Skip to main content
Log in

Effect of finger tracking combined with electrical stimulation on brain reorganization and hand function in subjects with stroke

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Synergism of rehabilitative interventions could maximize recovery following stroke. We examined whether the combination of peripherally initiated electrical stimulation of finger extensors and centrally operating finger tracking training could accentuate brain reorganization and its relationship to recovery, beyond the effects of either treatment alone. Twenty subjects with stroke were randomly assigned to an electrical stimulation (ES), tracking training (TR) or combination (CM) group. Each group was trained for ten 1-h sessions over 2–3 weeks. Pretest and posttest measurements consisted of the Box and Block and Jebsen Taylor tests of manual dexterity and a finger tracking test that was performed during functional magnetic resonance imaging (fMRI). fMRI variables included laterality index and BOLD signal intensity of primary motor (M1), primary sensory (S1), sensorimotor (SMC) and premotor (PMC) cortices as well as, supplementary motor area (SMA). ES and CM groups improved on dexterity, whereas the TR group did not. Improvement in the CM group was not greater than the other two groups. Subjects who had an intact M1 showed greater functional improvement than those who had direct involvement of M1. fMRI analysis did not yield significant changes from pretest to posttest. In the CM group only, functional improvement was positively correlated with laterality index change in M1, S1, SMC and PMC, indicating greater ipsilesional control and was negatively correlated with BOLD Signal Intensity change in ipsilesional S1 and SMA, indicating neurophysiological trimming of irrelevant neurons. The correlational results suggest that the combined intervention may be more influential on brain reorganization than either treatment alone but a larger sample size, longer duration of training, or a restricted inclusion of stroke location and volume may be needed to demonstrate a difference in efficacy for producing behavioral changes.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson DI, Magill RA, Sekiya H, Ryan G (2005) Support for an explanation of the guidance effect in motor skill learning. J Motor Behav 37:231–238

    Article  CAS  Google Scholar 

  • Bakhai A (2004) The burden of coronary, cerebrovascular and peripheral arterial disease. Pharmacoeconomics 22(Suppl 4):11–18

    Article  PubMed  Google Scholar 

  • Broeks JG, Lankhorst GJ, Rumping K, Prevo AJ (1999) The long-term outcome of arm function after stroke: results of a follow-up study. Disabil Rehabil 21:357–364

    Article  PubMed  CAS  Google Scholar 

  • Brown GG, Caligiuri M, Meloy MJ, Eberson SC, Kindermann SS, Frank LR, Eyler Zorrilla LT, Lohr JB (2004) Functional brain asymmetries during visuomotor tracking. J Clin Exp Neuropsychol 26:356–368

    Article  PubMed  Google Scholar 

  • Carey JR (1990) Manual stretch: effect on finger movement control and force control in stroke subjects with spastic extrinsic finger flexor muscles. Arch Phys Med Rehabil 71:888–894

    PubMed  CAS  Google Scholar 

  • Carey JR, Bogard CL, Youdas JW, Suman VJ (1995) Stimulus-response compatibility effects in a manual tracking task. Percept Mot Skills 81:1155–1170

    PubMed  CAS  Google Scholar 

  • Carey JR, Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey L, Rundquist P, Ugurbil K (2002) Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125:773–788

    Article  PubMed  Google Scholar 

  • 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 154:281–290

    Article  PubMed  Google Scholar 

  • Carey JR, Durfee WK, Bhatt E, Nagpal A, Weinstein SA, Anderson KM, Lewis SM (2007) Tracking vs. movement telerehabilitation training to change hand function and brain reorganization in stroke. Neurorehabil Neural Repair (in press)

  • Cauraugh J, Light K, Kim S, Thigpen M, Behrman A (2000) Chronic motor dysfunction after stroke: recovering wrist and finger extension by electromyography-triggered neuromuscular stimulation. Stroke 31:1360–1364

    PubMed  CAS  Google Scholar 

  • Chen CL, Tang FT, Chen HC, Chung CY, Wong MK (2000) Brain lesion size and location: effects on motor recovery and functional outcome in stroke patients. Arch Phys Med Rehabil 81:447–452

    Article  PubMed  CAS  Google Scholar 

  • Chen CC, Tyler CW, Baseler HA (2003) Statistical properties of BOLD magnetic resonance activity in the human brain. Neuroimage 20:1096–1109

