Use it or lose it: tonic activity of slow motoneurons promotes their survival and preferentially increases slow fiber-type groupings in muscles of old lifelong recreational sportsmen

  • Simone Mosole | simone.mosole@studenti.unipd.it Laboratory of Translation Myology, Department of Biomedical Sciences, University of Padova, Italy; Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.
  • Ugo Carraro IRCCS Fondazione Ospedale San Camillo, Venice, Italy.
  • Helmut Kern Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna; Department of Physical Medicine and Rehabilitation, Wilhelminenspital, Vienna, Austria.
  • Stefan Loefler Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.
  • Sandra Zampieri Laboratory of Translation Myology, Department of Biomedical Sciences, University of Padova, Italy; Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.

Abstract

Histochemistry, immuno-histochemistry, gel electrophoresis of single muscle fibers and electromyography of aging muscles and nerves suggest that: i) denervation contributes to muscle atrophy, ii) impaired mobility accelerates the process, and iii) lifelong running protects against loss of motor units. Recent corroborating results on the muscle effects of Functional Electrical Stimulation (FES) of aged muscles will be also mentioned, but we will in particular discuss how and why a lifelong increased physical activity sustains reinnervation of muscle fibers. By analyzing distribution and density of muscle fibers co-expressing fast and slow Myosin Heavy Chains (MHC) we are able to distinguish the transforming muscle fibers due to activity related plasticity, to those that adapt muscle fiber properties to denervation and reinnervation. In muscle biopsies from septuagenarians with a history of lifelong high-level recreational activity we recently observed in comparison to sedentary seniors: 1. decreased proportion of small-size angular myofibers (denervated muscle fibers); 2. considerable increase of fiber-type groupings of the slow type (reinnervated muscle fibers); 3. sparse presence of muscle fibers co-expressing fast and slow MHC. Immuno-histochemical characteristics fluctuate from those with scarce fiber-type modulation and groupings to almost complete transformed muscles, going through a process in which isolated fibers co-expressing fast and slow MHC fill the gaps among fiber groupings. Data suggest that lifelong high-level exercise allows the body to adapt to the consequences of the age-related denervation and that it preserves muscle structure and function by saving otherwise lost muscle fibers through recruitment to different slow motor units. This is an opposite behavior of that described in long term denervated or resting muscles. These effects of lifelong high level activity seems to act primarily on motor neurons, in particular on those always more active, i.e., on the slow motoneurons. The preferential reinnervation that follows along decades of increased activity maintains neuron and myofibers. All together the results open interesting perspectives for applications of FES and electroceuticals for rejuvenation of aged muscles to delay functional decline and loss of independence that are unavoidable burdens of advanced aging. Trial Registration: ClinicalTrials.gov: NCT01679977.

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Author Biographies

Simone Mosole, Laboratory of Translation Myology, Department of Biomedical Sciences, University of Padova, Italy; Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna

Laboratory of Translation Myology, Department of Biomedical Sciences, University of Padova, Italy

Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria

Ugo Carraro, IRCCS Fondazione Ospedale San Camillo, Venice
I.R.C.C.S. Fondazione Ospedale San Camillo, Venice, Italy
Helmut Kern, Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna; Department of Physical Medicine and Rehabilitation, Wilhelminenspital, Vienna

I.R.C.C.S. Fondazione Ospedale San Camillo, Venice, Italy

Department of Physical Medicine and Rehabilitation, Wilhelminenspital, Vienna, Austria.

Stefan Loefler, Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna
Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria
Sandra Zampieri, Laboratory of Translation Myology, Department of Biomedical Sciences, University of Padova, Italy; Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna

Laboratory of Translation Myology, Department of Biomedical Sciences, University of Padova, Italy

Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria

Published
2016-12-15
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Section
Myology Made in Italy
Keywords:
Aging, Human skeletal muscle, Lifelong physical exercise denervation and re-innervation, Fiber type grouping, Co-expression of fast and slow myosin heavy chains
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How to Cite
Mosole, S., Carraro, U., Kern, H., Loefler, S., & Zampieri, S. (2016). Use it or lose it: tonic activity of slow motoneurons promotes their survival and preferentially increases slow fiber-type groupings in muscles of old lifelong recreational sportsmen. European Journal of Translational Myology, 26(4). https://doi.org/10.4081/ejtm.2016.5972

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