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

Xiangsunze Zeng, Yuko Komanome, Tappei Kawasaki, Kengo Inada, Julius Jonaitis, Stefan R. Pulver, Hokto Kazama, Akinao Nose*

*Corresponding author for this work

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Abstract

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.
Original languageEnglish
JournalCurrent Biology
VolumeIn press
Early online date18 Oct 2021
DOIs
Publication statusE-pub ahead of print - 18 Oct 2021

Keywords

  • Central pattern generator
  • Motor development
  • Proprioceptive feedback
  • Gap junction
  • Pacemaking activity

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