F. Hobbiss, Gonçalo Borges, Marta Moita, César S. Mendes
bioRxiv 2022.07.19.500315; doi: https://doi.org/10.1101/2022.07.19.500315

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