Skip to main content
Top
Published in: Sports Medicine 2/2014

01-02-2014 | Review Article

Role of the Mirror-Neuron System in Cross-Education

Authors: Tjerk Zult, Glyn Howatson, Endre E. Kádár, Jonathan P. Farthing, Tibor Hortobágyi

Published in: Sports Medicine | Issue 2/2014

Login to get access

Abstract

The present review proposes the untested hypothesis that cross-education performed with a mirror increases the transfer of motor function to the resting limb compared with standard cross-education interventions without a mirror. The hypothesis is based on neuroanatomical evidence suggesting an overlap in activated brain areas when a unilateral motor task is performed with and without a mirror in the context of cross-education of the upper extremities. The review shows that the mirror-neuron system (MNS), connecting sensory neurons responding to visual properties of an observed action and motor neurons that discharge action potentials during the execution of a similar action, has the potential to enhance cross-education. After a literature search we narrowed the review to studies that examined healthy young adults who performed unilateral strength training and unilateral motor tasks with or without a mirror and assessed outcome measures in relation to the changes in brain activity, motor cortical excitability, and corticospinal excitability. We identified six chronic studies that examined the effects of unilateral strength training on neural adaptations and 15 cross-sectional studies that examined acute changes in brain activation, motor cortical and corticospinal excitability using imaging, electroencephalographic, magnetoencephalographic, and magnetic brain stimulation. There were two chronic and nine cross-sectional studies in which participants performed unilateral motor tasks while viewing the image of the active hand superimposed on the resting hand’s image. Collectively, the data suggest that the MNS is involved in cross-education and the hypothesis is tenable. However, future studies are needed to elucidate the precise mechanism of how the use of a mirror in a cross-education study augments transfer to the non-exercised limb. Recent studies show a strength-sparing effect in the immobilized arm after strength training of the free arm in healthy individuals, and improved bilateral function after unilateral exercise therapy in stroke patients. It is thus conceptually justified to conduct randomized clinical trials that supplement cross-education protocols with a mirror. Such a treatment could reduce muscle weakness caused by limb fractures, anterior-cruciate ligament reconstruction surgery, stroke, and other unilateral motor dysfunctions.
Appendix
Available only for authorised users
Literature
1.
go back to reference Piaget J. Play, dreams, and imitation in childhood. London: Routledge; 1951. Piaget J. Play, dreams, and imitation in childhood. London: Routledge; 1951.
2.
go back to reference Rizzolatti G, Fadiga L, Fogassi L, Gallese V. Resonance behaviors and mirror neurons. Arch Ital Biol. 1999;137(2–3):85–100.PubMed Rizzolatti G, Fadiga L, Fogassi L, Gallese V. Resonance behaviors and mirror neurons. Arch Ital Biol. 1999;137(2–3):85–100.PubMed
5.
6.
go back to reference Rizzolatti G, Fadiga L, Matelli M, Bettinardi V, Paulesu E, Perani D, et al. Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp Brain Res. 1996;111(2):246–52.PubMedCrossRef Rizzolatti G, Fadiga L, Matelli M, Bettinardi V, Paulesu E, Perani D, et al. Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp Brain Res. 1996;111(2):246–52.PubMedCrossRef
7.
go back to reference Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G. Cortical mechanisms of human imitation. Science. 1999;286(5449):2526–8.PubMedCrossRef Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G. Cortical mechanisms of human imitation. Science. 1999;286(5449):2526–8.PubMedCrossRef
8.
go back to reference Iacoboni M, Koski LM, Brass M, Bekkering H, Woods RP, Dubeau MC, et al. Reafferent copies of imitated actions in the right superior temporal cortex. Proc Natl Acad Sci USA. 2001;98(24):13995–9.PubMedCrossRef Iacoboni M, Koski LM, Brass M, Bekkering H, Woods RP, Dubeau MC, et al. Reafferent copies of imitated actions in the right superior temporal cortex. Proc Natl Acad Sci USA. 2001;98(24):13995–9.PubMedCrossRef
9.
go back to reference Farthing JP, Borowsky R, Chilibeck PD, Binsted G, Sarty GE. Neuro-physiological adaptations associated with cross-education of strength. Brain Topogr. 2007 Winter;20(2):77–8. Farthing JP, Borowsky R, Chilibeck PD, Binsted G, Sarty GE. Neuro-physiological adaptations associated with cross-education of strength. Brain Topogr. 2007 Winter;20(2):77–8.
