Neural circuit mechanisms underlying context-specific halting in Drosophila

Walking is a complex motor programme involving coordinated and distributed activity across the brain and the spinal cord. Halting appropriately at the correct time is a critical component of walking control. Despite progress in identifying neurons driving halting 1 – 6 , the underlying neural circui...

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Published in:	Nature (London) Vol. 634; no. 8032; pp. 191 - 200
Main Authors:	Sapkal, Neha, Mancini, Nino, Kumar, Divya Sthanu, Spiller, Nico, Murakami, Kazuma, Vitelli, Gianna, Bargeron, Benjamin, Maier, Kate, Eichler, Katharina, Jefferis, Gregory S. X. E., Shiu, Philip K., Sterne, Gabriella R., Bidaye, Salil S.
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 03-10-2024 Nature Publishing Group
Subjects:	14/19 14/69 631/378/116/1925 631/378/2629/1779 631/378/2632/1823 631/378/3920 64/24 Animals Brain Brain - cytology Brain - physiology Cholinergic Neurons - physiology Cholinergics Connectome Context Critical components Drosophila Drosophila melanogaster - cytology Drosophila melanogaster - physiology Feeding Behavior - physiology Female Fruit flies GABAergic Neurons - physiology Genotype & phenotype Grooming Grooming - physiology Humanities and Social Sciences Insects Models, Neurological Motor task performance multidisciplinary Neural Pathways - cytology Neural Pathways - physiology Neurons Science Science (multidisciplinary) Spinal cord Spinal Cord - cytology Spinal Cord - physiology Velocity Walking Walking - physiology γ-Aminobutyric acid
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Summary:	Walking is a complex motor programme involving coordinated and distributed activity across the brain and the spinal cord. Halting appropriately at the correct time is a critical component of walking control. Despite progress in identifying neurons driving halting 1 – 6 , the underlying neural circuit mechanisms responsible for overruling the competing walking state remain unclear. Here, using connectome-informed models 7 – 9 and functional studies, we explain two fundamental mechanisms by which Drosophila implement context-appropriate halting. The first mechanism (‘walk-OFF’) relies on GABAergic neurons that inhibit specific descending walking commands in the brain, whereas the second mechanism (‘brake’) relies on excitatory cholinergic neurons in the nerve cord that lead to an active arrest of stepping movements. We show that two neurons that deploy the walk-OFF mechanism inhibit distinct populations of walking-promotion neurons, leading to differential halting of forward walking or turning. The brake neurons, by constrast, override all walking commands by simultaneously inhibiting descending walking-promotion neurons and increasing the resistance at the leg joints. We characterized two behavioural contexts in which the distinct halting mechanisms were used by the animal in a mutually exclusive manner: the walk-OFF mechanism was engaged for halting during feeding and the brake mechanism was engaged for halting and stability during grooming. Two halting mechanisms, ‘walk-OFF’ and ‘brake’, are shown to be engaged by distinct neural circuits in Drosophila , in a context dependent manner.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	0028-0836 1476-4687 1476-4687
DOI:	10.1038/s41586-024-07854-7