Combined transcranial direct current stimulation and robotic upper limb therapy improves upper limb function in an adult with cerebral palsy

Kathleen M Friel, Peter Lee, Lindsey V Soles, Ana R P Smorenburg, Hsing-Ching Kuo, Disha Gupta, Dylan J Edwards, Kathleen M Friel, Peter Lee, Lindsey V Soles, Ana R P Smorenburg, Hsing-Ching Kuo, Disha Gupta, Dylan J Edwards

Abstract

Background: Robotic therapy can improve upper limb function in hemiparesis. Excitatory transcranial direct current stimulation (tDCS) can prime brain motor circuits before therapy.

Objective: We tested safety and efficacy of tDCS plus robotic therapy in an adult with unilateral spastic cerebral palsy (USCP).

Methods: In each of 36 sessions, anodal tDCS (2 mA, 20 min) was applied over the motor map of the affected hand. Immediately after tDCS, the participant completed robotic therapy, using the shoulder, elbow, and wrist (MIT Manus). The participant sat in a padded chair with affected arm abducted, forearm supported, and hand grasping the robot handle. The participant controlled the robot arm with his affected arm to move a cursor from the center of a circle to each of eight targets (960 movements). Motor function was tested before, after, and six months after therapy with the Wolf Motor Function Test (WMFT) and Fugl-Meyer (FM).

Results: Reaching accuracy on the robot task improved significantly after therapy. The WMFT and FM improved clinically meaningful amounts after therapy. The motor map of the affected hand expanded after therapy. Improvements were maintained six months after therapy.

Conclusions: Combined tDCS and robotics safely improved upper limb function in an adult with USCP.

Keywords: Neuromodulation; neuroplasticity; rehabilitation.

Figures

Fig.1
Fig.1
Representative traces of movement trials on the planar robot star reach task (top panel), wrist robot star reach task (middle panel), and planar robot circle drawing task (botton panel).
Fig.2
Fig.2
Over the intervention, movement smoothness did not significantly change on the planar (A) or wrist (B) robots. Reach error on both the planar (C) and wrist (D) robots improved significantly from pre-intervention to the midpoint (week 6; *p < 0.001). There was no further improvement in reach error after the intervention or at the six-month follow-up.
Fig.3
Fig.3
Directional differences in planar reach error over the intervention. Each bar graph summarized reach error in the direction at which the graph is located relative to the center. The largest reach errors were found in the directions that required the participant to extend his upper limb. Error rates significantly decreased during the first half of the intervention (*p < 0.01 compared to mid, post, and follow-up), and did not further improve during the second half of the intervention.
Fig.4
Fig.4
Directional differences in wrist reach error over the intervention. Each bar graph summarized reach error in the direction at which the graph is located relative to the center. Reaching error in equal amounts were found in the first half of the intervention (*p < 0.01 compared to mid, post, and follow-up), and did not further improve during the second half of the intervention.
Fig.5
Fig.5
Circularity of ellipses drawn on the planar robot. Twenty trials were performed every two weeks. The goal was to draw a perfect circle, whose ratio of major and minor axes would equal 1 (dotted line). During the half of the intervention, circularity improved compared to baseline (*p < 0.001). No further significant improvements occurred during the second half of the intervention.
Fig.6
Fig.6
Motor map of the participant’s impaired FDI muscle. The heat map represents the amplitude of the MEP across locations of the map (blue = low amplitude, red = high amplitude). The FDI motor map increased in size and excitability after therapy.

