Cargando…
A specialized spinal circuit for command amplification and directionality during escape behavior
In vertebrates, action selection often involves higher cognition entailing an evaluative process. However, urgent tasks, such as defensive escape, require an immediate implementation of the directionality of escape trajectory, necessitating local circuits. Here we reveal a specialized spinal circuit...
Autores principales: | , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8545473/ https://www.ncbi.nlm.nih.gov/pubmed/34663699 http://dx.doi.org/10.1073/pnas.2106785118 |
_version_ | 1784590008344117248 |
---|---|
author | Guan, Na N. Xu, Lulu Zhang, Tianrui Huang, Chun-Xiao Wang, Zhen Dahlberg, Elin Wang, Haoyu Wang, Fangfang Pallucchi, Irene Hua, Yunfeng El Manira, Abdeljabbar Song, Jianren |
author_facet | Guan, Na N. Xu, Lulu Zhang, Tianrui Huang, Chun-Xiao Wang, Zhen Dahlberg, Elin Wang, Haoyu Wang, Fangfang Pallucchi, Irene Hua, Yunfeng El Manira, Abdeljabbar Song, Jianren |
author_sort | Guan, Na N. |
collection | PubMed |
description | In vertebrates, action selection often involves higher cognition entailing an evaluative process. However, urgent tasks, such as defensive escape, require an immediate implementation of the directionality of escape trajectory, necessitating local circuits. Here we reveal a specialized spinal circuit for the execution of escape direction in adult zebrafish. A central component of this circuit is a unique class of segmentally repeating cholinergic V2a interneurons expressing the transcription factor Chx10. These interneurons amplify brainstem-initiated escape commands and rapidly deliver the excitation via a feedforward circuit to all fast motor neurons and commissural interneurons to direct the escape maneuver. The information transfer within this circuit relies on fast and reliable axo-axonic synaptic connections, bypassing soma and dendrites. Unilateral ablation of cholinergic V2a interneurons eliminated escape command propagation. Thus, in vertebrates, local spinal circuits can implement directionality of urgent motor actions vital for survival. |
format | Online Article Text |
id | pubmed-8545473 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-85454732021-10-27 A specialized spinal circuit for command amplification and directionality during escape behavior Guan, Na N. Xu, Lulu Zhang, Tianrui Huang, Chun-Xiao Wang, Zhen Dahlberg, Elin Wang, Haoyu Wang, Fangfang Pallucchi, Irene Hua, Yunfeng El Manira, Abdeljabbar Song, Jianren Proc Natl Acad Sci U S A Biological Sciences In vertebrates, action selection often involves higher cognition entailing an evaluative process. However, urgent tasks, such as defensive escape, require an immediate implementation of the directionality of escape trajectory, necessitating local circuits. Here we reveal a specialized spinal circuit for the execution of escape direction in adult zebrafish. A central component of this circuit is a unique class of segmentally repeating cholinergic V2a interneurons expressing the transcription factor Chx10. These interneurons amplify brainstem-initiated escape commands and rapidly deliver the excitation via a feedforward circuit to all fast motor neurons and commissural interneurons to direct the escape maneuver. The information transfer within this circuit relies on fast and reliable axo-axonic synaptic connections, bypassing soma and dendrites. Unilateral ablation of cholinergic V2a interneurons eliminated escape command propagation. Thus, in vertebrates, local spinal circuits can implement directionality of urgent motor actions vital for survival. National Academy of Sciences 2021-10-18 2021-10-19 /pmc/articles/PMC8545473/ /pubmed/34663699 http://dx.doi.org/10.1073/pnas.2106785118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Guan, Na N. Xu, Lulu Zhang, Tianrui Huang, Chun-Xiao Wang, Zhen Dahlberg, Elin Wang, Haoyu Wang, Fangfang Pallucchi, Irene Hua, Yunfeng El Manira, Abdeljabbar Song, Jianren A specialized spinal circuit for command amplification and directionality during escape behavior |
title | A specialized spinal circuit for command amplification and directionality during escape behavior |
title_full | A specialized spinal circuit for command amplification and directionality during escape behavior |
title_fullStr | A specialized spinal circuit for command amplification and directionality during escape behavior |
title_full_unstemmed | A specialized spinal circuit for command amplification and directionality during escape behavior |
title_short | A specialized spinal circuit for command amplification and directionality during escape behavior |
title_sort | specialized spinal circuit for command amplification and directionality during escape behavior |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8545473/ https://www.ncbi.nlm.nih.gov/pubmed/34663699 http://dx.doi.org/10.1073/pnas.2106785118 |
work_keys_str_mv | AT guannan aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT xululu aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT zhangtianrui aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT huangchunxiao aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT wangzhen aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT dahlbergelin aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT wanghaoyu aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT wangfangfang aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT pallucchiirene aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT huayunfeng aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT elmaniraabdeljabbar aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT songjianren aspecializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT guannan specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT xululu specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT zhangtianrui specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT huangchunxiao specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT wangzhen specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT dahlbergelin specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT wanghaoyu specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT wangfangfang specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT pallucchiirene specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT huayunfeng specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT elmaniraabdeljabbar specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior AT songjianren specializedspinalcircuitforcommandamplificationanddirectionalityduringescapebehavior |