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Continuous shifts in the active set of spinal interneurons during changes in locomotor speed

Abstract

The classic 'size principle' of motor control describes how increasingly forceful movements arise by the recruitment of motoneurons of progressively larger size and force output into the active pool. We explored the activity of pools of spinal interneurons in larval zebrafish and found that increases in swimming speed were not associated with the simple addition of cells to the active pool. Instead, the recruitment of interneurons at faster speeds was accompanied by the silencing of those driving movements at slower speeds. This silencing occurred both between and within classes of rhythmically active premotor excitatory interneurons. Thus, unlike motoneurons, there is a continuous shift in the set of cells driving the behavior, even though changes in the speed of the movements and the frequency of the motor pattern appear to be smoothly graded. We conclude that fundamentally different principles may underlie the recruitment of motoneuron and interneuron pools.

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Figure 1: Analysis of real and fictive evoked swimming movements.
Figure 2: Recruitment pattern of spinal motoneurons.
Figure 3: Anatomy of MCoD interneurons.
Figure 4: Pair-wise recordings of MCoDs and motoneurons.
Figure 5: Rhythmic firing behavior of MCoDs during fictive swimming.
Figure 6: Inhibition of MCoDs at fast swimming frequencies.
Figure 7: Dual MCoD and CiD interneuron recordings.
Figure 8: Frequency-dependent shifts in recruitment in and between classes.

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Acknowledgements

We are extremely grateful to S. Higashijima for providing us with the alx-gfp transgenic fish. We also thank L. Heller for fish care and M. Koyama for comments on the manuscript. This work was supported by fellowships from the US National Institutes of Health (NS44728 to D.L.M. and NS44758 to M.A.M.) and grants from the National Science Foundation (DMS-0107893 to W.B.L.) and US National Institutes of Health (NS26539 to J.R.F.).

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D.L.M. conducted experiments, analyzed data and helped write the manuscript; M.A.M. conducted early MCoD recordings; I.Y.Y.K. and W.B.L. wrote the medial axis portion of the computer code to analyze the movement; and J.R.F. supervised the project, helped write the manuscript and wrote some of the computer code for analysis of movement.

Corresponding author

Correspondence to Joseph R Fetcho.

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McLean, D., Masino, M., Koh, I. et al. Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neurosci 11, 1419–1429 (2008). https://doi.org/10.1038/nn.2225

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