Letter

Motor neurons control locomotor circuit function retrogradely via gap junctions

  • Nature volume 529, pages 399402 (21 January 2016)
  • doi:10.1038/nature16497
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Abstract

Motor neurons are the final stage of neural processing for the execution of motor behaviours. Traditionally, motor neurons have been viewed as the ‘final common pathway’, serving as passive recipients merely conveying to the muscles the final motor program generated by upstream interneuron circuits1,2. Here we reveal an unforeseen role of motor neurons in controlling the locomotor circuit function via gap junctions in zebrafish. These gap junctions mediate a retrograde analogue propagation of voltage fluctuations from motor neurons to control the synaptic release and recruitment of the upstream V2a interneurons that drive locomotion. Selective inhibition of motor neurons during ongoing locomotion de-recruits V2a interneurons and strongly influences locomotor circuit function. Rather than acting as separate units, gap junctions unite motor neurons and V2a interneurons into functional ensembles endowed with a retrograde analogue computation essential for locomotor rhythm generation. These results show that motor neurons are not a passive recipient of motor commands but an integral component of the neural circuits responsible for motor behaviour.

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Acknowledgements

We thank C. Wyart, S. Grillner, O. Kiehn and G. Silberberg as well as the members of our lab for comments on an early version of the manuscript. We are grateful to A. Baradel, C. Wyart, S. Higashijima and H. Baier for providing the zebrafish lines used in this study. This study was supported by grants from the Swedish Research Council, Karolinska Institute and the Swedish Brain Foundation.

Author information

Affiliations

  1. Department of Neuroscience, Karolinska Institute, 171 77 Stockholm, Sweden

    • Jianren Song
    • , Konstantinos Ampatzis
    • , E. Rebecka Björnfors
    •  & Abdeljabbar El Manira

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Contributions

J.S., K.A. and A.E.M. initiated the project and designed the experiments. J.S. performed all the electrophysiological and optogenetic experiments. K.A. performed the anatomical and contributed to the electrophysiological experiments. E.R.B. contributed to the anatomical and electrophysiological experiments. All the authors contributed to data analysis, discussed the results and participated in writing the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Abdeljabbar El Manira.

Extended data

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