Experimental Brain Research

, Volume 208, Issue 2, pp 217–227 | Cite as

Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors

Research Article

Abstract

Training a muscle group in one limb yields strength gains bilaterally—the so-called cross-education effect. However, to date there has been little study of the targeted application of this phenomenon in a manner relevant to clinical rehabilitation. For example, it may be applicable post-stroke, where hemiparesis leads to ankle flexor weakness. The purpose of this study was to examine the effects of high-intensity unilateral dorsiflexion resistance training on agonist (tibialis anterior, TA) and antagonist (plantarflexor soleus, SOL) muscular strength and H-reflex excitability in the trained and untrained limbs. Ankle flexor and extensor torque, as well as SOL and TA H-reflexes evoked during low-level contraction, were measured before and after 5 weeks of dorsiflexion training (n = 19). As a result of the intervention, dorsiflexor maximal voluntary isometric contraction force (MVIC) significantly increased (P < 0.05) in both the trained and untrained limbs by 14.7 and 8.4%, respectively. No changes in plantarflexor MVIC force were observed in either limb. Significant changes in H-reflex excitability threshold were also detected: H@thresh significantly increased in the trained TA and SOL; and H@max decreased in both SOL muscles. These findings reveal that muscular crossed effects can be obtained in the ankle dorsiflexor muscles and provide novel information on agonist and antagonist spinal adaptations that accompany unilateral training. It is possible that the ability to strengthen the ankle dorsiflexors bilaterally could be applied in post-stroke rehabilitation, where ankle flexor weakness could be counteracted via dorsiflexor training in the less-affected limb.

