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Principles governing recruitment of motoneurons during swimming in zebrafish

Nature Neuroscience volume 14, pages 93–99 (2011)Cite this article

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Abstract

Locomotor movements are coordinated by a network of neurons that produces sequential muscle activation. Different motoneurons need to be recruited in an orderly manner to generate movement with appropriate speed and force. However, the mechanisms governing recruitment order have not been fully clarified. Using an in vitro juvenile/adult zebrafish brainstem-spinal cord preparation, we found that motoneurons were organized into four pools with specific topographic locations and were incrementally recruited to produce swimming at different frequencies. The threshold of recruitment was not dictated by the input resistance of motoneurons, but was instead set by a combination of specific biophysical properties and the strength of the synaptic currents. Our results provide insights into the cellular and synaptic computations governing recruitment of motoneurons during locomotion.

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Figure 1: Synaptic activity of identified motoneurons.
Figure 2: Synaptic activity of the four different pools of motoneurons during locomotion.
Figure 3: Relationship between the motoneuron membrane potential oscillation amplitude and the swimming frequency.
Figure 4: Quantification of parameters important for the recruitment of the different pools of motoneurons.
Figure 5: Excitatory and inhibitory synaptic currents in the four pools of motoneurons.
Figure 6: The amplitude of synaptic currents is correlated with the order of recruitment of motoneurons.
Figure 7: Characteristic intrinsic properties of the four pools of motoneurons.

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Acknowledgements

We thank K. Dougherty, R. Hill, S. Grillner and D. McLean for comments and critical discussion of this manuscript. This work was funded by a grant from the Swedish Research Council, European Commission (FP7, Spinal Cord Repair), Söderberg Foundation and Karolinska Institutet. J.P.G. and J.A. received post-doctoral fellowships from the German Science Foundation.

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Author notes

  1. Jens Peter Gabriel

    Present address: Present address: Max Planck Institute for Medical Research, Heidelberg, Germany.,

  2. Jens Peter Gabriel and Jessica Ausborn: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden

    Jens Peter Gabriel, Jessica Ausborn, Konstantinos Ampatzis, Riyadh Mahmood, Emma Eklöf-Ljunggren & Abdeljabbar El Manira

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Contributions

J.P.G., J.A., K.A. and A.E.M. conceived the project and planned the experiments. J.P.G., J.A., K.A. and R.M. performed the experiments. All of the authors contributed to the analysis of the data, preparation of the figures and the writing of the manuscript.

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Correspondence to Abdeljabbar El Manira.

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Gabriel, J., Ausborn, J., Ampatzis, K. et al. Principles governing recruitment of motoneurons during swimming in zebrafish. Nat Neurosci 14, 93–99 (2011). https://doi.org/10.1038/nn.2704

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