Effects of Cross-Education on Neural Adaptations Following Non-Paretic Limb Training in Stroke: A Scoping Review with Implications for Neurorehabilitation

References

• Barker, R. N., Brauer, S. G., Barry, B. K., Gill, T. J., & Carson, R. G. (2012). Training-induced modifications of corticospinal reactivity in severely affected stroke survivors. Experimental Brain Research, 221(2), 211–221.
   PubMed Web of Science ®Google Scholar
• Bradnam, L. V., Stinear, C. M., Barber, P. A., & Byblow, W. D. (2012). Contralesional hemisphere control of the proximal paretic upper limb following stroke. Cerebral Cortex (New York, N.Y.: 1991), 22(11), 2662–2671.
   PubMed Web of Science ®Google Scholar
• Bradnam, L. V., Stinear, C. M., & Byblow, W. D. (2013). Ipsilateral motor pathways after stroke: Implications for non-invasive brain stimulation. Frontiers in Human Neuroscience, 7, 184.
   PubMed Web of Science ®Google Scholar
• Buetefisch, C. M. (2015). Role of the contralesional hemisphere in post-stroke recovery of upper extremity motor function. Frontiers in Neurology, 6, 214. https://doi.org/10.3389/fneur.2015.00214
   PubMed Web of Science ®Google Scholar
• Carroll, T. J., Lee, M., Hsu, M., & Sayde, J. (2008). Unilateral practice of a ballistic movement causes bilateral increases in performance and corticospinal excitability. Journal of Applied Physiology (Bethesda, Md.: 1985), 104(6), 1656–1664.
   PubMed Web of Science ®Google Scholar
• Chen, R., Lozano, A. M., & Ashby, P. (1999). Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Experimental Brain Research, 128(4), 539–542.
   PubMed Web of Science ®Google Scholar
• Chen, R., Tam, A., Bütefisch, C., Corwell, B., Ziemann, U., Rothwell, J. C., & Cohen, L. G. (1998). Intracortical inhibition and facilitation in different representations of the human motor cortex. Journal of Neurophysiology, 80(6), 2870–2881.
   PubMed Web of Science ®Google Scholar
• Cirer-Sastre, R., Beltrán-Garrido, J. V., & Corbi, F. (2017). Contralateral effects after unilateral strength training: A meta-analysis comparing training loads. Journal of Sports Science & Medicine, 16(2), 180–186.
   PubMed Web of Science ®Google Scholar
• Colomer-Poveda, D., Romero-Arenas, S., Hortobagyi, T., & Márquez, G. (2019). Does ipsilateral corticospinal excitability play a decisive role in the cross-education effect caused by unilateral resistance training? A systematic review. Neurología (English Edition).
   Google Scholar
• Colomer-Poveda, D., Romero-Arenas, S., Keller, M., Hortobágyi, T., & Márquez, G. (2019). Effects of acute and chronic unilateral resistance training variables on ipsilateral motor cortical excitability and cross-education: A systematic review. Physical Therapy in Sport: Official Journal of the Association of Chartered Physiotherapists in Sports Medicine, 40, 143–152.
   PubMed Web of Science ®Google Scholar
• Dai, T. H., Liu, J. Z., Sahgal, V., Brown, R. W., & Yue, G. H. (2001). Relationship between muscle output and functional MRI-measured brain activation. Experimental Brain Research, 140(3), 290–300.
   PubMed Web of Science ®Google Scholar
• Dehno, N., Kamali, F., Shariat, A., & Jaberzadeh, S. (2021). Unilateral strength training of the less affected hand improves cortical excitability and clinical outcomes in patients with subacute stroke: A randomized controlled trial. Archives of Physical Medicine and Rehabilitation, 102(5), 914–924.
   PubMed Web of Science ®Google Scholar
• Dobkin, B. H. (2004). Strategies for stroke rehabilitation. The Lancet Neurology, 3(9), 528–536.