    Article  PubMed  Google Scholar 

  • Chen SC, Chen YL, Chen CJ, Lai CH, Chiang WH, Chen WL (2005) Effects of surface electrical stimulation on the muscle–tendon junction of spastic gastrocnemius in stroke patients. Disabil Rehabil 27:105–110

    Article  PubMed  Google Scholar 

  • Cohen MS, DuBois RM (1999) Stability, repeatability, and the expression of signal magnitude in functional magnetic resonance imaging. J Magn Reson Imaging 10:33–40

    Article  PubMed  CAS  Google Scholar 

  • Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, Kennedy DN, Finklestein SP, Rosen BR (1997) A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28:2518–2527

    PubMed  CAS  Google Scholar 

  • Dassonville P, Lewis SM, Zhu XH, Ugurbil K, Kim SG, Ashe J (2001) The effect of stimulus–response compatibility on cortical motor activation. Neuroimage 13:1–14

    Article  PubMed  CAS  Google Scholar 

  • de Kroon JR, Ijzerman MJ, Chae J, Lankhorst GJ, Zilvold G (2005) Relation between stimulation characteristics and clinical outcome in studies using electrical stimulation to improve motor control of the upper extremity in stroke. J Rehabil Med 37:65–74

    Article  PubMed  Google Scholar 

  • Feydy A, Carlier R, Roby-Brami A, Bussel B, Cazalis F, Pierot L, Burnod Y, Maier MA (2002) Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke 33:1610–1617

    Article  PubMed  CAS  Google Scholar 

  • Frost SB, Barbay S, Friel KM, Plautz EJ, Nudo RJ (2003) Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J Neurophysiol 89(6):3205–3214

    Article  PubMed  CAS  Google Scholar 

  • Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878

    Article  PubMed  Google Scholar 

  • Hamdy S, Rothwell JC, Aziz Q, Singh KD, Thompson DG (1998) Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nature Neurosci 1:64–68

    Article  PubMed  CAS  Google Scholar 

  • Hamzei F, Dettmers C, Rijntjes M, Glauche V, Kiebel S, Weber B, Weiller C (2002) Visuomotor control within a distributed parieto-frontal network. Exp Brain Res 146:273–281

    Article  PubMed  Google Scholar 

  • Hamzei F, Liepert J, Dettmers C, Weiller C, Rijntjes M (2006) Two different reorganization patterns after rehabilitative therapy: an exploratory study with fMRI and TMS. Neuroimage 31:710–720

    Article  PubMed  Google Scholar 

  • Hess G, Aizenman CD, Donoghue JP (1996) Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J Neurophysiol 75:1765–1778

    PubMed  CAS  Google Scholar 

  • Hill H, Raab M (2005) Analyzing a complex visuomotor tracking task with brain-electrical event related potentials. Hum Mov Sci 24:1–30

    Article  PubMed  Google Scholar 

  • Holden MK (2005) Virtual environments for motor rehabilitation: review. Cyberpsychol Behav 8:187–211

    Article  PubMed  Google Scholar 

  • Hortobagyi T (2005) Cross education and the human central nervous system. IEEE Eng Med Biol Magaz 24:22–28

    Article  Google Scholar 

  • Hummelsheim H, Maier-Loth ML, Eickhof C (1997) The functional value of electrical muscle stimulation for the rehabilitation of the hand in stroke patients. Scand J Rehabil Med 29:3–10

    PubMed  CAS  Google Scholar 

  • Jancke L, Gaab N, Wustenberg T, Scheich H, Heinze HJ (2001) Short-term functional plasticity in the human auditory cortex: an fMRI study. Cogn Brain Res 12:479–485

    Article  CAS  Google Scholar 

  • Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA (1969) An objective and standardized test of hand function. Arch Phys Med Rehabil 50:311–319

    PubMed  CAS  Google Scholar 

  • Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633

    Article  PubMed  CAS  Google Scholar 

  • Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey LL, Lojovich JM, Carey JR (2004) Electrical stimulation driving functional improvements and cortical changes in subjects with stroke. Exp Brain Res 154:450–460

    Article  PubMed  Google Scholar 

  • Kleim JA, Barbay S, Nudo RJ (1998) Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80:3321–3325

