Effect of prolonged unweighting of human skeletal muscle on neuromotor force control

Abstract

The purpose of this study was to determine the effect of 4 weeks of unilateral lower limb suspension (ULLS) on the fluctuations in motor output and the associated physiological changes. Subjects (n = 17) performed steady isometric plantarflexion (PF) and knee extension (KE) tasks, and KE shortening and lengthening contractions (intensity = 25% maximum). Spinal excitability of the soleus muscle was assessed via the H-reflex, muscle cross-sectional area (CSA) via MRI, along with EMG activity during the PF tasks. Following ULLS, isometric force fluctuations increased ∼12% for the PF, and 22% for the KE (P < 0.05), with no difference in the pattern of PF muscle activation (P = 0.46). The unsteadiness of lengthening KE contractions increased 25% following ULLS (P = 0.03), while KE steadiness during shortening contractions was not altered (P = 0.98). Significant correlations were observed between the percent changes in PF isometric force fluctuations and H-reflex (r = 0.49, P = 0.04), and between the PF isometric force fluctuations and PF CSA (r = −0.61, P < 0.01). These findings suggest the effects of unweighting on neuromotor performance are muscle group and contraction type dependent, and that the disuse-paradigm altering muscle CSA and spinal excitability may serve to mediate the associated loss of steadiness.

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References

  1. Aagaard P, Simonsen EB, Andersen JL, Magnusson SP, Dyhre-Poulsen P (2002) Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92:2309–2318

    PubMed  Google Scholar 

  2. Adams GR, Caiozzo VJ, Baldwin KM (2003) Skeletal muscle unweighting: spaceflight and ground-based models. J Appl Physiol 95(6):2185–2201

    PubMed  Google Scholar 

  3. Akima H, Kubo K, Imai M, Kanehisa H, Suzuki Y, Gunji A, Fukunaga T (2001) Inactivity and muscle: effect of resistance training during bed rest on muscle size in the lower limb. Acta Physiol Scand 172(4):269–278

    PubMed  Article  CAS  Google Scholar 

  4. Alkner BA, Tesch PA (2004). Knee extensor and plantar flexor muscle size and function following 90 days of bed rest with or without resistance exercise. Eur J Appl Physiol 93(3):294–305

    PubMed  Article  Google Scholar 

  5. Berg HE, Dudley GA, Haggmark T, Ohlsen H, Tesch PA (1991). Effects of lower limb unloading on skeletal muscle mass and function in humans. J Appl Physiol 70(4):1882–1885

    PubMed  CAS  Google Scholar 

  6. Berry P, Berry I, Manelfe C (1993) Magnetic resonance imaging evaluation of lower limb muscles during bed rest—a microgravity simulation model. Aviat Space Environ Med 64(3 Pt 1):212–218

    PubMed  CAS  Google Scholar 

  7. Bleeker MW, Hopman MT, Rongen GA, Smits P (2004). Unilateral lower limb suspension can cause deep venous thrombosis. Am J Physiol Regul Integr Comp Physiol 286(6):R1176–R1177

    PubMed  Google Scholar 

  8. Burnett RA, Laidlaw DH, Enoka RM (2000) Coactivation of the antagonist muscle does not covary with steadiness in old adults. J Appl Physiol 89(1):61–71

    PubMed  CAS  Google Scholar 

  9. Clark BC, Fernhall B, Ploutz-Snyder LL (2006a) Adaptations in human neuromuscular function following prolonged unweighting: I. Skeletal muscle contractile properties and applied ischemia efficacy. J Appl Physiol 101(1):256–263

    Article  Google Scholar 

  10. Clark BC, Manini TM, Bolanowski SJ, Ploutz-Snyder LL (2006b) Adaptations in human neuromuscular function following prolonged unweighting: II. Neurological properties and motor imagery efficacy. J Appl Physiol 101(1):264–272

    Article  Google Scholar 

  11. Collaborative, overview (1994) Collaborative overview of randomised trials of antiplatelet therapy–III: Reduction in venous thrombosis and pulmonary embolism by antiplatelet prophylaxis among surgical and medical patients. Antiplatelet Trialists’ Collaboration. Bmj 308(6923):235–246

  12. Convertino VA, Doerr DF, Mathes KL, Stein SL, Buchanan P (1989) Changes in volume, muscle compartment, and compliance of the lower extremities in man following 30 days of exposure to simulated microgravity. Aviat Space Environ Med 60(7):653–658

    PubMed  CAS  Google Scholar 

  13. Cresswell AG, Loscher WN (2000) Significance of peripheral afferent input to the alpha-motoneurone pool for enhancement of tremor during an isometric fatiguing contraction. Eur J Appl Physio 82(1–2):129–136

    Article  CAS  Google Scholar 

  14. Cook SB, Clark BC, Ploutz-Snyder LL (2006) Accelerometry as a measure of subject compliance in unilateral lower limb suspension. Aviat Space Environ Med 77(9):953–956