10.
go back to reference Hortobágyi T. Cross education and the human central nervous system. IEEE Eng Med Biol Mag. 2005;24(1):22–8.PubMedCrossRef Hortobágyi T. Cross education and the human central nervous system. IEEE Eng Med Biol Mag. 2005;24(1):22–8.PubMedCrossRef
11.
go back to reference Zhou S. Chronic neural adaptations to unilateral exercise: mechanisms of cross education. Exerc Sport Sci Rev. 2000;28(4):177–84.PubMed Zhou S. Chronic neural adaptations to unilateral exercise: mechanisms of cross education. Exerc Sport Sci Rev. 2000;28(4):177–84.PubMed
12.
go back to reference Munn J, Herbert RD, Gandevia SC. Contralateral effects of unilateral resistance training: a meta-analysis. J Appl Physiol. 2004;96(5):1861–6.PubMedCrossRef Munn J, Herbert RD, Gandevia SC. Contralateral effects of unilateral resistance training: a meta-analysis. J Appl Physiol. 2004;96(5):1861–6.PubMedCrossRef
13.
go back to reference Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, et al. Interhemispheric plasticity in humans. Med Sci Sports Exerc. 2011;43(7):1188–99.PubMedCrossRef Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, et al. Interhemispheric plasticity in humans. Med Sci Sports Exerc. 2011;43(7):1188–99.PubMedCrossRef
14.
go back to reference 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(5):1514–22.PubMedCrossRef 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(5):1514–22.PubMedCrossRef
15.
go back to reference Howatson G, Taylor MB, Rider P, Motawar BR, McNally MP, Solnik S, et al. Ipsilateral motor cortical responses to TMS during lengthening and shortening of the contralateral wrist flexors. Eur J Neurosci. 2011;33(5):978–90.PubMedCentralPubMedCrossRef Howatson G, Taylor MB, Rider P, Motawar BR, McNally MP, Solnik S, et al. Ipsilateral motor cortical responses to TMS during lengthening and shortening of the contralateral wrist flexors. Eur J Neurosci. 2011;33(5):978–90.PubMedCentralPubMedCrossRef
16.
go back to reference Ruddy KL, Carson RG. Neural pathways mediating cross education of motor function. Front Hum Neurosci. 2013;29(7):397. Ruddy KL, Carson RG. Neural pathways mediating cross education of motor function. Front Hum Neurosci. 2013;29(7):397.
17.
go back to reference Howatson G, Zult T, Farthing JP, Zijdewind I, Hortobágyi T. Mirror training to augment cross-education during resistance training: a hypothesis. Front Hum Neurosci. 2013;24(7):396. Howatson G, Zult T, Farthing JP, Zijdewind I, Hortobágyi T. Mirror training to augment cross-education during resistance training: a hypothesis. Front Hum Neurosci. 2013;24(7):396.
18.
go back to reference Farthing JP, Krentz JR, Magnus CR, Barss TS, Lanovaz JL, Cummine J, et al. Changes in functional magnetic resonance imaging cortical activation with cross education to an immobilized limb. Med Sci Sports Exerc. 2011;43(8):1394–405.PubMedCrossRef Farthing JP, Krentz JR, Magnus CR, Barss TS, Lanovaz JL, Cummine J, et al. Changes in functional magnetic resonance imaging cortical activation with cross education to an immobilized limb. Med Sci Sports Exerc. 2011;43(8):1394–405.PubMedCrossRef
19.
go back to reference Matthys K, Smits M, Van der Geest JN, Van der Lugt A, Seurinck R, Stam HJ, et al. Mirror-induced visual illusion of hand movements: a functional magnetic resonance imaging study. Arch Phys Med Rehabil. 2009;90(4):675–81.PubMedCrossRef Matthys K, Smits M, Van der Geest JN, Van der Lugt A, Seurinck R, Stam HJ, et al. Mirror-induced visual illusion of hand movements: a functional magnetic resonance imaging study. Arch Phys Med Rehabil. 2009;90(4):675–81.PubMedCrossRef
20.
go back to reference Nojima I, Mima T, Koganemaru S, Thabit MN, Fukuyama H, Kawamata T. Human motor plasticity induced by mirror visual feedback. J Neurosci. 2012;32(4):1293–300.PubMedCrossRef Nojima I, Mima T, Koganemaru S, Thabit MN, Fukuyama H, Kawamata T. Human motor plasticity induced by mirror visual feedback. J Neurosci. 2012;32(4):1293–300.PubMedCrossRef
21.
go back to reference Thieme H, Mehrholz J, Pohl M, Behrens J, Dohle C. Mirror therapy for improving motor function after stroke. Cochrane Database Syst Rev. 2012;(3):CD008449. Thieme H, Mehrholz J, Pohl M, Behrens J, Dohle C. Mirror therapy for improving motor function after stroke. Cochrane Database Syst Rev. 2012;(3):CD008449.
22.
go back to reference Bowering KJ, O’Connell NE, Tabor A, Catley MJ, Leake HB, Moseley GL, et al. The effects of graded motor imagery and its components on chronic pain: a systematic review and meta-analysis. J Pain. 2013;14(1):3–13.PubMedCrossRef Bowering KJ, O’Connell NE, Tabor A, Catley MJ, Leake HB, Moseley GL, et al. The effects of graded motor imagery and its components on chronic pain: a systematic review and meta-analysis. J Pain. 2013;14(1):3–13.PubMedCrossRef
23.
go back to reference Läppchen CH, Ringer T, Blessin J, Seidel G, Grieshammer S, Lange R, et al. Optical illusion alters M1 excitability after mirror therapy: a TMS study. J Neurophysiol. 2012;108(10):2857–61.PubMedCrossRef Läppchen CH, Ringer T, Blessin J, Seidel G, Grieshammer S, Lange R, et al. Optical illusion alters M1 excitability after mirror therapy: a TMS study. J Neurophysiol. 2012;108(10):2857–61.PubMedCrossRef
24.