Keywords

Interlimb Cross-education Muscular crossed effect H-reflex Rehabilitation 

References

  1. Aagaard P (2003) Training-induced changes in neural functions. Exerc Sport Sci Rev 31:61–67CrossRefPubMedGoogle Scholar
  2. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Halkjær-Kristensen J, Dyhre-Poulsen P (2000) Neural inhibition during maximal eccentric and concentric quadriceps contraction: effects of resistance training. J Appl Physiol 89:2249–2257PubMedGoogle Scholar
  3. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (2002) Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92:2309–2318PubMedGoogle Scholar
  4. Abe T, DeHoyos DV, Pollock ML, Garzarella L (2000) Time course for strength and muscle thickness changes following upper and lower body resistance training in men and women. Eur J Appl Physiol 81:174–180CrossRefPubMedGoogle Scholar
  5. Bawa P, Chalmers GR, Stewart H, Eisen AA (2002) Responses of ankle extensor and flexor motoneurons to transcranial magnetic stimulation. J Neurophysiol 88:124–132PubMedGoogle Scholar
  6. Bird SP, Tarpenning KM, Marino F (2005) Designing resistance training programmes to enhance muscular fitness: a review of the acute programme variables. Sports Med 35:841–851CrossRefPubMedGoogle Scholar
  7. Buchthal F, Schmalbruch H (1970) Contraction times of twitches evoked by H-reflexes. Acta Physiol Scand 80:378–382CrossRefPubMedGoogle Scholar
  8. Capaday C, Lavoie BA, Barbeau H, Schneider C, Bonnard M (1999) Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J Neurophysiol 81:129–139PubMedGoogle Scholar
  9. Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911–917PubMedGoogle Scholar
  10. Carroll TJ, Herbert RD, Munn J, Lee M, Gandevia SC (2006) Contralateral effects of unilateral training: evidence and possible mechanisms. J Appl Physiol 101:1514–1522CrossRefPubMedGoogle Scholar
  11. Christie A, Kamen G (2010) Short-term training adaptations in maximal motor unit firing rates and after hyperpolarization duration. Muscle Nerve 41:651–660PubMedGoogle Scholar
  12. Colson S, Pousson M, Martin A, Van Hoecke J (1999) Isokinetic elbow flexion and coactivation following eccentric training. J Electromyogr Kinesiol 9:13–20CrossRefPubMedGoogle Scholar
  13. Dobkin B (2003) The clinical science of neurologic rehabilitation, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  14. Dragert K, Zehr EP (2009) Rhythmic arm cycling modulates Hoffmann reflex excitability differentially in the ankle flexor and extensor muscles. Neurosci Lett 450:235–238CrossRefPubMedGoogle Scholar
  15. Duncan P, Zorowitz R, Bates B, Choi J, Glasberg J, Graham G, Katz R, Reker D (2005) Management of adult stroke rehabilitation care. Stroke 36:e100–e143CrossRefPubMedGoogle Scholar
  16. Farthing JP (2009) Cross education of strength depends on limb dominance: implications for theory and application. Exerc Sport Sci Rev 37:179–187PubMedGoogle Scholar
  17. Farthing JP, Chilibeck PD, Binsted G (2005) Cross education of arm muscular strength is unidirectional in right-handed individuals. Med Sci Sport Ex 37:1594–1600CrossRefGoogle Scholar
  18. Farthing JP, Krentz JR, Magnus CRA (2009) Strength training the free limb attenuates strength loss during unilateral immobilization. J Appl Physiol 106:830–836CrossRefPubMedGoogle Scholar
  19. Fimland M, Helgerud J, Solstad GM, Iversen VM, Leivseth G, Hoff J (2009) Neural adaptations underlying cross-education after unilateral strength training. Eur J Appl Physiol 107:723–730CrossRefPubMedGoogle Scholar
  20. Folland JP, Williams AG (2007) The adaptations to strength training: morphological and neurological contributions to increased strength. Sports Med 37:145–168CrossRefPubMedGoogle Scholar
  21. Frigon A, Collins D, Zehr EP (2004) Effect of rhythmic arm movement on reflexes in the legs: modulation of soleus H-reflexes and somatosensory conditioning. J Neurophysiol 91:1516–1523CrossRefPubMedGoogle Scholar
  22. Gabriel D, Kamen G, Frost G (2006) Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med 36:133–149CrossRefPubMedGoogle Scholar
  23. Geertsen SS, Lundbye-Jensen J, Nielsen JB (2008) Increased central facilitation an antagonist reciprocal inhibition at the onset of dorsiflexion following explosive strength training. J Appl Physiol 105:915–922CrossRefPubMedGoogle Scholar
  24. Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Malkia E, Kraemer W, Newton R, Alen M (1998) Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol 84:1341–1349PubMedGoogle Scholar
  25. Holtermann A, Roeleveld K, Engstrom M, Sand T (2007) Enhanced H-reflex with resistance training is related to increased rate of force development. Eur J Appl Physiol 101:301–312CrossRefPubMedGoogle Scholar
  26. Hortobagyi T, Hill J, Houmard J, Fraser D, Lambert N, Israel R (1996) Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol 80:765–772PubMedGoogle Scholar