References

    1. Aarts P. B., Jongerius P. H., Geerdink Y. A., van Limbeek J., & Geurts A. C. (2010). Effectiveness of modified constraint-induced movement therapy in children with unilateral spastic cerebral palsy: A randomized controlled trial. Neurorehabil Neural Repair, 24(6), 509–518. doi:
    1. Bosecker C., Dipietro L., Volpe B., & Krebs H. I. (2010). Kinematic robot-based evaluation scales and clinical counterparts to measure upper limb motor performance in patients with chronic stroke. Neurorehabil Neural Repair, 24(1), 62–69. doi:
    1. Censor N. (2013). Generalization of perceptual and motor learning: A causal link with memory encoding and consolidation? Neuroscience, 250, 201–207. doi:
    1. Dong V. A., Tung I. H., Siu H. W., & Fong K. N. (2013). Studies comparing the efficacy of constraint-induced movement therapy and bimanual training in children with unilateral cerebral palsy: A systematic review. Dev Neurorehabil, 16(2), 133–143. doi:
    1. Edwards D. F., Lang C. E., Wagner J. M., Birkenmeier R., & Dromerick A. W. (2012). An evaluation of the Wolf Motor Function Test in motor trials early after stroke. Arch Phys Med Rehabil, 93(4), 660–668. doi:
    1. Eyre J. A., Smith M., Dabydeen L., Clowry G. J., Petacchi E., Battini R., ... & Cioni G. (2007). Is hemiplegic cerebral palsy equivalent to amblyopia of the corticospinal system? Ann Neurol, 62(5), 493–503. doi:
    1. Friel K. M., Kuo H. C., Fuller J., Ferre C. L., Brandao M., Carmel J. B., ... & Gordon A. M. (2016). Skilled Bimanual Training Drives Motor Cortex Plasticity in Children With Unilateral Cerebral Palsy. Neurorehabil Neural Repair, 30(9), 834–844. doi:
    1. Giacobbe V., Krebs H. I., Volpe B. T., Pascual-Leone A., Rykman A., Zeiarati G., ... & Edwards D. J. (2013). Transcranial direct current stimulation (tDCS) and robotic practice in chronic stroke: The dimension of timing. NeuroRehabilitation 33(1), 49–56. doi:
    1. Gladstone D. J., Danells C. J., & Black S. E. (2002). The fugl-meyer assessment of motor recovery after stroke: A critical review of its measurement properties. Neurorehabil Neural Repair, 16(3), 232–240.
    1. Jones T. A., Chu C. J., Grande L. A., & Gregory A. D. (1999). Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J Neurosci, 19(22), 10153–10163.
    1. Kitago T., & Krakauer J. W. (2013). Motor learning principles for neurorehabilitation. Handb Clin Neurol, 110, 93–103. doi:
    1. Kleim J. A., Kleim E. D., & Cramer S. C. (2007). Systematic assessment of training-induced changes in corticospinal output to hand using frameless stereotaxic transcranial magnetic stimulation. Nat Protoc, 2(7), 1675–1684. doi:
    1. Krebs H. I., Hogan N., Volpe B. T., Aisen M. L., Edelstein L., & Diels C. (1999). Overview of clinical trials with MIT-MANUS: A robot-aided neuro-rehabilitation facility. Technol Health Care, 7(6), 419–423.
    1. Liepert J., Graef S., Uhde I., Leidner O., & Weiller C. (2000). Training-induced changes of motor cortex representations in stroke patients. Acta Neurol Scand, 101(5), 321–326.
    1. Liew S. L., Santarnecchi E., Buch E. R., & Cohen L. G. (2014). Non-invasive brain stimulation in neurorehabilitation: Local and distant effects for motor recovery. Front Hum Neurosci, 8, 378 doi:
    1. Lin K. C., Hsieh Y. W., Wu C. Y., Chen C. L., Jang Y., & Liu J. S. (2009). Minimal detectable change and clinically important difference of the Wolf Motor Function Test in stroke patients. Neurorehabil Neural Repair, 23(5), 429–434. doi:
    1. Malouin F., Pichard L., Bonneau C., Durand A., & Corriveau D. (1994). Evaluating motor recovery early after stroke: Comparison of the Fugl-Meyer Assessment and the Motor Assessment Scale. Arch Phys Med Rehabil, 75(11), 1206–1212.
    1. Morris D. M., Uswatte G., Crago J. E., Cook E. W. 3rd, & Taub E. (2001). The reliability of the wolf motor function test for assessing upper extremity function after stroke. Arch Phys Med Rehabil, 82(6), 750–755. doi:
