An electrically coupled pioneer circuit enables motor development via proprioceptive feedback in Drosophila embryos

• Published in: Current biology 2021-12, Vol.31 (23), p.5327-5340.e5
• Main Authors: Zeng, Xiangsunze, Komanome, Yuko, Kawasaki, Tappei, Inada, Kengo, Jonaitis, Julius, Pulver, Stefan R., Kazama, Hokto, Nose, Akinao
• Format: Article
• Language: English
• Subjects: Animals; central pattern generator; Drosophila; Feedback, Sensory; gap junction; Gap Junctions; Interneurons; motor development; Movement - physiology; pacemaking activity; proprioceptive feedback
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.10.005

Precocious movements are widely seen in embryos of various animal species. Whether such movements via proprioceptive feedback play instructive roles in motor development or are a mere reflection of activities in immature motor circuits is a long-standing question. Here we image the emerging motor activities in Drosophila embryos that lack proprioceptive feedback and show that proprioceptive experience is essential for the development of locomotor central pattern generators (CPGs). Downstream of proprioceptive inputs, we identify a pioneer premotor circuit composed of two pairs of segmental interneurons, whose gap-junctional transmission requires proprioceptive experience and plays a crucial role in CPG formation. The circuit autonomously generates rhythmic plateau potentials via IP3-mediated Ca2+ release from internal stores, which contribute to muscle contractions and hence produce proprioceptive feedback. Our findings demonstrate the importance of self-generated movements in instructing motor development and identify the cells, circuit, and physiology at the core of this proprioceptive feedback. [Display omitted] •Proprioceptive experience of precocious movements is required for CPG formation•Proprioception regulates gap junctions in a pioneer M/A27h circuit•M/A27h circuit generates spontaneous activities and ensuing precocious movements•M/A27h spontaneous activities are crucial for motor development Zeng et al. show that proprioceptive experience of precocious movements is indispensable for CPG formation and identify a pioneer M/A27h circuit as the target of proprioception. The M/A27h circuit generates spontaneous activity that contributes to precocious movements, revealing a loop essential for motor development.