go back to reference Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recognition in the premotor cortex. Brain. 1996;119(Pt 2):593–609.PubMedCrossRef Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recognition in the premotor cortex. Brain. 1996;119(Pt 2):593–609.PubMedCrossRef
25.
go back to reference Rizzolatti G, Fadiga L, Gallese V, Fogassi L. Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res. 1996;3(2):131–41.PubMedCrossRef Rizzolatti G, Fadiga L, Gallese V, Fogassi L. Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res. 1996;3(2):131–41.PubMedCrossRef
26.
go back to reference Buccino G, Binkofski F, Riggio L. The mirror neuron system and action recognition. Brain Lang. 2004;89(2):370–6.PubMedCrossRef Buccino G, Binkofski F, Riggio L. The mirror neuron system and action recognition. Brain Lang. 2004;89(2):370–6.PubMedCrossRef
27.
29.
go back to reference Small SL, Buccino G, Solodkin A. The mirror neuron system and treatment of stroke. Dev Psychobiol. 2012;54(3):293–310.PubMedCrossRef Small SL, Buccino G, Solodkin A. The mirror neuron system and treatment of stroke. Dev Psychobiol. 2012;54(3):293–310.PubMedCrossRef
30.
go back to reference Jeannerod M. Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage. 2001;14(1 Pt 2):S103–9.PubMedCrossRef Jeannerod M. Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage. 2001;14(1 Pt 2):S103–9.PubMedCrossRef
31.
go back to reference Caspers S, Zilles K, Laird AR, Eickhoff SB. ALE meta-analysis of action observation and imitation in the human brain. Neuroimage. 2010;50(3):1148–67.PubMedCrossRef Caspers S, Zilles K, Laird AR, Eickhoff SB. ALE meta-analysis of action observation and imitation in the human brain. Neuroimage. 2010;50(3):1148–67.PubMedCrossRef
32.
go back to reference Grezes J, Decety J. Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia. 2002;40(2):212–22.PubMedCrossRef Grezes J, Decety J. Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia. 2002;40(2):212–22.PubMedCrossRef
33.
go back to reference Molenberghs P, Cunnington R, Mattingley JB. Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci Biobehav Rev. 2012;36(1):341–9.PubMedCrossRef Molenberghs P, Cunnington R, Mattingley JB. Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci Biobehav Rev. 2012;36(1):341–9.PubMedCrossRef
34.
go back to reference Munzert J, Lorey B, Zentgraf K. Cognitive motor processes: the role of motor imagery in the study of motor representations. Brain Res Rev. 2009;60(2):306–26.PubMedCrossRef Munzert J, Lorey B, Zentgraf K. Cognitive motor processes: the role of motor imagery in the study of motor representations. Brain Res Rev. 2009;60(2):306–26.PubMedCrossRef
35.
go back to reference Brighina F, La Bua V, Oliveri M, Piazza A, Fierro B. Magnetic stimulation study during observation of motor tasks. J Neurol Sci. 2000;174(2):122–6.PubMedCrossRef Brighina F, La Bua V, Oliveri M, Piazza A, Fierro B. Magnetic stimulation study during observation of motor tasks. J Neurol Sci. 2000;174(2):122–6.PubMedCrossRef
36.
go back to reference Clark DJ, Patten C. Eccentric versus concentric resistance training to enhance neuromuscular activation and walking speed following stroke. Neurorehabil Neural Repair. 2013;27(4):335-44. Clark DJ, Patten C. Eccentric versus concentric resistance training to enhance neuromuscular activation and walking speed following stroke. Neurorehabil Neural Repair. 2013;27(4):335-44.
37.
go back to reference Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol. 1995;73(6):2608–11.PubMed Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol. 1995;73(6):2608–11.PubMed
38.
go back to reference Patuzzo S, Fiaschi A, Manganotti P. Modulation of motor cortex excitability in the left hemisphere during action observation: a single- and paired-pulse transcranial magnetic stimulation study of self- and non-self-action observation. Neuropsychologia. 2003;41(9):1272–8.PubMedCrossRef Patuzzo S, Fiaschi A, Manganotti P. Modulation of motor cortex excitability in the left hemisphere during action observation: a single- and paired-pulse transcranial magnetic stimulation study of self- and non-self-action observation. Neuropsychologia. 2003;41(9):1272–8.PubMedCrossRef
39.
go back to reference Roosink M, Zijdewind I. Corticospinal excitability during observation and imagery of simple and complex hand tasks: implications for motor rehabilitation. Behav Brain Res. 2010;213(1):35–41.PubMedCrossRef Roosink M, Zijdewind I. Corticospinal excitability during observation and imagery of simple and complex hand tasks: implications for motor rehabilitation. Behav Brain Res. 2010;213(1):35–41.PubMedCrossRef
40.
