Cell Volume 179, ISSUE 2, P355-372.e23, October 03, 2019
Single-Cell Reconstruction of Emerging Population Activity in an Entire Developing Circuit
Single-Cell Reconstruction of Emerging Population Activity in an Entire Developing Circuit
Yinan Wan, Ziqiang Wei, Loren L. Looger, Minoru Koyama, Shaul Druckmann, Philipp J. Keller
Highlights
• Neurons are tracked from birth to entire circuit at cell-type and functional levels
• Neurogenesis and emergence of coordinated activity is analyzed at a single-cell level
• Motoneurons, active first, form ensembles that synchronize globally, based on size
• Neuron maturation is stereotyped, based on birth time and anatomical origin
Summary
Animal survival requires a functioning nervous system to develop during embryogenesis. Newborn neurons must assemble into circuits producing activity patterns capable of instructing behaviors. Elucidating how this process is coordinated requires new methods that follow maturation and activity of all cells across a developing circuit. We present an imaging method for comprehensively tracking neuron lineages, movements, molecular identities, and activity in the entire developing zebrafish spinal cord, from neurogenesis until the emergence of patterned activity instructing the earliest spontaneous motor behavior. We found that motoneurons are active first and form local patterned ensembles with neighboring neurons. These ensembles merge, synchronize globally after reaching a threshold size, and finally recruit commissural interneurons to orchestrate the left-right alternating patterns important for locomotion in vertebrates. Individual neurons undergo functional maturation stereotypically based on their birth time and anatomical origin. Our study provides a general strategy for reconstructing how functioning circuits emerge during embryogenesis.
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