    PubMed  CAS  Google Scholar 

  • Kobayashi H, Onishi H, Ihashi K, Yagi R, Handa Y (1999) Reduction in subluxation and improved muscle function of the hemiplegic shoulder joint after therapeutic electrical stimulation. J Electromyogr Kinesiol 9:327–336

    Article  PubMed  CAS  Google Scholar 

  • Krakauer JW (2006) Motor learning: its relevance to stroke recovery and neurorehabilitation. Curr Opin Neurol 19:84–90

    Article  PubMed  Google Scholar 

  • Kunkel A, Kopp B, Muller G, Villringer K, Villringer A, Taub E, Flor H (1999) Constraint-induced movement therapy for motor recovery in chronic stroke patients. Arch Phys Med Rehabil 80:624–628

    Article  PubMed  CAS  Google Scholar 

  • Lee TD, Magill RA (1983) The locus of contextual interference in motor skill acquisition. J Exp Psychol Learn Memory Cogn 9:730–746

    Article  Google Scholar 

  • Linn SL, Granat MH, Lees KR (1999) Prevention of shoulder subluxation after stroke with electrical stimulation. Stroke 30:963–968

    PubMed  CAS  Google Scholar 

  • Liu Y, Rouiller EM (1999) Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys. Exp Brain Res 128(1–2):149–159

    Article  PubMed  CAS  Google Scholar 

  • Luft AR, Kaelin-Lang A, Hauser TK, Buitrago MM, Thakor NV, Hanley DF, Cohen LG (2002) Modulation of rodent cortical motor excitability by somatosensory input. Exp Brain Res 142:562–569

    Article  PubMed  Google Scholar 

  • Luft AR, McCombe-Waller S, Whitall J, Forrester LW, Macko R, Sorkin JD, Schulz JB, Goldberg AP, Hanley DF (2004) Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial. J Am Med Assoc 292:1853–1861

    Article  CAS  Google Scholar 

  • Marshall RS, Perera GM, Lazar RM, Krakauer JW, Constantine RC, DeLaPaz RL (2000) Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke 31:656–661

    PubMed  CAS  Google Scholar 

  • Mathiowetz V, Volland G, Kashman N, Weber K (1985) Adult norms for the Box and Block Test of manual dexterity. Am J Occupat Therapy 39:386–391

    CAS  Google Scholar 

  • Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM (1996) Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16:785–807

    PubMed  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Page SJ, Gater DR, Bach YRP (2004) Reconsidering the motor recovery plateau in stroke rehabilitation. Arch Phys Med Rehabil 85:1377–1381

    Article  PubMed  Google Scholar 

  • Plautz EJ, Milliken GW, Nudo RJ (2000) Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Memory 74:27–55

    Article  CAS  Google Scholar 

  • Proctor R, Reeve T (1990) Stimulus-response compatibility. an integrated perspective. Elsevier, North-Holland, Amsterdam

    Google Scholar 

  • Ramsey NF, Jansma JM, Jager G, Van Raalten T, Kahn RS (2004) Neurophysiological factors in human information processing capacity. Brain 127:517–525

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ring H, Rosenthal N (2005) Controlled study of neuroprosthetic functional electrical stimulation in sub-acute post-stroke rehabilitation. J Rehabil Med 37:32–36

    Article  PubMed  Google Scholar 

  • Rioult-Pedotti MS, Friedman D, Hess G, Donoghue JP (1998) Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1:230–234

    Article  PubMed  CAS  Google Scholar 

  • Rosenkranz K, Rothwell JC (2006) Differences between the effects of three plasticity inducing protocols on the organization of the human motor cortex. Euro J Neurosci 23:822–829

    Article  Google Scholar 

  • Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Ann Rev Neurosci 23:393–415

    Article  PubMed  CAS  Google Scholar 

  • Sawaki L, Wu CW, Kaelin-Lang A, Cohen LG (2006) Effects of somatosensory stimulation on use-dependent plasticity in chronic stroke. Stroke 37:246–247

    Article  PubMed  Google Scholar 

  • Schmidt R (1988) Motor control and learning: a behavioral emphasis. Human Kinetics, Champaign

    Google Scholar 

  • Serrien DJ, Strens LH, Cassidy MJ, Thompson AJ, Brown P (2004) Functional significance of the ipsilateral hemisphere during movement of the affected hand after stroke. Exp Neurol 190:425–432