go back to reference Rossini PM, Rossi S, Pasqualetti P, Tecchio F. Corticospinal excitability modulation to hand muscles during movement imagery. Cereb Cortex. 1999;9(2):161–7.PubMedCrossRef Rossini PM, Rossi S, Pasqualetti P, Tecchio F. Corticospinal excitability modulation to hand muscles during movement imagery. Cereb Cortex. 1999;9(2):161–7.PubMedCrossRef
41.
go back to reference Buccino G, Vogt S, Ritzl A, Fink GR, Zilles K, Freund HJ, et al. Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron. 2004;42(2):323–34.PubMedCrossRef Buccino G, Vogt S, Ritzl A, Fink GR, Zilles K, Freund HJ, et al. Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron. 2004;42(2):323–34.PubMedCrossRef
42.
go back to reference Rowe JB, Toni I, Josephs O, Frackowiak RS, Passingham RE. The prefrontal cortex: response selection or maintenance within working memory? Science. 2000;288(5471):1656–60.PubMedCrossRef Rowe JB, Toni I, Josephs O, Frackowiak RS, Passingham RE. The prefrontal cortex: response selection or maintenance within working memory? Science. 2000;288(5471):1656–60.PubMedCrossRef
43.
go back to reference Imamizu H, Kuroda T, Yoshioka T, Kawato M. Functional magnetic resonance imaging examination of two modular architectures for switching multiple internal models. J Neurosci. 2004;24(5):1173–81.PubMedCrossRef Imamizu H, Kuroda T, Yoshioka T, Kawato M. Functional magnetic resonance imaging examination of two modular architectures for switching multiple internal models. J Neurosci. 2004;24(5):1173–81.PubMedCrossRef
44.
go back to reference Sutbeyaz S, Yavuzer G, Sezer N, Koseoglu BF. Mirror therapy enhances lower-extremity motor recovery and motor functioning after stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2007;88(5):555–9.PubMedCrossRef Sutbeyaz S, Yavuzer G, Sezer N, Koseoglu BF. Mirror therapy enhances lower-extremity motor recovery and motor functioning after stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2007;88(5):555–9.PubMedCrossRef
45.
go back to reference Ramachandran VS, Rogers-Ramachandran D, Cobb S. Touching the phantom limb. Nature. 1995;377(6549):489–90.PubMedCrossRef Ramachandran VS, Rogers-Ramachandran D, Cobb S. Touching the phantom limb. Nature. 1995;377(6549):489–90.PubMedCrossRef
46.
go back to reference Cramer SC, Finklestein SP, Schaechter JD, Bush G, Rosen BR. Activation of distinct motor cortex regions during ipsilateral and contralateral finger movements. J Neurophysiol. 1999;81(1):383–7.PubMed Cramer SC, Finklestein SP, Schaechter JD, Bush G, Rosen BR. Activation of distinct motor cortex regions during ipsilateral and contralateral finger movements. J Neurophysiol. 1999;81(1):383–7.PubMed
47.
go back to reference Kristeva R, Keller E, Deecke L, Kornhuber HH. Cerebral potentials preceding unilateral and simultaneous bilateral finger movements. Electroencephalogr Clin Neurophysiol. 1979;47(2):229–38.PubMedCrossRef Kristeva R, Keller E, Deecke L, Kornhuber HH. Cerebral potentials preceding unilateral and simultaneous bilateral finger movements. Electroencephalogr Clin Neurophysiol. 1979;47(2):229–38.PubMedCrossRef
48.
go back to reference Newton J, Sunderland A, Butterworth SE, Peters AM, Peck KK, Gowland PA. A pilot study of event-related functional magnetic resonance imaging of monitored wrist movements in patients with partial recovery. Stroke. 2002;33(12):2881–7.PubMedCrossRef Newton J, Sunderland A, Butterworth SE, Peters AM, Peck KK, Gowland PA. A pilot study of event-related functional magnetic resonance imaging of monitored wrist movements in patients with partial recovery. Stroke. 2002;33(12):2881–7.PubMedCrossRef
49.
go back to reference Zijdewind I, Butler JE, Gandevia SC, Taylor JL. The origin of activity in the biceps brachii muscle during voluntary contractions of the contralateral elbow flexor muscles. Exp Brain Res. 2006;175(3):526–35.PubMedCrossRef Zijdewind I, Butler JE, Gandevia SC, Taylor JL. The origin of activity in the biceps brachii muscle during voluntary contractions of the contralateral elbow flexor muscles. Exp Brain Res. 2006;175(3):526–35.PubMedCrossRef
50.
go back to reference Lee M, Gandevia SC, Carroll TJ. Unilateral strength training increases voluntary activation of the opposite untrained limb. Clin Neurophysiol. 2009;120(4):802–8.PubMedCrossRef Lee M, Gandevia SC, Carroll TJ. Unilateral strength training increases voluntary activation of the opposite untrained limb. Clin Neurophysiol. 2009;120(4):802–8.PubMedCrossRef
51.
