Skip to main content
Log in

Neuro-Physiological Adaptations Associated with Cross-Education of Strength

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

Cross-education of strength is the increase in strength of the untrained contralateral limb after unilateral training of the opposite homologous limb. We investigated central and peripheral neural adaptations associated with cross-education of strength. Twenty-three right-handed females were randomized into a unilateral training group or an imagery group. A sub-sample of eight subjects (four training, four imagery) was assessed with functional magnetic resonance imaging (fMRI) for patterns of cortical activation during exercise. Strength training was 6 weeks of maximal isometric ulnar deviation of the right arm, four times per week. Peak torque, muscle thickness (ultrasound), agonist–antagonist electromyography (EMG), and fMRI were assessed before and after training. Strength training was highly effective for increasing strength in trained (45.3%; P < 0.01) and untrained (47.1%; P < 0.01) limbs. The imagery group showed no increase in strength for either arm. Muscle thickness increased only in the trained arm of the training group (8.4%; P < 0.001). After training, there was an enlarged region of activation in contralateral sensorimotor cortex and left temporal lobe during muscle contractions with the untrained left arm (P < 0.001). Training was associated with a significantly greater change in agonist muscle EMG pooled over both limbs, compared to the imagery group (P < 0.05). These results suggest that cross-education of strength may be partly controlled by adaptations within sensorimotor cortex, consistent with previous studies of motor learning. However, this research demonstrates the involvement of temporal lobe regions that subserve semantic memory for movement, which has not been previously studied in this context. We argue that temporal lobe regions might play a significant role in the cross-education of strength.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Arthurs OJ, Boniface S. How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci 2002;25: 27–31.

    Article  PubMed  CAS  Google Scholar 

  2. Binkofski F, Amunts K, Stephan KM, Posse S, Schormann T, Freund HJ, Zilles K, Seitz RJ. Broca’s region subserves imagery of motion: a combined cytoarchitectonic and fMRI study. Hum Brain Mapp 2000;11:273–85.

    Article  PubMed  CAS  Google Scholar 

  3. Borowsky R, Loehr J, Friesen CK, Kraushaar G, Kingstone A, Sarty G. Modularity and intersection of ‹what’, ‹where’, and ‹how’ processing of visual stimuli: a new method of fMRI localization. Brain Topogr 2005;18:67–75.

    Article  PubMed  Google Scholar 

  4. Bryden MP. Measuring handedness with questionnaires. Neuropsychologia 1977;15:617–24.

    Article  PubMed  CAS  Google Scholar 

  5. Carolan B, Cafarelli E. Adaptations in coactivation after isometric resistance training. J Appl Physiol 1992;73:911–7.

    PubMed  CAS  Google Scholar 

  6. Carroll TJ, Herbert RD, Munn J, Lee M, Gandevia SC. Contralateral effects of unilateral strength training: evidence and possible mechanisms. J Appl Physiol 2006;101:1514–22.

    Article  PubMed  Google Scholar 

  7. Cox RW. AFNI: software for analysis and visualization of functional MR neuroimages. Comput Biomed Res 1996;29: 162–73.

    Article  PubMed  CAS  Google Scholar 

  8. Ehrsson HH, Fagergren A, Jonsson T, Westling G, Johansson RS, Forssberg H. Cortical activity in precision- versus power-grip tasks: an fMRI study. J Neurophysiol 2000;83:528–36.

    PubMed  CAS  Google Scholar 

  9. Evetovich TK, Housh TJ, Housh DJ, Johnson GO, Smith DB, Ebersole KT. The effect of concentric isokinetic strength training of the quadriceps femoris on electromyography and muscle strength in the trained and untrained limb. J Strength Cond Res 2001;15:439–45.

    Article  PubMed  CAS  Google Scholar 

  10. Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol 2004;96:1486–95.

    Article  PubMed  Google Scholar 

  11. Farthing JP, Chilibeck PD. The effects of eccentric training at different velocities on cross-education. Eur J Appl Physiol 2003;89:570–7.

    Article  PubMed  Google Scholar 

  12. Farthing JP, Chilibeck PD, Binsted G. Cross-education of arm muscular strength is unidirectional in right-handed individuals. Med Sci Sports Exerc 2005;37:1594–600.

    Article  PubMed  Google Scholar 

  13. Farthing JP, Cummine J, Borowsky R, Chilibeck PD, Binsted G, Sarty GE. False activation in the brain ventricles related to task-correlated breathing in fMRI speech and motor paradigms. Magn Reson Mater Phy 2007;20:157–68.

    Article  Google Scholar 

  14. Gerardin E, Sirigu A, Lehericy S, Poline JB, Gaymard B, Marsault C, Agid Y, Le Bihan D. Partially overlapping neural networks for real and imagined hand movements. Cereb Cortex 2000;10:1093–104.

    Article  PubMed  CAS  Google Scholar 

  15. Ghez C. The cerebellum. In: Kandel ER, Schwartz JH, Jessell TM, editors. Principles of neural science. Norwalk, Connecticut: Appleton and Lange; 1991.

