An injury-induced serotonergic neuron subpopulation contributes to axon regrowth and function restoration after spinal cord injury in zebrafish

Chun-Xiao Huang, Yacong Zhao, Jie Mao, Zhen Wang, Lulu Xu, Jianwei Cheng, Na N. Guan () and Jianren Song ()
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Chun-Xiao Huang: Tongji University
Yacong Zhao: Tongji University
Jie Mao: Tongji University
Zhen Wang: Tongji University
Lulu Xu: Tongji University
Jianwei Cheng: Tongji University
Na N. Guan: Tongji University
Jianren Song: Tongji University

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: Abstract Spinal cord injury (SCI) interrupts long-projecting descending spinal neurons and disrupts the spinal central pattern generator (CPG) that controls locomotion. The intrinsic mechanisms underlying re-wiring of spinal neural circuits and recovery of locomotion after SCI are unclear. Zebrafish shows axonal regeneration and functional recovery after SCI making it a robust model to study mechanisms of regeneration. Here, we use a two-cut SCI model to investigate whether recovery of locomotion can occur independently of supraspinal connections. Using this injury model, we show that injury induces the localization of a specialized group of intraspinal serotonergic neurons (ISNs), with distinctive molecular and cellular properties, at the injury site. This subpopulation of ISNs have hyperactive terminal varicosities constantly releasing serotonin activating 5-HT1B receptors, resulting in axonal regrowth of spinal interneurons. Axon regrowth of excitatory interneurons is more pronounced compared to inhibitory interneurons. Knock-out of htr1b prevents axon regrowth of spinal excitatory interneurons, negatively affecting coordination of rostral-caudal body movements and restoration of locomotor function. On the other hand, treatment with 5-HT1B receptor agonizts promotes functional recovery following SCI. In summary, our data show an intraspinal mechanism where a subpopulation of ISNs stimulates axonal regrowth resulting in improved recovery of locomotor functions following SCI in zebrafish.

Date: 2021
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DOI: 10.1038/s41467-021-27419-w

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