   PubMed Web of Science ®Google Scholar
• Dragert, K., & Zehr, E. P. (2011). Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors. Experimental Brain Research, 208(2), 217–227. https://doi.org/10.1007/s00221-010-2472-3
   PubMed Web of Science ®Google Scholar
• Dragert, K., & Zehr, E. P. (2013). High-intensity unilateral dorsiflexor resistance training results in bilateral neuromuscular plasticity after stroke. Experimental Brain Research, 225(1), 93–104. https://doi.org/10.1007/s00221-012-3351-x
   PubMed Web of Science ®Google Scholar
• Ehrensberger, M., Simpson, D., Broderick, P., Blake, C., Horgan, F., Hickey, P., OʼReilly, J., & Monaghan, K. (2019). Unilateral strength training and mirror therapy in patients with chronic stroke: A pilot randomized trial. American Journal of Physical Medicine & Rehabilitation, 98(8), 657–665. https://doi.org/10.1097/PHM.0000000000001162
   PubMed Web of Science ®Google Scholar
• Farthing, J. P. (2009). Cross-education of strength depends on limb dominance: Implications for theory and application. Exercise and Sport Sciences Reviews, 37(4), 179–187. https://doi.org/10.1097/JES.0b013e3181b7e882
   PubMed Web of Science ®Google Scholar
• Farthing, J. P., Borowsky, R., Chilibeck, P. D., Binsted, G., & Sarty, G. E. (2007). Neuro-physiological adaptations associated with cross-education of strength. Brain Topography, 20(2), 77–88. https://doi.org/10.1007/s10548-007-0033-2
   PubMed Web of Science ®Google Scholar
• Farthing, J. P., Krentz, J. R., Magnus, C. R., Barss, T. S., Lanovaz, J. L., Cummine, J., Esopenko, C., Sarty, G. E., & Borowsky, R. (2011). Changes in functional magnetic resonance imaging cortical activation with cross education to an immobilized limb. Medicine & Science in Sports & Exercise, 43(8), 1394–1405. https://doi.org/10.1249/MSS.0b013e318210783c
   PubMed Web of Science ®Google Scholar
• Frazer, A. K., Pearce, A. J., Howatson, G., Thomas, K., Goodall, S., & Kidgell, D. J. (2018). Determining the potential sites of neural adaptation to cross-education: Implications for the cross-education of muscle strength. European Journal of Applied Physiology, 118(9), 1751–1772.
   PubMed Web of Science ®Google Scholar
• French, B., Thomas, L. H., Coupe, J., McMahon, N. E., Connell, L., Harrison, J., Sutton, C. J., Tishkovskaya, S., Watkins, C. L., & Thomas, L. H. (2016). Repetitive task training for improving functional ability after stroke. The Cochrane Database of Systematic Reviews, 11(11), CD006073. https://doi.org/10.1002/14651858.CD006073.pub3
   PubMed Web of Science ®Google Scholar
• Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Blaha, M. J., Dai, S., Ford, E. S., Fox, C. S., Franco, S., Fullerton, H. J., Gillespie, C., Hailpern, S. M., Heit, J. A., Howard, V. J., Huffman, M. D., Judd, S. E., Kissela, B. M., Kittner, S. J., … Stroke Statistics, S, American Heart Association Statistics Committee and Stroke Statistics Subcommittee (2014). Heart disease and stroke statistics–2014 update: A report from the American Heart Association. Circulation (New York, N.Y, ), 129(3), e28–e292. https://doi.org/10.1161/01.cir.0000441139.02102.80
   Web of Science ®Google Scholar
• Goodwill, A. M., Pearce, A. J., & Kidgell, D. J. (2012). Corticomotor plasticity following unilateral strength training. Muscle & Nerve, 46(3), 384–393.