go back to reference Schulte T, Muller-Oehring EM. Contribution of callosal connections to the interhemispheric integration of visuomotor and cognitive processes. Neuropsychol Rev. 2010;20(2):174–90.PubMedCentralPubMedCrossRef Schulte T, Muller-Oehring EM. Contribution of callosal connections to the interhemispheric integration of visuomotor and cognitive processes. Neuropsychol Rev. 2010;20(2):174–90.PubMedCentralPubMedCrossRef
52.
go back to reference Tominaga W, Matsubayashi J, Furuya M, Matsuhashi M, Mima T, Fukuyama H, et al. Asymmetric activation of the primary motor cortex during observation of a mirror reflection of a hand. PLoS One. 2011;6(11):e28226.PubMedCentralPubMedCrossRef Tominaga W, Matsubayashi J, Furuya M, Matsuhashi M, Mima T, Fukuyama H, et al. Asymmetric activation of the primary motor cortex during observation of a mirror reflection of a hand. PLoS One. 2011;6(11):e28226.PubMedCentralPubMedCrossRef
53.
go back to reference Carson RG, Ruddy KL. Vision modulates corticospinal suppression in a functionally specific manner during movement of the opposite limb. J Neurosci. 2012;32(2):646–52.PubMedCrossRef Carson RG, Ruddy KL. Vision modulates corticospinal suppression in a functionally specific manner during movement of the opposite limb. J Neurosci. 2012;32(2):646–52.PubMedCrossRef
54.
go back to reference Arevalo AL, Baldo JV, Dronkers NF. What do brain lesions tell us about theories of embodied semantics and the human mirror neuron system? Cortex. 2012;48(2):242–54.PubMedCentralPubMedCrossRef Arevalo AL, Baldo JV, Dronkers NF. What do brain lesions tell us about theories of embodied semantics and the human mirror neuron system? Cortex. 2012;48(2):242–54.PubMedCentralPubMedCrossRef
55.
go back to reference Catmur C, Gillmeister H, Bird G, Liepelt R, Brass M, Heyes C. Through the looking glass: counter-mirror activation following incompatible sensorimotor learning. Eur J Neurosci. 2008;28(6):1208–15.PubMedCrossRef Catmur C, Gillmeister H, Bird G, Liepelt R, Brass M, Heyes C. Through the looking glass: counter-mirror activation following incompatible sensorimotor learning. Eur J Neurosci. 2008;28(6):1208–15.PubMedCrossRef
56.
go back to reference Yavuzer G, Selles R, Sezer N, Sutbeyaz S, Bussmann JB, Koseoglu F, et al. Mirror therapy improves hand function in subacute stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2008;89(3):393–8.PubMedCrossRef Yavuzer G, Selles R, Sezer N, Sutbeyaz S, Bussmann JB, Koseoglu F, et al. Mirror therapy improves hand function in subacute stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2008;89(3):393–8.PubMedCrossRef
57.
go back to reference Ramachandran VS, Rogers-Ramachandran D. Synaesthesia in phantom limbs induced with mirrors. Proc Biol Sci. 1996;263(1369):377–86.PubMedCrossRef Ramachandran VS, Rogers-Ramachandran D. Synaesthesia in phantom limbs induced with mirrors. Proc Biol Sci. 1996;263(1369):377–86.PubMedCrossRef
58.
go back to reference Garry MI, Loftus A, Summers JJ. Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability. Exp Brain Res. 2005;163(1):118–22.PubMedCrossRef Garry MI, Loftus A, Summers JJ. Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability. Exp Brain Res. 2005;163(1):118–22.PubMedCrossRef
59.
go back to reference Rosen B, Lundborg G. Training with a mirror in rehabilitation of the hand. Scand J Plast Reconstr Surg Hand Surg. 2005;39(2):104–8.PubMedCrossRef Rosen B, Lundborg G. Training with a mirror in rehabilitation of the hand. Scand J Plast Reconstr Surg Hand Surg. 2005;39(2):104–8.PubMedCrossRef
60.
go back to reference Verhagen AP, de Vet HC, de Bie RA, Kessels AG, Boers M, Bouter LM, et al. The Delphi list: a criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus. J Clin Epidemiol. 1998;51(12):1235–41.PubMedCrossRef Verhagen AP, de Vet HC, de Bie RA, Kessels AG, Boers M, Bouter LM, et al. The Delphi list: a criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus. J Clin Epidemiol. 1998;51(12):1235–41.PubMedCrossRef
61.
go back to reference Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17(1):1–12.PubMedCrossRef Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17(1):1–12.PubMedCrossRef
62.
go back to reference Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713–21.PubMed Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713–21.PubMed
63.
go back to reference Sehm B, Perez MA, Xu B, Hidler J, Cohen LG. Functional neuroanatomy of mirroring during a unimanual force generation task. Cereb Cortex. 2010;20(1):34–45.PubMedCrossRef Sehm B, Perez MA, Xu B, Hidler J, Cohen LG. Functional neuroanatomy of mirroring during a unimanual force generation task. Cereb Cortex. 2010;20(1):34–45.PubMedCrossRef
64.