    1. Norouzi-Gheidari N., Archambault P. S., & Fung J. (2012). Effects of robot-assisted therapy on stroke rehabilitation in upper limbs: Systematic review and meta-analysis of the literature. J Rehabil Res Dev, 49(4), 479–496.
    1. Nudo R. J. (2003). Functional and structural plasticity in motor cortex: Implications for stroke recovery. Phys Med Rehabil Clin N Am, 14(Suppl. 1), S57–76.
    1. Page S. J., Fulk G. D., & Boyne P. (2012). Clinically important differences for the upper-extremity Fugl-Meyer Scale in people with minimal to moderate impairment due to chronic stroke. Phys Ther, 92(6), 791–798. doi:
    1. Paulus W. (2004). Outlasting excitability shifts induced by direct current stimulation of the human brain. Suppl Clin Neurophysiol, 57, 708–714.
    1. Raithatha R., Carrico C., Powell E. S., Westgate P. M., Chelette Ii , K. C., Lee K., ... & Sawaki L. (2016). Non-invasive brain stimulation and robot-assisted gait training after incomplete spinal cord injury: A randomized pilot study. NeuroRehabilitation, 38(1), 15–25. doi:
    1. Sawaki L., Butler A. J., Leng X., Wassenaar P. A., Mohammad Y. M., Blanton S., ... & Wittenberg G. F. (2008). Constraint-induced movement therapy results in increased motor map area in subjects 3 to 9 months after stroke. Neurorehabil Neural Repair, 22(5), 505–513. doi: 22/5/505 [pii]
    1. Smorenburg A. R., Gordon A. M., Kuo H. C., Ferre C. L., Brandao M., Bleyenheuft Y., ... & Friel K. M. (2017). Does corticospinal tract connectivity influence the response to intensive bimanual therapy in children with unilateral cerebral palsy? Neurorehabil Neural Repair, 31(3), 250–260. doi:
    1. Staudt M. (2007). (Re-)organization of the developing human brain following periventricular white matter lesions. Neurosci Biobehav Rev, 31(8), 1150–1156. doi: S0149-7634(07)00063-2 [pii]
    1. Staudt M., Gerloff C., Grodd W., Holthausen H., Niemann G., & Krageloh-Mann I. (2004). Reorganization in congenital hemiparesis acquired at different gestational ages. Ann Neurol, 56(6), 854–863. doi:
    1. Straudi S., Fregni F., Martinuzzi C., Pavarelli C., Salvioli S., & Basaglia N. (2016). tDCS and Robotics on Upper Limb Stroke Rehabilitation: Effect Modification by Stroke Duration and Type of Stroke. Biomed Res Int, 2016, 5068127 doi:
    1. Takechi U., Matsunaga K., Nakanishi R., Yamanaga H., Murayama N., Mafune K., & Tsuji S. (2014). Longitudinal changes of motor cortical excitability and transcallosal inhibition after subcortical stroke. Clin Neurophysiol, 125(10), 2055–2069. doi:
    1. Takeuchi N., & Izumi S. (2012). Maladaptive plasticity for motor recovery after stroke: Mechanisms and approaches. Neural Plast, 2012, 359728 doi:
    1. Turner D. L., Ramos-Murguialday A., Birbaumer N., Hoffmann U., & Luft A. (2013). Neurophysiology of robot-mediated training and therapy: A perspective for future use in clinical populations. Front Neurol, 4, 184 doi:
    1. Volpe B. T., Huerta P. T., Zipse J. L., Rykman A., Edwards D., Dipietro L., ... & Krebs H. I. (2009). Robotic devices as therapeutic and diagnostic tools for stroke recovery. Arch Neurol, 66(9), 1086–1090. doi:
    1. Yozbatiran N., Keser Z., Davis M., Stampas A., O’Malley M. K., Cooper-Hay C., ... & Francisco G. E. (2016). Transcranial direct current stimulation (tDCS) of the primary motor cortex and robot-assisted arm training in chronic incomplete cervical spinal cord injury: A proof of concept sham-randomized clinical study. NeuroRehabilitation, 39(3), 401–411. doi:
    1. Zimerman M., Heise K. F., Hoppe J., Cohen L. G., Gerloff C., & Hummel F. C. (2012). Modulation of training by single-session transcranial direct current stimulation to the intact motor cortex enhances motor skill acquisition of the paretic hand. Stroke, 43(8), 2185–2191. doi:

Source: PubMed

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