  27. Klimstra M, Zehr EP (2008) A sigmoid function is the best fit for the ascending limb of the Hoffmann reflex recruitment curve. Exp Brain Res 186:93–105CrossRefPubMedGoogle Scholar
  28. Lagerquist O, Zehr EP, Baldwin ER, Klakowicz PM, Collins DF (2006a) Diurnal changes in the amplitude of the Hoffmann reflex in the human soleus but not in the flexor carpi radialis muscle. Exp Brain Res 170:1–6CrossRefPubMedGoogle Scholar
  29. Lagerquist O, Zehr EP, Docherty D (2006b) Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect. J Appl Physiol 100:83–90CrossRefPubMedGoogle Scholar
  30. Lee M, Carroll TJ (2007) Cross education: possible mechanisms for the contralateral effects of unilateral resistance training. Sports Med 37:1–14CrossRefPubMedGoogle Scholar
  31. Loadman PM, Zehr EP (2007) Rhythmic arm cycling produces a non-specific signal that suppresses Soleus H-reflex amplitude in stationary legs. Exp Brain Res 179:199–208CrossRefPubMedGoogle Scholar
  32. Morita H, Crone C, Christenhuis D, Peterson NT, Nielsen J (2001) Modulation of presynaptic inhibition and disynaptic reciprocal Ia inhibition during voluntary movement in spasticity. Brain 124:826–837CrossRefPubMedGoogle Scholar
  33. Moritani T, deVries H (1979) Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 58:115–130PubMedGoogle Scholar
  34. Morris S, Dodd K, Morris M (2004) Outcomes of progressive resistance strength training following stroke: a systematic review. Clin Rehab 18:27–39CrossRefGoogle Scholar
  35. Munn J, Herbert R, Gandevia C (2004) Contralateral effects of unilateral resistance training: a meta-analysis. J Appl Physiol 96:1861–1866CrossRefPubMedGoogle Scholar
  36. Munn J, Herbert R, Hancock M, Gandevia C (2005) Training with unilateral resistance exercise increases contralateral strength. J Appl Physiol 99:1880–1884CrossRefPubMedGoogle Scholar
  37. Quevedo J, Fedirchuk B, Gosgnach S, McCrea DA (2000) Group I disynaptic excitation of cat hindlimb flexor and bifunctional motoneurones during fictive locomotion. J Physiol 525:549–564CrossRefPubMedGoogle Scholar
  38. Reeves N, Maganaris C, Narici M (2005) Plasticity of dynamic muscle performance with strength training in elderly humans. Muscle Nerve 31:355–364CrossRefPubMedGoogle Scholar
  39. Rossignol S, Dubuc R, Gossard J (2006) Dynamic sensorimotor interactions in locomotion. Physiol Rev 86:89–154CrossRefPubMedGoogle Scholar
  40. Sackley C, Disler PB, Turner-Stokes L, Wade DT, Brittle N, Hoppitt T (2009) Rehabilitation interventions for foot drop in neuromuscular disease. Cochrane Database Syst Rev 8:CD003908Google Scholar
  41. Schubert M, Curt A, Jensen L, Dietz V (1997) Corticospinal input in human gait: modulation of magnetically evoked motor responses. Exp Brain Res 115:234–246CrossRefPubMedGoogle Scholar
  42. Scripture EW, Smith TL, Brown EM (1894) On the education of muscular control and power. Studies Yale Psychol Lab 2:114–119Google Scholar
  43. Sheskin DJ (2004) Handbook of parametric and non-parametric statistical procedures, 3rd edn. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  44. Tanaka R (1974) Reciprocal Ia inhibition during voluntary movements in man. Exp Brain Res 21:529–540CrossRefPubMedGoogle Scholar
  45. Taylor N, Dodd K, Damiano D (2005) Progressive resistance exercise in physical therapy: a summary of systematic reviews. Phys Ther 85:1208–1223PubMedGoogle Scholar
  46. Van Cutsem M, Duchateau J, Hainaut K (1998) Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans. J Physiol 513:295–305CrossRefPubMedGoogle Scholar
  47. Zehr EP (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468CrossRefPubMedGoogle Scholar
  48. Zehr EP (2006) Training-induced adaptive plasticity in human somatosensory reflex pathways. J Appl Physiol 101:1783–1794CrossRefPubMedGoogle Scholar
  49. Zehr EP, Klimstra M, Dragert K, Barzi Y, Bowden M, Javan B, Phadke C (2007a) Enhancement of arm and leg locomotor coupling with augmented cutaneous feedback from the hand. J Neurophysiol 98:1810–1814CrossRefPubMedGoogle Scholar
  50. Zehr EP, Klimstra M, Johnson EA, Carroll TJ (2007b) Rhythmic leg cycling modulates forearm muscle H-reflex amplitude and corticospinal tract excitability. Neurosci Lett 419:10–14CrossRefPubMedGoogle Scholar
  51. Zhou S (2000) Chronic adaptations to unilateral exercise: mechanisms of cross education. Ex Sport Sci Rev 29:177–184Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Rehabilitation Neuroscience LaboratoryUniversity of VictoriaVictoriaCanada
  2. 2.Centre for Biomedical ResearchUniversity of VictoriaVictoriaCanada
  3. 3.Human Discovery ScienceInternational Collaboration on Repair Discoveries (ICORD)VancouverCanada

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