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A topographic map of recruitment in spinal cord

Abstract

Animals move over a range of speeds by using rhythmic networks of neurons located in the spinal cord1,2,3,4,5,6. Here we use electrophysiology and in vivo imaging in larval zebrafish (Danio rerio) to reveal a systematic relationship between the location of a spinal neuron and the minimal swimming frequency at which the neuron is active. Ventral motor neurons and excitatory interneurons are rhythmically active at the lowest swimming frequencies, with increasingly more dorsal excitatory neurons engaged as swimming frequency rises. Inhibitory interneurons follow the opposite pattern. These inverted patterns of recruitment are independent of cell soma size among interneurons, but may be partly explained by concomitant dorso-ventral gradients in input resistance. Laser ablations of ventral, but not dorsal, excitatory interneurons perturb slow movements, supporting a behavioural role for the topography. Our results reveal an unexpected pattern of organization within zebrafish spinal cord that underlies the production of movements of varying speeds.

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Figure 1: Activation of motor neurons depends on their position in spinal cord.
Figure 2: Activity patterns of excitatory spinal interneurons are also correlated with position.
Figure 3: Reverse gradients of recruitment for excitatory and inhibitory interneurons.
Figure 4: Ablation of ventral excitatory interneurons perturbs slow swimming movements, while ablation of dorsal ones does not.

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Acknowledgements

We are grateful to A. Hon and S. Kishore for performing En-1:GFP DNA injections and L. Heller for care and maintenance of the fish. We also thank A. Bass, D. Bhatt, P. Brehm, R. Harris-Warrick, A. Kinkhabwala, S. Kishore, M. Koyama, J. Liao and J. Olthoff for comments on the manuscript. This work was supported by grants from the National Institutes of Health and from the Ministry of Education, Science, Technology, Sports and Culture of Japan.

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Correspondence to Joseph R. Fetcho.

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Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Table 1 and additional references. (PDF 674 kb)

Supplementary Movie 1

This file contains Supplementary Movie 1 showing a series of images captured while focusing through the preparation containing the CiD interneuron shown in Figure 2 a. (MOV 3649 kb)

Supplementary Movie 2

This file contains Supplementary Movie 2 showing a series of images captured while focusing through the preparation containing the CiD interneuron shown in Figure 2 b. (MOV 495 kb)

Supplementary Movie 3

This file contains Supplementary Movie 3 showing a series of images captured while focusing through the preparation containing the MCoD interneuron shown in Figure 2 c. (MOV 1107 kb)

Supplementary Movie 4

This file contains Supplementary Movie 4 showing the combined fin and axial movements of a larval fish swimming slowly prior to MCoD ablations. (MOV 9216 kb)

Supplementary Movie 5

This file contains Supplementary Movie 5 showing alternating fin movements without associated axial movements after ablations of MCoDs in the same fish as in the preablation movie. (MOV 7974 kb)

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McLean, D., Fan, J., Higashijima, Si. et al. A topographic map of recruitment in spinal cord. Nature 446, 71–75 (2007). https://doi.org/10.1038/nature05588

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