   PubMed Web of Science ®Google Scholar
• Green, L. A., & Gabriel, D. A. (2018). The effect of unilateral training on contralateral limb strength in young, older, and patient populations: A meta-analysis of cross education. Physical Therapy Reviews, 23(4-5), 238–249. https://doi.org/10.1080/10833196.2018.1499272
   Web of Science ®Google Scholar
• Harris, J. E., & Eng, J. J. (2010). Strength training improves upper-limb function in individuals with stroke: A meta-analysis. Stroke, 41(1), 136–140. https://doi.org/10.1161/STROKEAHA.109.567438
   PubMed Web of Science ®Google Scholar
• Hinder, M. R., Carroll, T. J., & Summers, J. J. (2013). Inter-limb transfer of ballistic motor skill following non-dominant limb training in young and older adults. Experimental Brain Research, 227(1), 19–29. https://doi.org/10.1007/s00221-013-3481-9
   PubMed Web of Science ®Google Scholar
• Hortobagyi, T., Richardson, S. P., Lomarev, M., Shamim, E., Meunier, S., Russman, H., Dang, N., & Hallett, M. (2011). Interhemispheric plasticity in humans. Medicine & Science in Sports & Exercise, 43(7), 1188–1199. https://doi.org/10.1249/MSS.0b013e31820a94b8
   PubMed Web of Science ®Google Scholar
• Jorgensen, H. S., Nakayama, H., Raaschou, H. O., & Olsen, T. S. (1995). Recovery of walking function in stroke patients: The Copenhagen Stroke Study. Archives of Physical Medicine and Rehabilitation, 76(1), 27–32. https://doi.org/10.1016/S0003-9993(95)80038-7
   PubMed Web of Science ®Google Scholar
• Kidgell, D. J., Frazer, A. K., Daly, R. M., Rantalainen, T., Ruotsalainen, I., Ahtiainen, J., Avela, J., & Howatson, G. (2015). Increased cross-education of muscle strength and reduced corticospinal inhibition following eccentric strength training. Neuroscience, 300, 566–575.
   PubMed Web of Science ®Google Scholar
• Kidgell, D. J., & Pearce, A. J. (2010). Corticospinal properties following short-term strength training of an intrinsic hand muscle. Human Movement Science, 29(5), 631–641.
   PubMed Web of Science ®Google Scholar
• Kidgell, D. J., Stokes, M. A., & Pearce, A. J. (2011). Strength training of one limb increases corticomotor excitability projecting to the contralateral homologous limb. Motor Control, 15(2), 247–266. https://doi.org/10.1123/mcj.15.2.247
   PubMed Web of Science ®Google Scholar
• Kim, C. Y., & Kim, H. D. (2018). Effect of crossed-education using a tilt table task-oriented approach in subjects with post-stroke hemiplegia: A randomized controlled trial. Journal of Rehabilitation Medicine, 50(9), 792–799. https://doi.org/10.2340/16501977-2376
   PubMed Web of Science ®Google Scholar
• Kleim, J. A., & Jones, T. A. (2008). Principles of experience-dependent neural plasticity: Implications for rehabilitation after brain damage. Journal of Speech, Language, and Hearing Research: JSLHR, 51(1), S225–S239.
   PubMed Web of Science ®Google Scholar
• Kobayashi, M., Hutchinson, S., Schlaug, G., & Pascual-Leone, A. (2003). Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions. NeuroImage, 20(4), 2259–2270.
   PubMed Web of Science ®Google Scholar
• van Kuijk, A. A., Pasman, J. W., Geurts, A. C. H., & Hendricks, H. T. (2005). How salient is the silent period? The role of the silent period in the prognosis of upper extremity motor recovery after severe stroke. Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society, 22(1), 10–24.
   PubMed Web of Science ®Google Scholar
• Kujirai, T., Caramia, M. D., Rothwell, J. C., Day, B. L., Thompson, P. D., Ferbert, A., Wroe, S., Asselman, P., & Marsden, C. D. (1993). Corticocortical inhibition in human motor cortex. The Journal of Physiology, 471, 501–519.
   PubMed Web of Science ®Google Scholar
• Latella, C., Kidgell, D. J., & Pearce, A. J. (2012). Reduction in corticospinal inhibition in the trained and untrained limb following unilateral leg strength training. European Journal of Applied Physiology, 112(8), 3097–3107.
   PubMed Web of Science ®Google Scholar
• Lee, M., Hinder, M. R., Gandevia, S. C., & Carroll, T. J. (2010). The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. The Journal of Physiology, 588(Pt 1), 201–212.