go back to reference Foltys H, Meister IG, Weidemann J, Sparing R, Thron A, Willmes K, et al. Power grip disinhibits the ipsilateral sensorimotor cortex: a TMS and fMRI study. Neuroimage. 2003;19(2 Pt 1):332–40.PubMedCrossRef Foltys H, Meister IG, Weidemann J, Sparing R, Thron A, Willmes K, et al. Power grip disinhibits the ipsilateral sensorimotor cortex: a TMS and fMRI study. Neuroimage. 2003;19(2 Pt 1):332–40.PubMedCrossRef
65.
go back to reference Muellbacher W, Facchini S, Boroojerdi B, Hallett M. Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clin Neurophysiol. 2000;111(2):344–9.PubMedCrossRef Muellbacher W, Facchini S, Boroojerdi B, Hallett M. Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clin Neurophysiol. 2000;111(2):344–9.PubMedCrossRef
66.
go back to reference Hoy KE, Georgiou-Karistianis N, Laycock R, Fitzgerald PB. Using transcranial magnetic stimulation to investigate the cortical origins of motor overflow: a study in schizophrenia and healthy controls. Psychol Med. 2007;37(4):583–94.PubMedCrossRef Hoy KE, Georgiou-Karistianis N, Laycock R, Fitzgerald PB. Using transcranial magnetic stimulation to investigate the cortical origins of motor overflow: a study in schizophrenia and healthy controls. Psychol Med. 2007;37(4):583–94.PubMedCrossRef
67.
go back to reference Perez MA, Cohen LG. Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. J Neurosci. 2008;28(22):5631–40.PubMedCentralPubMedCrossRef Perez MA, Cohen LG. Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. J Neurosci. 2008;28(22):5631–40.PubMedCentralPubMedCrossRef
68.
go back to reference Chen R, Yung D, Li JY. Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J Neurophysiol. 2003;89(3):1256–64.PubMedCrossRef Chen R, Yung D, Li JY. Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J Neurophysiol. 2003;89(3):1256–64.PubMedCrossRef
69.
go back to reference Hortobágyi T, Taylor JL, Petersen NT, Russell G, Gandevia SC. Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. J Neurophysiol. 2003;90(4):2451–9.PubMedCrossRef Hortobágyi T, Taylor JL, Petersen NT, Russell G, Gandevia SC. Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. J Neurophysiol. 2003;90(4):2451–9.PubMedCrossRef
70.
go back to reference Dragert K, Zehr EP. Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors. Exp Brain Res. 2011;208(2):217–27.PubMedCrossRef Dragert K, Zehr EP. Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors. Exp Brain Res. 2011;208(2):217–27.PubMedCrossRef
71.
go back to reference Bologna M, Caronni A, Berardelli A, Rothwell JC. Practice-related reduction of electromyographic mirroring activity depends on basal levels of interhemispheric inhibition. Eur J Neurosci. 2012;36(12):3749–57.PubMedCrossRef Bologna M, Caronni A, Berardelli A, Rothwell JC. Practice-related reduction of electromyographic mirroring activity depends on basal levels of interhemispheric inhibition. Eur J Neurosci. 2012;36(12):3749–57.PubMedCrossRef
72.
go back to reference Lee M, Hinder MR, Gandevia SC, Carroll TJ. The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol. 2010;588(Pt 1):201–12.PubMedCrossRef Lee M, Hinder MR, Gandevia SC, Carroll TJ. The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol. 2010;588(Pt 1):201–12.PubMedCrossRef
73.
go back to reference Duchateau J, Hortobágyi T, Enoka RM. Acute and long-term neural adaptations to training. In: Gollhofer A, Taube W, Nielsen JB, editors. Motor control and learning. London: Routledge; 2012. p. 319–50. Duchateau J, Hortobágyi T, Enoka RM. Acute and long-term neural adaptations to training. In: Gollhofer A, Taube W, Nielsen JB, editors. Motor control and learning. London: Routledge; 2012. p. 319–50.
74.
go back to reference Hubers A, Orekhov Y, Ziemann U. Interhemispheric motor inhibition: its role in controlling electromyographic mirror activity. Eur J Neurosci. 2008;28(2):364–71.PubMedCrossRef Hubers A, Orekhov Y, Ziemann U. Interhemispheric motor inhibition: its role in controlling electromyographic mirror activity. Eur J Neurosci. 2008;28(2):364–71.PubMedCrossRef
75.
go back to reference Hortobágyi T, Lambert NJ, Hill JP. Greater cross education following training with muscle lengthening than shortening. Med Sci Sports Exerc. 1997;29(1):107–12.PubMedCrossRef Hortobágyi T, Lambert NJ, Hill JP. Greater cross education following training with muscle lengthening than shortening. Med Sci Sports Exerc. 1997;29(1):107–12.PubMedCrossRef
76.
go back to reference Cincotta M, Borgheresi A, Balestrieri F, Giovannelli F, Rossi S, Ragazzoni A, et al. Involvement of the human dorsal premotor cortex in unimanual motor control: an interference approach using transcranial magnetic stimulation. Neurosci Lett. 2004;367(2):189–93.PubMedCrossRef Cincotta M, Borgheresi A, Balestrieri F, Giovannelli F, Rossi S, Ragazzoni A, et al. Involvement of the human dorsal premotor cortex in unimanual motor control: an interference approach using transcranial magnetic stimulation. Neurosci Lett. 2004;367(2):189–93.PubMedCrossRef
77.