    Article  PubMed  Google Scholar 

  • Sherwood DE, Lee TD (2003) Schema theory: critical review and implications for the role of cognition in a new theory of motor learning. Res Quart Exer Sport 74:376–382

    Google Scholar 

  • Shumway-Cook A, Woollacott MH (2001) Motor control: theory and practical applications. Lippincot Williams and Wilkins, Baltimore

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ste-Marie DM, Clark SE, Findlay LC, Latimer AE (2004) High levels of contextual interference enhance handwriting skill acquisition. J Motor Behav 36:115–126

    Article  Google Scholar 

  • Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD (2007) Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 130:170–180

    Article  PubMed  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotoxic atlas of the human brain. Thieme, New York

    Google Scholar 

  • Thom T, Haase N, Rosamond W, Howard VJ, Rumsfeld J, Manolio T, Zheng ZJ, Flegal K, O’Donnell C, Kittner S, Lloyd-Jones D, Goff DC Jr, Hong Y, Adams R, Friday G, Furie K, Gorelick P, Kissela B, Marler J, Meigs J, Roger V, Sidney S, Sorlie P, Steinberger J, Wasserthiel-Smoller S, Wilson M, Wolf P, American Heart Association Statistics C, Stroke Statistics S (2006) Heart disease and stroke statistics-2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 113:e85–e151

    Article  PubMed  Google Scholar 

  • Toni I, Krams M, Turner R, Passingham RE (1998) The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 8:50–61

    Article  PubMed  CAS  Google Scholar 

  • Uy J, Ridding MC (2003) Increased cortical excitability induced by transcranial DC and peripheral nerve stimulation. J Neurosci Methods 127:193–197

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ward NS, Newton JM, Swayne OB, Lee L, Thompson AJ, Greenwood RJ, Rothwell JC, Frackowiak RS (2006) Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain 129:809–819

    Article  PubMed  Google Scholar 

  • Werhahn KJ, Conforto AB, Kadom N, Hallett M, Cohen LG (2003) Contribution of the ipsilateral motor cortex to recovery after chronic stroke. Ann Neurol 54:464–472

    Article  PubMed  Google Scholar 

  • Wilder RP, Wind TC, Jones EV, Crider BE, Edlich RF (2002) Functional electrical stimulation for a dropped foot. J Long-Term Effects Med Implants 12:149–159

    Google Scholar 

  • Woldag H, Hummelsheim H (2002) Evidence-based physiotherapeutic concepts for improving arm and hand function in stroke patients: a review. J Neurol 249:518–528

    Article  PubMed  Google Scholar 

  • Wu CW, van Gelderen P, Hanakawa T, Yaseen Z, Cohen LG (2005) Enduring representational plasticity after somatosensory stimulation. Neuroimage 27:872–884

    Article  PubMed  Google Scholar 

  • Wu CW, Seo HJ, Cohen LG (2006) Influence of electric somatosensory stimulation on paretic-hand function in chronic stroke. Arch Phys Med Rehabil 87:351–357

    Article  PubMed  Google Scholar 

  • Yozbatiran N, Donmez B, Kayak N, Bozan O (2006) Electrical stimulation of wrist and fingers for sensory and functional recovery in acute hemiplegia. Clin Rehabil 20:4–11

    Article  PubMed  Google Scholar 

  • Zhou W, Weldon P, Tang B, King WM (2003) Rapid motor learning in the translational vestibulo-ocular reflex. J Neurosci 23:4288–4298

    PubMed  CAS  Google Scholar 

  • Ziemann U, Ilic TV, Pauli C, Meintzschel F, Ruge D (2004) Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24:1666–1672

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge for the support of this work from grants from the National Institute on Disability and Rehabilitation Research (US Department of Education # H133G010077) and from National Center for Research Resources, National Institutes of Health (P41 RR008079 and M01-RR00400).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ela Bhatt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhatt, E., Nagpal, A., Greer, K.H. et al. Effect of finger tracking combined with electrical stimulation on brain reorganization and hand function in subjects with stroke. Exp Brain Res 182, 435–447 (2007). https://doi.org/10.1007/s00221-007-1001-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-007-1001-5

Keywords

Navigation