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Published in: Experimental Brain Research 1/2011

01-03-2011 | Research Article

Non-invasive brain stimulation enhances fine motor control of the hemiparetic ankle: implications for rehabilitation

Authors: Sangeetha Madhavan, Kenneth A. Weber II, James W. Stinear

Published in: Experimental Brain Research | Issue 1/2011

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Abstract

We set out to answer two questions with this study: 1. Can stroke patients improve voluntary control of their paretic ankle by practising a visuo-motor ankle-tracking task? 2. Are practice effects enhanced with non-invasive brain stimulation? A carefully selected sample of chronic stroke patients able to perform the experimental task attended three data collection sessions. Facilitatory transcranial direct current stimulation (tDCS) was applied in a random order over the lower limb primary motor cortex of the lesioned hemisphere or the non-lesioned hemisphere or sham stimulation was delivered over the lesioned hemisphere. In each session, tDCS was applied as patients practiced tracking a sinusoidal waveform for 15 min using dorsiflexion–plantarflexion movements of their paretic ankle. The difference in tracking error prior to, and after, the 15 min of practice was calculated. A practice effect was revealed following sham stimulation, and this effect was enhanced with tDCS applied over the lesioned hemisphere. The practice effect observed following sham stimulation was eliminated by tDCS applied over the non-lesioned hemisphere. The study provides the first evidence that non-invasive brain stimulation applied to the lesioned motor cortex of moderate- to well-recovered stroke patients enhances voluntary control of the paretic ankle. The results provide a basis for examining whether this enhanced ankle control can be induced in patients with greater impairments and whether enhanced control of a single or multiple lower limb joints improves hemiparetic gait patterns.
Literature
go back to reference Bienenstock E, Cooper L, Munro P (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32–48PubMed Bienenstock E, Cooper L, Munro P (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32–48PubMed
go back to reference Bolognini N, Pascual-Leone A, Fregni F (2009) Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuro Eng Rehab 17:6–8 Bolognini N, Pascual-Leone A, Fregni F (2009) Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuro Eng Rehab 17:6–8
go back to reference Carey JR, Anderson KM, Kimberley TJ, Lewis SM, Auerbach EJ, Ugurbil K (2004) fMRI analysis of ankle movement tracking training in subject with stroke. Exp Brain Res 154:281–290CrossRefPubMed Carey JR, Anderson KM, Kimberley TJ, Lewis SM, Auerbach EJ, Ugurbil K (2004) fMRI analysis of ankle movement tracking training in subject with stroke. Exp Brain Res 154:281–290CrossRefPubMed
go back to reference Fregni F, Boggio PS, Mansur CG, Wagner T, Ferreira MJ, Lima MC et al (2005) Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport 16:1551–1555CrossRefPubMed Fregni F, Boggio PS, Mansur CG, Wagner T, Ferreira MJ, Lima MC et al (2005) Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport 16:1551–1555CrossRefPubMed
go back to reference Hummel F, Celnik P, Giraux P, Floel A, Wu WH, Gerloff C et al (2005) Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128:490–499CrossRefPubMed Hummel F, Celnik P, Giraux P, Floel A, Wu WH, Gerloff C et al (2005) Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128:490–499CrossRefPubMed
go back to reference Iyer M, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann E (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64:872–875PubMed Iyer M, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann E (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64:872–875PubMed
go back to reference Jayaram G, Stinear JW (2009) The effects of transcranial stimulation on paretic lower limb motor excitability during walking. J Clin Neurophysiol 26:272–279CrossRefPubMed Jayaram G, Stinear JW (2009) The effects of transcranial stimulation on paretic lower limb motor excitability during walking. J Clin Neurophysiol 26:272–279CrossRefPubMed
go back to reference Jeffery DT, Norton JA, Roy FD, Gorassini MA (2007) Effects of transcranial direct current stimulation on the excitability of the leg motor cortex. Exp Brain Res 182:281–287CrossRefPubMed Jeffery DT, Norton JA, Roy FD, Gorassini MA (2007) Effects of transcranial direct current stimulation on the excitability of the leg motor cortex. Exp Brain Res 182:281–287CrossRefPubMed
go back to reference Jensen JL, Marstrand PC, Nielsen JB (2005) Motor skill training and strength training are associated with different plastic changes in the central nervous system. J App Phys 99:1558–1568CrossRef Jensen JL, Marstrand PC, Nielsen JB (2005) Motor skill training and strength training are associated with different plastic changes in the central nervous system. J App Phys 99:1558–1568CrossRef
go back to reference Jørgensen HS, Nakayama H, Raaschou HO, Olsen TS (1995) Recovery of walking function in stroke patients: the Copenhagen stroke study. Arch Phys Med Rehab 76:27–32CrossRef Jørgensen HS, Nakayama H, Raaschou HO, Olsen TS (1995) Recovery of walking function in stroke patients: the Copenhagen stroke study. Arch Phys Med Rehab 76:27–32CrossRef