go back to reference Giovannelli F, Borgheresi A, Balestrieri F, Ragazzoni A, Zaccara G, Cincotta M, et al. Role of the right dorsal premotor cortex in “physiological” mirror EMG activity. Exp Brain Res. 2006;175(4):633–40.PubMedCrossRef Giovannelli F, Borgheresi A, Balestrieri F, Ragazzoni A, Zaccara G, Cincotta M, et al. Role of the right dorsal premotor cortex in “physiological” mirror EMG activity. Exp Brain Res. 2006;175(4):633–40.PubMedCrossRef
78.
go back to reference Kidgell DJ, Stokes MA, Pearce AJ. Strength training of one limb increases corticomotor excitability projecting to the contralateral homologous limb. Motor Control. 2011;15(2):247–66.PubMed Kidgell DJ, Stokes MA, Pearce AJ. Strength training of one limb increases corticomotor excitability projecting to the contralateral homologous limb. Motor Control. 2011;15(2):247–66.PubMed
79.
go back to reference Pearce AJ, Hendy A, Bowen WA, Kidgell DJ. Corticospinal adaptations and strength maintenance in the immobilized arm following 3 weeks unilateral strength training. Scand J Med Sci Sports. doi: 10.1111/j.1600-0838.2012.01453.x. [Epub ahead of print]. Pearce AJ, Hendy A, Bowen WA, Kidgell DJ. Corticospinal adaptations and strength maintenance in the immobilized arm following 3 weeks unilateral strength training. Scand J Med Sci Sports. doi: 10.​1111/​j.​1600-0838.​2012.​01453.​x. [Epub ahead of print].
80.
go back to reference Fukumura K, Sugawara K, Tanabe S, Ushiba J, Tomita Y. Influence of mirror therapy on human motor cortex. Int J Neurosci. 2007;117(7):1039–48.PubMedCrossRef Fukumura K, Sugawara K, Tanabe S, Ushiba J, Tomita Y. Influence of mirror therapy on human motor cortex. Int J Neurosci. 2007;117(7):1039–48.PubMedCrossRef
81.
go back to reference Hamzei F, Läppchen CH, Glauche V, Mader I, Rijntjes M, Weiller C. Functional plasticity induced by mirror training: the mirror as the element connecting both hands to one hemisphere. Neurorehabil Neural Repair. 2012;26(5):484–96.PubMedCrossRef Hamzei F, Läppchen CH, Glauche V, Mader I, Rijntjes M, Weiller C. Functional plasticity induced by mirror training: the mirror as the element connecting both hands to one hemisphere. Neurorehabil Neural Repair. 2012;26(5):484–96.PubMedCrossRef
82.
go back to reference Funase K, Tabira T, Higashi T, Liang N, Kasai T. Increased corticospinal excitability during direct observation of self-movement and indirect observation with a mirror box. Neurosci Lett. 2007;419(2):108–12.PubMedCrossRef Funase K, Tabira T, Higashi T, Liang N, Kasai T. Increased corticospinal excitability during direct observation of self-movement and indirect observation with a mirror box. Neurosci Lett. 2007;419(2):108–12.PubMedCrossRef
83.
go back to reference Shinoura N, Suzuki Y, Watanabe Y, Yamada R, Tabei Y, Saito K, et al. Mirror therapy activates outside of cerebellum and ipsilateral M1. NeuroRehabilitation. 2008;23(3):245–52.PubMed Shinoura N, Suzuki Y, Watanabe Y, Yamada R, Tabei Y, Saito K, et al. Mirror therapy activates outside of cerebellum and ipsilateral M1. NeuroRehabilitation. 2008;23(3):245–52.PubMed
84.
go back to reference Tominaga W, Matsubayashi J, Deguchi Y, Minami C, Kinai T, Nakamura M, et al. A mirror reflection of a hand modulates stimulus-induced 20-Hz activity. Neuroimage. 2009;46(2):500–4.PubMedCrossRef Tominaga W, Matsubayashi J, Deguchi Y, Minami C, Kinai T, Nakamura M, et al. A mirror reflection of a hand modulates stimulus-induced 20-Hz activity. Neuroimage. 2009;46(2):500–4.PubMedCrossRef
85.
go back to reference Farthing JP. Cross-education of strength depends on limb dominance: implications for theory and application. Exerc Sport Sci Rev. 2009;37(4):179–87.PubMed Farthing JP. Cross-education of strength depends on limb dominance: implications for theory and application. Exerc Sport Sci Rev. 2009;37(4):179–87.PubMed
86.
go back to reference Catmur C, Walsh V, Heyes C. Associative sequence learning: the role of experience in the development of imitation and the mirror system. Philos Trans R Soc Lond B Biol Sci. 2009;364(1528):2369–80.PubMedCrossRef Catmur C, Walsh V, Heyes C. Associative sequence learning: the role of experience in the development of imitation and the mirror system. Philos Trans R Soc Lond B Biol Sci. 2009;364(1528):2369–80.PubMedCrossRef
87.