    PubMed  Google Scholar 

  15. Cram JR, Kasman GS (1998) Introduction to surface electromyography. Aspen, Gaithersburg

    Google Scholar 

  16. Duchateau J (1995) Bed rest induces neural and contractile adaptations in triceps surae. Med Sci Sports Exerc 27(12):1581–1589

    PubMed  CAS  Google Scholar 

  17. Duchateau J, Enoka RM (2002). Neural adaptations with chronic activity patterns in able-bodied humans. Am J Phys Med Rehabil 81:S17–S27

    PubMed  Article  Google Scholar 

  18. Duchateau J, Hainaut K (1990). Effects of immobilization on contractile properties, recrutiment and firing rates of human motor units. J Physiology 422:55–65

    CAS  Google Scholar 

  19. Dudley GA, Ploutz-Snyder LL (2001) Deconditioning and bed rest: musculoskeletal response. ACSM’s Resource Manual for Guidleines for Exercise Testing and Prescription. J. L. Roitman. Williams & Wilkins, Baltimore, pp 200–205

  20. Edgerton VR, Roy RR, Allen DL, Monti RJ (2002). Adaptations in skeletal mulsce disuse or decreased-use atrophy. Am J Phys Med 81:S127–S147

    Article  Google Scholar 

  21. Enoka RM, Christou EA, Hunter SK, Kornatz KW, Semmler JG, Taylor AM, Tracy BL (2003) Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol 13:1–12

    PubMed  Article  Google Scholar 

  22. Fitts RH, Riley DR, Widrick JJ (2000) Physiology of a microgravity environment invited review: microgravity and skeletal muscle. J Appl Physiol 89(2):823–839

    PubMed  CAS  Google Scholar 

  23. Fitts RH, Riley DR, Widrick JJ (2001). Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol 204(Pt 18):3201–3208

    PubMed  CAS  Google Scholar 

  24. Gamrin L, Berg HE, Essen P, Tesch PA, Hultman E, Garlick PJ, McNurlan MA, Wernerman J (1998) The effect of unloading on protein synthesis in human skeletal muscle. Acta Physiol Scand 163(4):369–377

    PubMed  CAS  Google Scholar 

  25. Gardiner PF (2001) Neuromuscular aspects of physical activity. Human Kinetics, Champaign, IL

    Google Scholar 

  26. Hather BM, Adams GR, Tesch PA, Dudley GA (1992). Skeletal muscle responses to lower limb suspension in humans. J Appl Physiol 72(4):1493–1498

    PubMed  CAS  Google Scholar 

  27. Howell JN, Fuglevand AJ, Walsh ML, Bigland-Ritchie B (1995) Motor unit activity during isometric and concentric–eccentric contractions of the human first dorsal interosseus muscle. J Neurophysiol 74(2):901–904

    PubMed  CAS  Google Scholar 

  28. Kornatz KW, Christou EA, Enoka RM (2005) Practice reduces motor unit discharge variability in a hand muscle and improves manual dexterity in old adults. J Appl Physiol 98(6):2072–2080

    PubMed  Article  Google Scholar 

  29. Kossev A, Christova P (1998) Discharge pattern of human motor units during dynamic concentric and eccentric contractions. Electroencephalogr Clin Neurophysiol 109(3):245–255

    PubMed  Article  CAS  Google Scholar 

  30. Kozlovskaya IB, Kirenskaya AV (2004) Mechanisms of disorders of the characteristics of fine movements in long-term hypokinesia. Neurosci Behav Physiol 34(7):747–754

    PubMed  Article  CAS  Google Scholar 

  31. Laidlaw DH, Bilodeau M, Enoka RM (2000) Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve 23(4):600–612

    PubMed  Article  CAS  Google Scholar 

  32. LeBlanc AD, Schneider VS, Evans HJ, Pientok C, Rowe R, Spector E (1992) Regional changes in muscle mass following 17 weeks of bed rest. J Appl Physiol 73(5):2172–2178

    PubMed  CAS  Google Scholar 

  33. Liu YS, Huang WF, Liu XH, Wang J, Zhao DM, Wu X (2003) Effects of exercise training during 21 d-6 degrees head down bed rest on dynamic posture equilibrium and motor coordination. Space Med Med Eng 16(4):264–268

    Google Scholar 

  34. Manini TM, Clark BC, Tracy BL, Burke J, Ploutz-Snyder L (2005) Resistance and functional training reduces knee extensor position fluctuations in functionally limited older adults. Eur J Appl Physiol 95(5–6):436–446

    PubMed  Article  Google Scholar 

  35. Manini TM, Clark BC, Nalls MA, Goodpaster BH, Ploutz-Snyder LL, Harris TB (2007) Reduced physical activity increases inter-muscular adipose tissue. Am J Clin Nutr (in press)

  36. Morita H, Petersen N, Christensen LO, Sinkjaer T, Nielsen J (1998) Sensitivity of H-reflexes and stretch reflexes to presynaptic inhibition in humans. J Neurophysiol 80(2):610–620

