Induction of Cortical Plastic Changes in Wrist Muscles by Paired Associative Stimulation in the Recovery Phase of Stroke Patients

Abstract

Background. Paired associative stimulation (PAS) combining peripheral nerve and transcranial magnetic stimulation (TMS) have been proposed to induce long-term changes in excitability of the cerebral cortex and potentially optimize motor recovery in stroke patients. Objective. This pilot study examined whether short-lasting changes in cortical excitability could be induced by a single session of PAS within the first months after stroke. Methods. Six hemiparetic patients with a subcortical stroke were included. The single session PAS protocol was applied at 1, 5, and 12 months after stroke. During the follow-up, the clinical recovery of wrist function was assessed in parallel to the PAS study by the Fugl-Meyer motor scale and dynamometry of wrist extension. Results. The PAS protocol induced a significant extensor carpi radialis motor evoked potential facilitation (mean +78.5%) on the paretic side 5 months after stroke. The facilitation was still present 12 months after stroke but on average smaller (+30 %). Conclusions. These electrophysiological findings suggest that patients with subcortical infarcts may respond to PAS in an earlier than later period after stroke. If the clinical efficacy of interventions such as PAS is confirmed, it could be proposed early as add-on therapy to optimize training-induced plasticity processes.

Keywords

Paired associative stimulation Stroke Transcranial magnetic stimulation Cortical plasticity Recovery

References

Uy J. , Ridding MC , Hillier S. , Thompson PD , Miles TS Does induction of plastic change in motor cortex improve leg function after stroke? Neurology. 2003;61:982-984.

Butefisch CM , Kleiser R. , Seitz RJ Post-lesional cerebral reorganisation: evidence from functional neuroimaging and transcranial magnetic stimulation. J Physiol Paris. 2006;99:437-454.

Di Lazzaro V. , Dileone M. , Profice P. , et al. Direct demonstration that repetitive transcranial magnetic stimulation can enhance corticospinal excitability in stroke. Stroke. 2006;37:2850-2853.

Hummel F. , Celnik P. , Giraux P. , et al. Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain. 2005;128 (pt 3):490-499.

Khedr EM , Ahmed MA , Fathy N. , Rothwell JC Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology. 2005;65:466-468.

Kim YH , You SH , Ko MH , et al. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke. 2006;37:1471-1476.

Mansur CG , Fregni F. , Boggio PS , et al. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology. 2005;64:1802-1804.

Takeuchi N. , Chuma T. , Matsuo Y. , Watanabe I. , Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke. 2005;36:2681-2686.

Talelli P. , Rothwell J. Does brain stimulation after stroke have a future? Curr Opin Neurol. 2006;19:543-550.

10.

Castel-Lacanal E. , Gerdelat-Mas A. , Marque P. , Loubinoux I. , Simonetta-Moreau M. Induction of cortical plastic changes in wrist muscles by paired associative stimulation in healthy subjects and post-stroke patients. Exp Brain Res. 2007;180:113-122.

11.

Ridding MC , Taylor JL Mechanisms of motor-evoked potential facilitation following prolonged dual peripheral and central stimulation in humans. J Physiol. 2001;537(pt 2):623-631.

12.

Stefan K. , Kunesch E. , Cohen LG , Benecke R. , Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation . Brain. 2000;123(pt 3):572-584.

13.

Kamper DG , Harvey RL , Suresh S. , Rymer WZ Relative contributions of neural mechanisms versus muscle mechanics in promoting finger extension deficits following stroke. Muscle Nerve. 2003;28:309-318.

14.

Powell J. , Pandyan AD , Granat M. , Cameron M. , Stott DJ Electrical stimulation of wrist extensors in poststroke hemiplegia. Stroke. 1999;30: 1384-1389.

15.

Fugl-Meyer AR , Jaasko L. , Leyman I. , Olsson S. , Steglind S. The poststroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med. 1975;7:13-31.

16.

Stefan K. , Wycislo M. , Classen J. Modulation of associative human motor cortical plasticity by attention. J Neurophysiol. 2004;92:66-72.

17.

Rossini PM , Barker AT , Berardelli A. , et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 1994;91:79-92.

18.

Sale MV , Ridding MC , Nordstrom MA Factors influencing the magnitude and reproducibility of corticomotor excitability changes induced by paired associative stimulation. Exp Brain Res. 2007;181:615-626.

19.

Verheyden G. , Nieuwboer A. , De Wit L. , et al. Time course of trunk, arm, leg, and functional recovery after ischemic stroke. Neurorehabil Neural Repair. 2008;22:173-179.

20.

Prabhakaran S. , Zarahn E. , Riley C. , et al. Inter-individual variability in the capacity for motor recovery after ischemic stroke. Neurorehabil Neural Repair. 2008;22:64-71.

21.

Jorgensen HS , Nakayama H. , Raaschou HO , Vive-Larsen J. , Stoier M. , Olsen TS Outcome and time course of recovery in stroke. II. Time course of recovery. The Copenhagen Stroke Study. Arch Phys Med Rehabil. 1995;76:406-412.

22.

Feys H. , De Weerdt W. , Verbeke G. , et al. Early and repetitive stimulation of the arm can substantially improve the long-term outcome after stroke: a 5-year follow-up study of a randomized trial. Stroke. 2004;35: 924-929.

23.

Wolters A. , Sandbrink F. , Schlottmann A. , et al. A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol. 2003 ;89:2339-2345.

24.

Stefan K. , Kunesch E. , Benecke R. , Cohen LG , Classen J. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol. 2002;543(pt 2):699-708.

25.

Pyndt HS , Ridding MC Modification of the human motor cortex by associative stimulation. Exp Brain Res. 2004;159:123-128.

26.

Butefisch C. , Weβling M. , Netz J. , Seitz R. , Homberg V. Relationship between interhemispheric inhibition and motor cortex excitability in sub-acute stroke patients. Neurorehabil Neural Repair. 2008;22:4-21.

27.

Liepert J. , Restemeyer C. , Kucinski T. , Zittel S. , Weiller C. Motor strokes: the lesion location determines motor excitability changes. Stroke. 2005;36: 2648-2653.

28.

Meunier S. , Russmann H. , Simonetta-Moreau M. , Hallett M. Changes in spinal excitability after PAS. J Neurophysiol. 2007;97:3131-3135.

29.

Bienenstock EL , Cooper LN , Munro PW Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 1982;2:32-48.

30.

Tombari D. , Loubinoux I. , Pariente J. , et al. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. Neuroimage. 2004;23:827-39.

31.

Chollet F. , DiPiero V. , Wise RJ , Brooks DJ , Dolan RJ , Frackowiak RS The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol. 1991;29:63-71.

32.

Ward NS , Brown MM , Thompson AJ , Frackowiak RS Neural correlates of motor recovery after stroke: a longitudinal fMRI study . Brain. 2003;126(pt 11):2476-2496.

33.

Kwakkel G. , van Peppen R. , Wagenaar RC , et al. Effects of augmented exercise therapy time after stroke: a meta-analysis . Stroke. 2004;35:2529-2539.

34.

Dobkin BH Confounders in rehabilitation trials of task-oriented training: Lessons from the designs of the EXCITE and SCILT multicenter trials. Neurorehabil Neural Repair. 2007;21:3-13.