    Google Scholar 

  16. Gibala MJ, MacDougall JD, Sale DG. The effects of tapering on strength performance in trained athletes. Int J Sports Med 1994;15:492–7.

    Article  PubMed  CAS  Google Scholar 

  17. Grafton ST, Hazeltine E, Ivry RB. Functional anatomy of sequence learning in normal humans. J Cogn Neurosci 1995;7:497–510.

    Article  Google Scholar 

  18. Grafton ST, Hazeltine E, Ivry RB. Motor sequence learning with the nondominant left hand: a pet functional imaging study. Exp Brain Res 2002;146:369–78.

    Article  PubMed  Google Scholar 

  19. Hellebrandt FA. Cross education: ipsilateral and contralateral effects of unimanual training. J Appl Physiol 1991;4:136–44.

    Google Scholar 

  20. Herbert RD, Dean C, Gandevia SC. Effects of real and imagined training on voluntary muscle activation during isometric contractions. Acta Physiol Scand 1998;163:361–8.

    Article  PubMed  CAS  Google Scholar 

  21. Hortobágyi T. Cross education and the human central nervous system. IEEE Eng Med Biol Mag 2005;24:22–8.

    Article  PubMed  Google Scholar 

  22. Hortobágyi T, Lambert NJ, Hill JP. Greater cross-education following training with muscle lengthening than shortening. Med Sci Sports Exerc 1997;29:107–12.

    PubMed  Google Scholar 

  23. Imamizu H, Shimojo S. The locus of visual-motor learning at the task or manipulator level: implications from intermanual transfer. J Exp Psychol Hum Percept Perform 1995;21:719–33.

    Article  PubMed  CAS  Google Scholar 

  24. Ito M. Mechanisms of motor learning in the cerebellum. Brain Res 2000;886:237–45.

    Article  PubMed  CAS  Google Scholar 

  25. Jueptner M, Frith CD, Brooks DJ, Frackowiak RSJ, Passingham RE. Anatomy of motor Learning. II. Subcortical structures and learning by trial and error. J Neurophysiol 1997;77:1325–37.

    PubMed  CAS  Google Scholar 

  26. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 1995;377:155–8.

    Article  PubMed  CAS  Google Scholar 

  27. Kristeva R, Cheyne D, Deecke L. Neuromagnetic fields accompanying unilateral and bilateral voluntary movements: topography and analysis of cortical sources. Electroencephalogr Clin Neurophysiol 1991;81:284–98.

    Article  PubMed  CAS  Google Scholar 

  28. Lagerquist O, Zehr EP, Docherty D. Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect. J Appl Physiol 2006;100:83–90.

    Article  PubMed  Google Scholar 

  29. Lee M, Carroll TJ. Cross education: possible mechanisms for the contralateral effects of unilateral resistance training. Sports Med 2007;37:1–14.

    Article  PubMed  Google Scholar 

  30. Liu JZ, Dai TH, Elster TH, Sahgal V, Brown RW, Yue GH. Simultaneous measurement of human joint force, surface electromyograns, and functional MRI-measured brain activation. J Neurosci Method 2000, 101:49–57.

    Article  CAS  Google Scholar 

  31. Martin A. Functional neuroimaging of semantic memory. In: Cabeza R, Kingstone A editors. Functional neuroimaging of semantic memory. Cambridge: MIT; 2001.

    Google Scholar 

  32. Martin A, Haxby JV, Lalonde FM, Wiggs CL, Ungerleider LG. Discrete cortical regions associated with knowledge of color and knowledge of action. Science 1995;270:102–5.

    Article  PubMed  CAS  Google Scholar 

  33. Moritani T, deVries HA. Neural factors verses hypertrophy in the time course of muscle strength gain. Am J Phys Med 1979;58:115–30.

    PubMed  CAS  Google Scholar 

  34. Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Facchini S, Boroojerdi B, Poewe W, Hallet M. Early consolidation in human primary motor cortex. Nature 2002;415:640–44.

    Article  PubMed  CAS  Google Scholar 

  35. Munn J, Herbert RD, Gandevia SC. Contralateral effects of unilateral resistance training: a meta-analysis. J Appl Physiol 2004;96:1861–6.

    Article  PubMed  CAS  Google Scholar 

  36. Naito E, Kochiyama T, Kitada R, Nakamura S, Matsumura M, Yonekura Y, Sadato N. Internally simulated movement sensations during motor imagery activate cortical motor areas and the cerebellum. J Neurosci 2002;22:3683–91.

    PubMed  CAS  Google Scholar 

  37. Nirkko AC, Ozdoba C, Redmond SM, Burki M, Schroth G, Hess CW, Weisendanger M. Different ipsilateral representations for distal and proximal movements in the sensorimotor cortex: activation and deactivation patterns. NeuroImage 2001;13:825–35.

    Article  PubMed  CAS  Google Scholar 

  38. Obayashi S. Possible mechanism for transfer of motor skill learning: implication of the cerebellum. Cerebellum 2004;3: 204–11.