   PubMed Web of Science ®Google Scholar
• Leung, M., Rantalainen, T., Teo, W.-P., & Kidgell, D. (2018). The ipsilateral corticospinal responses to cross-education are dependent upon the motor-training intervention. Experimental Brain Research, 236(5), 1331–1346.
   PubMed Web of Science ®Google Scholar
• Leung, M., Rantalainen, T., Teo, W. P., & Kidgell, D. (2015). Motor cortex excitability is not differentially modulated following skill and strength training. Neuroscience, 305, 99–108. https://doi.org/10.1016/j.neuroscience.2015.08.007
   PubMed Web of Science ®Google Scholar
• Maher, C. G., Sherrington, C., Herbert, R. D., Moseley, A. M., & Elkins, M. (2003). Reliability of the PEDro scale for rating quality of randomized controlled trials. Physical Therapy, 83(8), 713–721.
   PubMed Web of Science ®Google Scholar
• Manca, A., Dragone, D., Dvir, Z., & Deriu, F. (2017). Cross-education of muscular strength following unilateral resistance training: A meta-analysis. European Journal of Applied Physiology, 117(11), 2335–2354.
   PubMed Web of Science ®Google Scholar
• Manca, A., Ginatempo, F., Cabboi, M. P., Mercante, B., Ortu, E., Dragone, D., De Natale, E. R., Dvir, Z., Rothwell, J. C., & Deriu, F. (2016). No evidence of neural adaptations following chronic unilateral isometric training of the intrinsic muscles of the hand: A randomized controlled study. European Journal of Applied Physiology, 116(10), 1993–2005. https://doi.org/10.1007/s00421-016-3451-6
   PubMed Web of Science ®Google Scholar
• Manca, A., Hortobagyi, T., Rothwell, J., & Deriu, F. (2018). Neurophysiological adaptations in the untrained side in conjunction with cross-education of muscle strength: A systematic review and meta-analysis. Journal of Applied Physiology, 124(6), 1502–1518. https://doi.org/10.1152/japplphysiol.01016.2017
   PubMed Web of Science ®Google Scholar
• Mason, J., Frazer, A. K., Horvath, D. M., Pearce, A. J., Avela, J., Howatson, G., & Kidgell, D. J. (2018). Ipsilateral corticomotor responses are confined to the homologous muscle following cross-education of muscular strength. Applied Physiology. Nutrition, and Metabolism, 43(1), 11–22.
   Google Scholar
• McCambridge, A. B., Stinear, J. W., & Byblow, W. D. (2018). Revisiting interhemispheric imbalance in chronic stroke: A tDCS study. Clinical Neurophysiology, 129(1), 42–50. https://doi.org/10.1016/j.clinph.2017.10.016
   PubMed Web of Science ®Google Scholar
• Meyer, B. U., Röricht, S., Schmierer, K., Irlbacher, K., Meierkord, H., Niehaus, L., & Grosse, P. (1999). First diagnostic applications of transcallosal inhibition in diseases affecting callosal neurones (multiple sclerosis, hydrocephalus, Huntington's disease). Electroencephalography and Clinical Neurophysiology. Supplement, 51, 233–242.
   PubMedGoogle Scholar
• Misawa, S., Kuwabara, S., Matsuda, S., Honma, K., Ono, J., & Hattori, T. (2008). The ipsilateral cortico-spinal tract is activated after hemiparetic stroke. European Journal of Neurology, 15(7), 706–711. https://doi.org/10.1111/j.1468-1331.2008.02168.x
   PubMed Web of Science ®Google Scholar
• Moriello, C., Finch, L., & Mayo, N. E. (2011). Relationship between muscle strength and functional walking capacity among people with stroke. The Journal of Rehabilitation Research and Development, 48(3), 267–275. https://doi.org/10.1682/JRRD.2010.04.0066
   PubMed Web of Science ®Google Scholar
• Palmer, H. S., Håberg, A. K., Fimland, M. S., Solstad, G. M., Iversen, V. M., Hoff, J., Helgerud, J., & Eikenes, L. (2013). Structural brain changes after 4 wk of unilateral strength training of the lower limb. Journal of Applied Physiology (Bethesda, Md.: 1985), 115(2), 167–175.