    PubMed  CAS  Google Scholar 

  37. Moritz CT, Barry BK, Pascoe MA, Enoka RM (2005) Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J Neurophysiol 93(5):2449–2459

    PubMed  Article  Google Scholar 

  38. Morris RJ, Woodcock JP (2004) Evidence-based compression: prevention of stasis and deep vein thrombosis. Ann Surg 239(2):162–171

    PubMed  Article  Google Scholar 

  39. Nicogossian AE, Huntoon CL, Pool SL (eds) (1994) Space physiology and medicine. Lea and Febiger, Philadelphia

  40. Ploutz-Snyder LL, Tesch PA, Crittenden DJ, Dudley GA (1995) Effect of unweighting on skeletal muscle use during exercise. 79(1):168–175

    Google Scholar 

  41. Polgar J, Johnson MA, Weightman D, Appleton D (1973) Data on fibre size in thirty-six human muscles. An autopsy study. J Neurol Sci 19(3):307–318

    PubMed  Article  CAS  Google Scholar 

  42. Recktenwald MR, Hodgson JA, Roy RR, Riazanski S, McCall GE, Kozlovskaya I, Washburn DA, Fanton JW, Edgerton VR (1999). Effects of spaceflight on rhesus quadrupedal locomotion after return to 1G. J Neurophysiol 81(5):2451–2463

    PubMed  CAS  Google Scholar 

  43. Roy RR, Hodgson JA, Aragon J, Day MK, Kozlovskaya I, Edgerton VR (1996) Recruitment of the Rhesus soleus and medial gastrocnemius before, during and after spaceflight. J Gravit Physiol 3(1):11–15

    PubMed  CAS  Google Scholar 

  44. Schulze K, Gallagher P, Trappe S (2002). Ressitance training preserves skeletal muscle function during unloading in humans. Med Sci Sports Exerc 34:303–313

    PubMed  Article  Google Scholar 

  45. Seki K, Taniguchi Y, Narusawa M (2001). Effects of joint immobilization on firing rate modulation of human motor units. J Physiol 530(Pt 3):507–519

    PubMed  Article  CAS  Google Scholar 

  46. Shinohara M, Moritz CT, Pascoe MA, Enoka RM (2005). Prolonged muscle vibration increases stretch reflex amplitude, motor unit discharge rate, and force fluctuations in a hand muscle. J Appl Physiol 99(5):1835–1842

    PubMed  Article  Google Scholar 

  47. Shinohara M, Yoshitake Y, Kouzaki M, Fukuoka H, Fukunaga T (2003) Strength training counteracts motor performance losses during bed rest. J Appl Physiol 95(4):1485–1492

    PubMed  Google Scholar 

  48. Tax AA, Denier van der Gon JJ, Erkelens CJ (1990). Differences in coordination of elbow flexor muscles in force tasks and in movement tasks. Exp Brain Res 81(3):567–572

    PubMed  Article  CAS  Google Scholar 

  49. Taylor AM, Christou EA, Enoka RM (2003) Multiple features of motor-unit activity influence force fluctuations during isometric contractions. J Neurophysiol 90(2):1350–1361

    PubMed  Article  Google Scholar 

  50. Tesch PA, Trieschmann JT, Ekberg A (2004) Hypertrophy of chronically unloaded muscle subjected to resistance exercise. J Appl Physiol 96(4):1451–1458

    PubMed  Article  CAS  Google Scholar 

  51. Tracy BL, Maluf KS, Stephenson JL, Hunter SK, Enoka RM (2005) Variability of motor unit discharge and force fluctuations across a range of muscle forces in older adults. Muscle Nerve 32(4):533–540

    PubMed  Article  Google Scholar 

  52. Widrick JJ, Trappe SW, Romatowski JG, Riley DA, Costill DL, Fitts RH (2002) Unilateral lower limb suspension does not mimic bed rest or spaceflight effects on human muscle fiber function. J Appl Physiol 93(1): 354–360

    PubMed  CAS  Google Scholar 

  53. Yoshitake Y, Shinohara M, Kouzaki M, Fukunaga T (2004) Fluctuations in plantar flexion force are reduced after prolonged tendon vibration. J Appl Physiol 97(6):2090-2097

    PubMed  Article  Google Scholar 

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Acknowledgments

This project was supported in part by a National Aeronautics and Space Administration (NASA) Training Fellowship (NGT5-50446), and the 2004 & 2005 NASA Space Physiology Research Grants via the American College of Sports Medicine Foundation. Additionally, Dynastream Innovations, Inc, and BSN-JOBST provided product supply and technical support.

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Correspondence to Brian C. Clark.

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Data for this project were collected in the Musculoskeletal Research Laboratory at Syracuse University.

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Clark, B.C., Pierce, J.R., Manini, T.M. et al. Effect of prolonged unweighting of human skeletal muscle on neuromotor force control. Eur J Appl Physiol 100, 53–62 (2007). https://doi.org/10.1007/s00421-007-0399-6

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Keywords

  • Force control
  • Steadiness
  • Disuse
  • Atrophy
  • H-reflex