    Article  PubMed  Google Scholar 

  39. Parlow SE, Kinsbourne M. Asymmetrical transfer of training between hands: implications for interhemispheric communication in normal brain. Brain Cogn 1989;11:98–113.

    Article  PubMed  CAS  Google Scholar 

  40. Pascual-Leone A, Grafman J, Hallet M. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 1994;263:1287–9.

    Article  PubMed  CAS  Google Scholar 

  41. Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 1995;74:1037–45.

    PubMed  CAS  Google Scholar 

  42. Pearce AJ, Thickbroom GW, Byrnes ML. Functional reorganization of the corticomotor projection to the hand in skilled racquet players. Exp Brain Res 2000;130:238–43.

    Article  PubMed  CAS  Google Scholar 

  43. Ranganathan VK, Siemionow V, Liu JZ, Sahgal V, Yue GH. From mental power to muscle power-gaining strength by using the mind. Neuropsychol 2004;42:944–56.

    Article  Google Scholar 

  44. Romero DH, Lacourse MG, Lawrence KE, Schandler S, Cohen MJ. Event-related potentials as a function of movement parameter variations during motor imagery and isometric action. Behav Brain Res 2000;117:83–96.

    Article  PubMed  CAS  Google Scholar 

  45. Sakai K, Ramnani N, Passingham RE. Learning of sequences of finger movements and timing: frontal lobe and action-oriented representation. J Neurophysiol 2002;88:2035–46.

    PubMed  Google Scholar 

  46. Sanes JN. Neocortical mechanisms in motor learning. Cur Opin Neuro Biol 2003;13:225–31.

    Article  CAS  Google Scholar 

  47. Sarty GE, Borowsky R. Functional MRI activation maps from empirically defined curve fitting. Concepts Magn Reson Part B (Magn Reson Eng) 2005;24B:46–55.

    Article  Google Scholar 

  48. Shadmehr R, Holcomb HH. Neural correlates of motor memory consolidation. Science 1997;277:821–5.

    Article  PubMed  CAS  Google Scholar 

  49. Shima N, Ishida K, Katayama K, Morotome Y, Sato Y, Miyamura M. Cross education of muscular strength during unilateral resistance training and detraining. Eur J Appl Physiol 2002;86:287–94.

    Article  PubMed  Google Scholar 

  50. Sohn YH, Jung HY, Kaelin-Lang A, Hallett M. Effect of levetiracetam on rapid motor learning in humans. Arch Neurol 2002;59:1909–12.

    Article  PubMed  Google Scholar 

  51. Staines WR, Padilla M, Knight RT. Frontal-parietal event-related potential changes associated with practicing a novel visuomotor task. Brain Res Cogn Brain Res 2002;13:195–202.

    Article  PubMed  Google Scholar 

  52. Talairach J, Tournoux P. Co-Planar steroetaxic atlas of the human brain. Stuttgart: Theime; 1988.

    Google Scholar 

  53. Toma K, Honda M, Hanakawa T, Okada T, Fukuyama H, Ikeda A, Nishizawa S, Konishi J, Shibasaki H. Activities of the primary and supplementary motor areas increase in preperation and execution of voluntary muscle relaxation: an event-related fMRI study. J Neurosci 1999;19:3527–34.

    PubMed  CAS  Google Scholar 

  54. Tulving E. Elements of episodic memory. New York NY: Oxford University Press; 1983.

    Google Scholar 

  55. Yue G, Cole KJ. Strength increases from the motor program: comparison of training with maximal voluntary and imagined muscle contractions. J Neurophysiol 1992;67:1114–23.

    PubMed  CAS  Google Scholar 

  56. Zhou S. Chronic neural adaptations to unilateral exercise: mechanisms of cross-education. Exerc Sport Sci Rev 2000;28:177–84.

    PubMed  CAS  Google Scholar 

  57. Ziemann U, Muellbacher W, Hallett M, Cohen LG. Modulation of practice-dependent plasticity in human motor cortex. Brain 2001;124:1171–81.

    Article  PubMed  CAS  Google Scholar 

  58. Zijdewind I, Toering ST, Bessem B, Van Der Laan O, Diercks RL. Effects of imagery motor training on torque production of ankle plantar flexor muscles. Muscle Nerve 2003;28:168–73.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Jonathan Farthing was supported by a graduate scholarship from the Natural Sciences and Engineering Research Council of Canada. Gordon Sarty, Ron Borowsky, and Gord Binsted are each supported by grants from the Natural Sciences and Engineering Research Council of Canada, which contributed to this research. We acknowledge the technical support of Jennifer Hadley during the MRI scanning procedures and MRI data processing. We acknowledge Heather Whelan and Doug Jacobson for their technical assistance and support for the testing of participants.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathan P. Farthing.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Farthing, J.P., Borowsky, R., Chilibeck, P.D. et al. Neuro-Physiological Adaptations Associated with Cross-Education of Strength. Brain Topogr 20, 77–88 (2007). https://doi.org/10.1007/s10548-007-0033-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-007-0033-2

Keywords

Navigation