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Maturation of persistent and hyperpolarization-activated inward currents shape the recruitment of motoneuron subtypes during postnatal development

View ORCID ProfileSimon A. Sharples, View ORCID ProfileGareth B. Miles
doi: https://doi.org/10.1101/2021.06.16.448644
Simon A. Sharples
School of Psychology and Neuroscience, University of St. Andrews, Fife, United Kingdom
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Gareth B. Miles
School of Psychology and Neuroscience, University of St. Andrews, Fife, United Kingdom
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  • For correspondence: gbm4@st-andrews.ac.uk
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Abstract

The fine control of movement is a prerequisite for complex behaviour and is mediated by the orderly recruitment of motor units composed of slow and fast twitch muscle fibres. The size principle was initially proposed to account for orderly recruitment; however, motoneuron size is a poor predictor of recruitment amongst functionally defined motor unit subtypes. While intrinsic properties of motoneurons are key regulators of motoneuron recruitment, the underlying currents involved are not well defined. Whole-cell patch-clamp electrophysiology was deployed to study intrinsic properties, and the underlying currents, that contribute to the differential recruitment of fast and slow motoneurons. Motoneurons were studied during the first three postnatal weeks in mice to identify key properties that establish orderly recruitment and contribute to the emergence of fine motor control. We find that fast and slow motoneurons are functionally homogeneous during the first postnatal week and are recruited based on size, irrespective of motoneuron subtype. The recruitment of fast and slow motoneurons becomes staggered during the second postnatal week due to the differential maturation of passive and active properties, particularly persistent inward currents (PICs). The current required to recruit fast motoneurons increases further in the third postnatal week, despite no additional changes in passive properties or PICs. This further staggering of recruitment currents reflects development of a hyperpolarization-activated inward current during week 3. Our results suggest that motoneuron recruitment is multifactorial, with recruitment order established during postnatal development through the differential maturation of passive properties and sequential integration of persistent and hyperpolarization-activated inward currents.

Key Points

  • Fast and slow motoneurons become functionally diversified during postnatal development leading to the establishment of differential recruitment of fast and slow motoneuron subtypes.

  • This functional development and diversification of motoneuron subtype recruitment is established through the differential maturation of passive and active properties.

  • Fast motoneuron recruitment is delayed relative to slow motoneurons due to more depolarised thresholds for persistent inward currents and selective expression of a resting hyperpolarization-activated inward current.

  • Recruitment of motoneuron subtypes is multifaceted and supported by differences in passive and active properties.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 17, 2021.
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Maturation of persistent and hyperpolarization-activated inward currents shape the recruitment of motoneuron subtypes during postnatal development
Simon A. Sharples, Gareth B. Miles
bioRxiv 2021.06.16.448644; doi: https://doi.org/10.1101/2021.06.16.448644
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Maturation of persistent and hyperpolarization-activated inward currents shape the recruitment of motoneuron subtypes during postnatal development
Simon A. Sharples, Gareth B. Miles
bioRxiv 2021.06.16.448644; doi: https://doi.org/10.1101/2021.06.16.448644

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