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Resistance to disuse atrophy in a turtle hindlimb muscle

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Abstract

The purpose of this study was to characterize the changes in a turtle hindlimb muscle (external gastrocnemius) after exposure to three conditions of disuse: immobilization, tenotomy, and spinalization. Histochemical analysis and measurement of muscle fiber cross-sectional area and weighted cross-sectional area were used to assess the potential conversion of muscle fiber types and changes in fiber size. It was found that unlike its counterpart in mammalian endotherms, the external gastrocnemius muscle of the adult turtle, Trachemys scripta elegans, was remarkably resistant to each model of reduced muscle function. It is suggested that such resistance to disuse is due to intrinsic mechanisms that enable heterothermic mammals and ectothermic vertebrates to tolerate an unfavorable climate and food and water shortages by using hypometabolic states.

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Notes

  1. There is no universally accepted terminology for homeothermic mammals that maintain a constant body temperature (termed “endotherms” here) versus mammals that have the capacity to become hypometabolic via hibernation or estivation (“heterotherms”). In contrast, “ectotherm” is universally accepted as appropriate terminology for a non-mammalian vertebrate that can also convert to a hypometabolic state. For an extensive review of this terminology issue, see Schmidt-Nielsen (1997, p 218)

  2. For a chronological review of disuse literature on endotherms, including humans, that is relevant to this article see: Vrbová 1963; Fischbach and Robbins 1969; Shafiq et al. 1969; Booth and Kelso 1973; Maier et al. 1976; MacDougall et al. 1977, 1980; Mayer et al. 1981; Witzmann et al. 1982; Baker 1983; Alaimo et al. 1984; Hnik et al. 1985; Alford et al. 1987; Hikida et al. 1989; Roy et al. 1987, 1991; Robinson et al. 1991; Goldspink et al. 1992; Gordon and Pattullo 1993; Gordon 1995; Nordstrom et al. 1995; Ferrando et al. 1996; McComas 1996; Edgerton et al. 1996, 2002; Semmler et al. 2000; Adams et al. 2003; Otis et al. 2004

  3. It has been shown previously that when the turtle is spinalized under hypothermic anesthesia, it subsequently displays hindlimb cutaneous reflexes. These are evident one hour post surgery, after the preparation is warmed to room temperature (e.g., Mortin et al. 1985; Earhart and Stein 2000).

Abbreviations

CSA:

cross-sectional area (of muscle fiber)

EG:

external gastrocnemius (muscle)

Foth :

fast, other fiber

Fg:

fast, glycolytic turtle muscle fiber

FOG:

fast, oxidative-glycolytic fiber

SC:

spinal cord

SO:

slow, oxidative fiber

wCSA:

weighted cross-sectional area

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Acknowledgements

We would like to thank Dr. Roger Enoka for reviewing a draft of this article. The authors also thank Dr. Clark Lantz for use of his Bioquant analysis system, and Patricia Pierce for her technical assistance. The work was supported in part by NS 20577 and NS 07309 (to D.G.S.), NS 20762 and NS 01686 (to J.C.M.), GM 08444 (to W.H. Dantzler), and a University of Newcastle Visiting Faculty Award (to R.J.C. for D.G.S.). The report’s contents are solely the responsibility of the authors and do not necessarily represent the views of Dr Enoka or the awarding agencies. All protocols involving the use of turtles were approved by the Institutional Animal Care and Use Committee (IACUC) of The University of Arizona and were in conformity with local state and federal regulations for the care and use of laboratory animals.

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Authors and Affiliations

  1. Program in Physical Therapy, Arizona School of Health Sciences, A.T. Still University of Health Sciences, Mesa, AZ 85206, USA

    J. C. McDonagh

  2. School of Biomedical Sciences, Faculty of Health, University of Newcastle, 2308, Callaghan, NSW, Australia

    R. J. Callister

  3. Department of Rehabilitation Services, Flagstaff Medical Center, 1200 N. Beaver St., Flagstaff, AZ 86001, USA

    M. L. Favron

  4. Department of Physiology, The University of Arizona College of Medicine, Tucson, AZ 85724-5051, USA

    D. G. Stuart

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  1. J. C. McDonagh
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Correspondence to D. G. Stuart.

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McDonagh, J.C., Callister, R.J., Favron, M.L. et al. Resistance to disuse atrophy in a turtle hindlimb muscle. J Comp Physiol A 190, 321–329 (2004). https://doi.org/10.1007/s00359-004-0501-z

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