go back to reference Kantak SS, Sullivan KJ, Fisher BE, Knowlton BJ, Winstein CJ (2010) Neural substrates of motor memory consolidation depend on practice structure. Nat Neurosci 13:923–925CrossRefPubMed Kantak SS, Sullivan KJ, Fisher BE, Knowlton BJ, Winstein CJ (2010) Neural substrates of motor memory consolidation depend on practice structure. Nat Neurosci 13:923–925CrossRefPubMed
go back to reference Madhavan S, Stinear JW (2010) Focal and bidirectional modulation of lower limb motor cortex using anodal transcranial direct current stimulation. Brain Stim 3:42–50CrossRef Madhavan S, Stinear JW (2010) Focal and bidirectional modulation of lower limb motor cortex using anodal transcranial direct current stimulation. Brain Stim 3:42–50CrossRef
go back to reference Madhavan S, Rogers LM, Stinear JW (2010) A paradox: after stroke, the non-lesioned lower limb motor cortex may be maladaptive. Eur J Neurosci 32:1032–1039CrossRefPubMed Madhavan S, Rogers LM, Stinear JW (2010) A paradox: after stroke, the non-lesioned lower limb motor cortex may be maladaptive. Eur J Neurosci 32:1032–1039CrossRefPubMed
go back to reference Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409CrossRefPubMed Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409CrossRefPubMed
go back to reference Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899–1901PubMed Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899–1901PubMed
go back to reference Nitsche MA, Doemkes S, Karaköse T, Antal A, Liebetanz D, Lang N et al (2007) Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 97:3109–3117CrossRefPubMed Nitsche MA, Doemkes S, Karaköse T, Antal A, Liebetanz D, Lang N et al (2007) Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 97:3109–3117CrossRefPubMed
go back to reference Olney SJ, Richards CL (1996) Hemiplegic gait following stroke: Part I. Characteristics. Gait Posture 4:136–148CrossRef Olney SJ, Richards CL (1996) Hemiplegic gait following stroke: Part I. Characteristics. Gait Posture 4:136–148CrossRef
go back to reference Perez MA, Lungholt BK, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159:197–205CrossRefPubMed Perez MA, Lungholt BK, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159:197–205CrossRefPubMed
go back to reference Reis J, Robertson E, Krakauer JW, Rothwell J, Marshall L, Gerloff C (2008) Consensus: “Can tDCS and TMS enhance motor learning and memory formation?”. Brain Stimul 1:363–369CrossRef Reis J, Robertson E, Krakauer JW, Rothwell J, Marshall L, Gerloff C (2008) Consensus: “Can tDCS and TMS enhance motor learning and memory formation?”. Brain Stimul 1:363–369CrossRef
go back to reference Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E (2009) Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci USA 106:1590–1595CrossRefPubMed Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E (2009) Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci USA 106:1590–1595CrossRefPubMed
go back to reference Rovner BW, Folstein MF (1987) Mini-mental state exam in clinical practice. Hosp. Pract (Off Ed) 22:103, 106, 110 Rovner BW, Folstein MF (1987) Mini-mental state exam in clinical practice. Hosp. Pract (Off Ed) 22:103, 106, 110
go back to reference Stinear J, Hornby T (2005) Stimulation-induced changes in lower limb corticomotor excitability during treadmill walking in humans. J Physiol 567:701–711CrossRefPubMed Stinear J, Hornby T (2005) Stimulation-induced changes in lower limb corticomotor excitability during treadmill walking in humans. J Physiol 567:701–711CrossRefPubMed
go back to reference Tanaka S, Hanakawa T, Honda M, Watanabe K (2009) Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation. Exp Brain Res 96:459–465CrossRef Tanaka S, Hanakawa T, Honda M, Watanabe K (2009) Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation. Exp Brain Res 96:459–465CrossRef
go back to reference van Hedel HJ, Wirth B, Curt A (2010) Ankle motor skill is intact in spinal cord injury, unlike stroke: implications for rehabilitation. Neurology 74:1271–1278CrossRefPubMed van Hedel HJ, Wirth B, Curt A (2010) Ankle motor skill is intact in spinal cord injury, unlike stroke: implications for rehabilitation. Neurology 74:1271–1278CrossRefPubMed
go back to reference Wheaton LA, Villagra F, Hanley DF, Macko RF, Forrester LW (2009) Reliability of TMS motor evoked potentials in quadriceps of subjects with chronic hemiparesis after stroke. J Neurol Sci 276:115–117CrossRefPubMed Wheaton LA, Villagra F, Hanley DF, Macko RF, Forrester LW (2009) Reliability of TMS motor evoked potentials in quadriceps of subjects with chronic hemiparesis after stroke. J Neurol Sci 276:115–117CrossRefPubMed
Metadata
Title
Non-invasive brain stimulation enhances fine motor control of the hemiparetic ankle: implications for rehabilitation
Authors
Sangeetha Madhavan
Kenneth A. Weber II
James W. Stinear
Publication date
01-03-2011
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 1/2011
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-010-2511-0

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