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Heterogeneity in form and function of the rat extensor digitorum longus motor unit

Journal of anatomy, 2022-04, Vol.240 (4), p.700-710 [Peer Reviewed Journal]

2021 The Authors. published by John Wiley & Sons Ltd on behalf of Anatomical Society. ;2021 The Authors. Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society. ;2021. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. ;ISSN: 0021-8782 ;EISSN: 1469-7580 ;DOI: 10.1111/joa.13590 ;PMID: 34761377

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  • Title:
    Heterogeneity in form and function of the rat extensor digitorum longus motor unit
  • Author: Kissane, Roger W. P. ; Chakrabarty, Samit ; Askew, Graham N. ; Egginton, Stuart
  • Subjects: Animals ; Capillaries ; capillary supply ; Glycolysis ; Mathematical models ; motoneuron ; Motor Neurons ; Muscle Fibers, Skeletal - physiology ; Muscle, Skeletal - physiology ; Original Paper ; Original Papers ; oxygen modelling ; Rats ; Skeletal muscle ; work loop
  • Is Part Of: Journal of anatomy, 2022-04, Vol.240 (4), p.700-710
  • Description: The motor unit comprises a variable number of muscle fibres that connect through myelinated nerve fibres to a motoneuron (MN), the central drivers of activity. At the simplest level of organisation there exist phenotypically distinct MNs that activate corresponding muscle fibre types, but within an individual motor pool there typically exists a mixed population of fast and slow firing MNs, innervating groups of Type II and Type I fibres, respectively. Characterising the heterogeneity across multiple levels of motor unit organisation is critical to understanding changes that occur in response to physiological and pathological perturbations. Through a comprehensive assessment of muscle histology and ex vivo function, mathematical modelling and neuronal tracing, we demonstrate regional heterogeneities at the level of the MN, muscle fibre type composition and oxygen delivery kinetics of the rat extensor digitorum longus (EDL) muscle. Specifically, the EDL contains two phenotypically distinct regions: a relatively oxidative medial and a more glycolytic lateral compartment. Smaller muscle fibres in the medial compartment, in combination with a greater local capillary density, preserve tissue O2 partial pressure (PO2) during modelled activity. Conversely, capillary supply to the lateral compartment is calculated to be insufficient to defend active muscle PO2 but is likely optimised to facilitate metabolite removal. Simulation of in vivo muscle length change and phasic activation suggest that both compartments are able to generate similar net power. However, retrograde tracing demonstrates (counter to previous observations) that a negative relationship between soma size and C‐bouton density exists. Finally, we confirm a lack of specificity of SK3 expression to slow MNs. Together, these data provide a reference for heterogeneities across the rat EDL motor unit and re‐emphasise the importance of sampling technique. Labelled motoneurons (MNs) across the extensor digitorum longus (EDL) motor pool highlight the negative relationship between soma area and vesicular acetylcholine transporter Density and SK3 Density. These MNs innervate phenotypically distinct portions of the EDL muscle that is synchronously recruited to provide power for movement. At the level of individual fibres and capillaries heterogeneities in oxygen supply and demand are evident, which when scaled up combine to meet the demands of the muscle, principally maintenance of oxidative phosphorylation in the medial and removal of lactate in the lateral compartment.
  • Publisher: England: Wiley Subscription Services, Inc
  • Language: English
  • Identifier: ISSN: 0021-8782
    EISSN: 1469-7580
    DOI: 10.1111/joa.13590
    PMID: 34761377
  • Source: Geneva Foundation Free Medical Journals at publisher websites
    MEDLINE
    PubMed Central
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