   PubMed Web of Science ®Google Scholar
• Perez, M. A., & Cohen, L. G. (2008). Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. Journal of Neuroscience, 28(22), 5631–5640. https://doi.org/10.1523/JNEUROSCI.0093-08.2008
   PubMed Web of Science ®Google Scholar
• Ruddy, K. L., & Carson, R. G. (2013). Neural pathways mediating cross education of motor function. Frontiers in Human Neuroscience, 7, 397.
   PubMed Web of Science ®Google Scholar
• Ruddy, K. L., Leemans, A., Woolley, D. G., Wenderoth, N., & Carson, R. G. (2017). Structural and functional cortical connectivity mediating cross education of motor function. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 37(10), 2555–2564.
   PubMed Web of Science ®Google Scholar
• Simpson, D., Ehrensberger, M., Horgan, F., Blake, C., Roberts, D., Broderick, P., & Monaghan, K. (2019). Unilateral dorsiflexor strengthening with mirror therapy to improve motor function after stroke: A pilot randomized study. Physiotherapy Research International: The Journal for Researchers and Clinicians in Physical Therapy, 24(4), e1792.
   PubMed Web of Science ®Google Scholar
• Sohn, Y. H., Wiltz, K., & Hallett, M. (2002). Effect of volitional inhibition on cortical inhibitory mechanisms. Journal of Neurophysiology, 88(1), 333–338.
   PubMed Web of Science ®Google Scholar
• Stinear, C. M., Lang, C. E., Zeiler, S., & Byblow, W. D. (2020). Advances and challenges in stroke rehabilitation. The Lancet Neurology, 19(4), 348–360. https://doi.org/10.1016/S1474-4422(19)30415-6
   PubMed Web of Science ®Google Scholar
• Stoykov, M. E., Corcos, D. M., & Madhavan, S. (2017). Movement-based priming: Clinical applications and neural mechanisms. Journal of Motor Behavior, 49(1), 88–97.
   PubMed Web of Science ®Google Scholar
• Sun, Y., Ledwell, N. M. H., Boyd, L. A., & Zehr, E. P. (2018). Unilateral wrist extension training after stroke improves strength and neural plasticity in both arms. Experimental Brain Research, 236(7), 2009–2021. https://doi.org/10.1007/s00221-018-5275-6
   PubMed Web of Science ®Google Scholar
• Tricco, A. C., Lillie, E., Zarin, W., O'Brien, K. K., Colquhoun, H., Levac, D., Moher, D., Peters, M. D. J., Horsley, T., Weeks, L., Hempel, S., Akl, E. A., Chang, C., McGowan, J., Stewart, L., Hartling, L., Aldcroft, A., Wilson, M. G., Garritty, C., … Straus, S. E. (2018). PRISMA Extension for Scoping Reviews (PRISMA-ScR): Checklist and explanation. Annals of Internal Medicine, 169(7), 467–473.
   PubMed Web of Science ®Google Scholar
• Urbin, M. A., Harris-Love, M. L., Carter, A. R., & Lang, C. E. (2015). High-intensity, unilateral resistance training of a non-paretic muscle group increases active range of motion in a severely paretic upper extremity muscle group after stroke. Frontiers in Neurology, 6, 119. https://doi.org/10.3389/fneur.2015.00119
   PubMed Web of Science ®Google Scholar
• Zhou, S. (2000). Chronic neural adaptations to unilateral exercise: Mechanisms of cross education. Exercise and Sport Sciences Reviews, 28(4), 177–184.
   PubMedGoogle Scholar
• Zult, T., Goodall, S., Thomas, K., Solnik, S., Hortobagyi, T., & Howatson, G. (2016). Mirror training augments the cross-education of strength and affects inhibitory paths. Medicine and Science in Sports and Exercise, 48(6), 1001–1013. https://doi.org/10.1249/MSS.0000000000000871
   PubMed Web of Science ®Google Scholar