go back to reference Shin HW, Sohn YH. Interhemispheric transfer of paired associative stimulation-induced plasticity in the human motor cortex. Neuroreport. 2011;22(4):166–70.PubMedCrossRef Shin HW, Sohn YH. Interhemispheric transfer of paired associative stimulation-induced plasticity in the human motor cortex. Neuroreport. 2011;22(4):166–70.PubMedCrossRef
88.
go back to reference Stromberg BV. Contralateral therapy in upper extremity rehabilitation. Am J Phys Med. 1986;65(3):135–43.PubMed Stromberg BV. Contralateral therapy in upper extremity rehabilitation. Am J Phys Med. 1986;65(3):135–43.PubMed
89.
go back to reference Stromberg BV. Influence of cross-education training in postoperative hand therapy. South Med J. 1988;81(8):989–91.PubMedCrossRef Stromberg BV. Influence of cross-education training in postoperative hand therapy. South Med J. 1988;81(8):989–91.PubMedCrossRef
90.
go back to reference Farthing JP, Krentz JR, Magnus CR. Strength training the free limb attenuates strength loss during unilateral immobilization. J Appl Physiol. 2009;106(3):830–6.PubMedCrossRef Farthing JP, Krentz JR, Magnus CR. Strength training the free limb attenuates strength loss during unilateral immobilization. J Appl Physiol. 2009;106(3):830–6.PubMedCrossRef
91.
go back to reference Magnus CR, Arnold CM, Johnston G, Dal-Bello Haas V, Basran J, Krentz JR, et al. Cross-education for improving strength and mobility after distal radius fractures: a randomized controlled trial. Arch Phys Med Rehabil. 2013;94(7):1247-55. Magnus CR, Arnold CM, Johnston G, Dal-Bello Haas V, Basran J, Krentz JR, et al. Cross-education for improving strength and mobility after distal radius fractures: a randomized controlled trial. Arch Phys Med Rehabil. 2013;94(7):1247-55.
92.
go back to reference Ausenda C, Carnovali M. Transfer of motor skill learning from the healthy hand to the paretic hand in stroke patients: a randomized controlled trial. Eur J Phys Rehabil Med. 2011;47(3):417–25.PubMed Ausenda C, Carnovali M. Transfer of motor skill learning from the healthy hand to the paretic hand in stroke patients: a randomized controlled trial. Eur J Phys Rehabil Med. 2011;47(3):417–25.PubMed
93.
go back to reference Michielsen ME, Selles RW, van der Geest JN, Eckhardt M, Yavuzer G, Stam HJ, et al. Motor recovery and cortical reorganization after mirror therapy in chronic stroke patients: a phase II randomized controlled trial. Neurorehabil Neural Repair. 2011;25(3):223–33.PubMedCrossRef Michielsen ME, Selles RW, van der Geest JN, Eckhardt M, Yavuzer G, Stam HJ, et al. Motor recovery and cortical reorganization after mirror therapy in chronic stroke patients: a phase II randomized controlled trial. Neurorehabil Neural Repair. 2011;25(3):223–33.PubMedCrossRef
94.
go back to reference Dragert K, Zehr EP. High-intensity unilateral dorsiflexor resistance training results in bilateral neuromuscular plasticity after stroke. Exp Brain Res. 2013;225(1):93-104. Dragert K, Zehr EP. High-intensity unilateral dorsiflexor resistance training results in bilateral neuromuscular plasticity after stroke. Exp Brain Res. 2013;225(1):93-104.
95.
go back to reference Papandreou M, Billis E, Papathanasiou G, Spyropoulos P, Papaioannou N. Cross-exercise on quadriceps deficit after ACL reconstruction. J Knee Surg. 2013;26(1):51–8.PubMed Papandreou M, Billis E, Papathanasiou G, Spyropoulos P, Papaioannou N. Cross-exercise on quadriceps deficit after ACL reconstruction. J Knee Surg. 2013;26(1):51–8.PubMed
96.
go back to reference Papandreou MG, Billis EV, Antonogiannakis EM, Papaioannou NA. Effect of cross exercise on quadriceps acceleration reaction time and subjective scores (Lysholm questionnaire) following anterior cruciate ligament reconstruction. J Orthop Surg Res. 2009; 4:2. doi:10.1186/1749-799X-4-2. Papandreou MG, Billis EV, Antonogiannakis EM, Papaioannou NA. Effect of cross exercise on quadriceps acceleration reaction time and subjective scores (Lysholm questionnaire) following anterior cruciate ligament reconstruction. J Orthop Surg Res. 2009; 4:2. doi:10.​1186/​1749-799X-4-2.
Metadata
Title
Role of the Mirror-Neuron System in Cross-Education
Authors
Tjerk Zult
Glyn Howatson
Endre E. Kádár
Jonathan P. Farthing
Tibor Hortobágyi
Publication date
01-02-2014
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 2/2014
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-013-0105-2

Other articles of this Issue 2/2014

Sports Medicine 2/2014 Go to the issue