Skilled Bimanual Training Drives Motor Cortex Plasticity in Children With Unilateral Cerebral Palsy
Kathleen M Friel, Hsing-Ching Kuo, Jason Fuller, Claudio L Ferre, Marina Brandão, Jason B Carmel, Yannick Bleyenheuft, Jaimie L Gowatsky, Arielle D Stanford, Stefan B Rowny, Bruce Luber, Bruce Bassi, David L K Murphy, Sarah H Lisanby, Andrew M Gordon, Kathleen M Friel, Hsing-Ching Kuo, Jason Fuller, Claudio L Ferre, Marina Brandão, Jason B Carmel, Yannick Bleyenheuft, Jaimie L Gowatsky, Arielle D Stanford, Stefan B Rowny, Bruce Luber, Bruce Bassi, David L K Murphy, Sarah H Lisanby, Andrew M Gordon
Abstract
Background Intensive bimanual therapy can improve hand function in children with unilateral spastic cerebral palsy (USCP). We compared the effects of structured bimanual skill training versus unstructured bimanual practice on motor outcomes and motor map plasticity in children with USCP. Objective We hypothesized that structured skill training would produce greater motor map plasticity than unstructured practice. Methods Twenty children with USCP (average age 9.5; 12 males) received therapy in a day camp setting, 6 h/day, 5 days/week, for 3 weeks. In structured skill training (n = 10), children performed progressively more difficult movements and practiced functional goals. In unstructured practice (n = 10), children engaged in bimanual activities but did not practice skillful movements or functional goals. We used the Assisting Hand Assessment (AHA), Jebsen-Taylor Test of Hand Function (JTTHF), and Canadian Occupational Performance Measure (COPM) to measure hand function. We used single-pulse transcranial magnetic stimulation to map the representation of first dorsal interosseous and flexor carpi radialis muscles bilaterally. Results Both groups showed significant improvements in bimanual hand use (AHA; P < .05) and hand dexterity (JTTHF; P < .001). However, only the structured skill group showed increases in the size of the affected hand motor map and amplitudes of motor evoked potentials (P < .01). Most children who showed the most functional improvements (COPM) had the largest changes in map size. Conclusions These findings uncover a dichotomy of plasticity: the unstructured practice group improved hand function but did not show changes in motor maps. Skill training is important for driving motor cortex plasticity in children with USCP.
Keywords: hemiplegia; neuroplasticity; pediatric; rehabilitation; transcranial magnetic stimulation.
© The Author(s) 2016.
Figures
![Figure 1](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4981562/bin/nihms746149f1.jpg)
Figure 2
Coronal MRI slices showing a…
Figure 2
Coronal MRI slices showing a cross-section of each child’s lesion. The color of…
Figure 3
Changes in motor maps after…
Figure 3
Changes in motor maps after training. Colored dots represent movement evoked by TMS…
Figure 4
Changes in magnitude of motor…
Figure 4
Changes in magnitude of motor evoked potentials in TMS maps after structured skill…
- Commentary: Skilled Bimanual Training Drives Motor Cortex Plasticity in Children With Unilateral Cerebral Palsy.Serrien DJ. Serrien DJ. Front Hum Neurosci. 2017 Jun 7;11:297. doi: 10.3389/fnhum.2017.00297. eCollection 2017. Front Hum Neurosci. 2017. PMID: 28638332 Free PMC article. No abstract available.
- Comparison of Structured Skill and Unstructured Practice During Intensive Bimanual Training in Children With Unilateral Spastic Cerebral Palsy.Brandão MB, Ferre C, Kuo HC, Rameckers EA, Bleyenheuft Y, Hung YC, Friel K, Gordon AM. Brandão MB, et al. Neurorehabil Neural Repair. 2014 Jun;28(5):452-61. doi: 10.1177/1545968313516871. Epub 2013 Dec 27. Neurorehabil Neural Repair. 2014. PMID: 24376067
- Does Corticospinal Tract Connectivity Influence the Response to Intensive Bimanual Therapy in Children With Unilateral Cerebral Palsy?Smorenburg AR, Gordon AM, Kuo HC, Ferre CL, Brandao M, Bleyenheuft Y, Carmel JB, Friel KM. Smorenburg AR, et al. Neurorehabil Neural Repair. 2017 Mar;31(3):250-260. doi: 10.1177/1545968316675427. Epub 2016 Nov 17. Neurorehabil Neural Repair. 2017. PMID: 27856938 Free PMC article.
- Less-Affected Hand Function in Children With Hemiparetic Unilateral Cerebral Palsy: A Comparison Study With Typically Developing Peers.Rich TL, Menk JS, Rudser KD, Feyma T, Gillick BT. Rich TL, et al. Neurorehabil Neural Repair. 2017 Oct-Nov;31(10-11):965-976. doi: 10.1177/1545968317739997. Epub 2017 Nov 12. Neurorehabil Neural Repair. 2017. PMID: 29130382 Free PMC article.
- Hand-arm bimanual intensive therapy including lower extremities (HABIT-ILE) for children with cerebral palsy.Bleyenheuft Y, Gordon AM. Bleyenheuft Y, et al. Phys Occup Ther Pediatr. 2014 Nov;34(4):390-403. doi: 10.3109/01942638.2014.932884. Epub 2014 Oct 1. Phys Occup Ther Pediatr. 2014. PMID: 25271469 Review.
- To constrain or not to constrain, and other stories of intensive upper extremity training for children with unilateral cerebral palsy.Gordon AM. Gordon AM. Dev Med Child Neurol. 2011 Sep;53 Suppl 4:56-61. doi: 10.1111/j.1469-8749.2011.04066.x. Dev Med Child Neurol. 2011. PMID: 21950396 Review.
- Pediatric Patients With Hemiplegia: A Systematic Review of a Randomized Controlled Trial.Varma A, Khan NR, Varma A, Sharma NS, Vagha JD, Naqvi WM, Besekar S. Varma A, et al. Cureus. 2023 Jan 23;15(1):e34074. doi: 10.7759/cureus.34074. eCollection 2023 Jan. Cureus. 2023. PMID: 36843815 Free PMC article. Review.
- Functional Neuroplasticity and Motor Skill Change Following Gross Motor Interventions for Children With Diplegic Cerebral Palsy.Hilderley AJ, Wright FV, Taylor MJ, Chen JL, Fehlings D. Hilderley AJ, et al. Neurorehabil Neural Repair. 2023 Jan;37(1):16-26. doi: 10.1177/15459683221143503. Epub 2022 Dec 15. Neurorehabil Neural Repair. 2023. PMID: 36524254 Free PMC article. Clinical Trial.
- Active versus resting neuro-navigated robotic transcranial magnetic stimulation motor mapping.Kahl CK, Giuffre A, Wrightson JG, Kirton A, Condliffe EG, MacMaster FP, Zewdie E. Kahl CK, et al. Physiol Rep. 2022 Jun;10(12):e15346. doi: 10.14814/phy2.15346. Physiol Rep. 2022. PMID: 35748041 Free PMC article.
- Robotic mapping of motor cortex in children with perinatal stroke and hemiparesis.Kuo HC, Zewdie E, Giuffre A, Gan LS, Carlson HL, Wrightson J, Kirton A. Kuo HC, et al. Hum Brain Mapp. 2022 Aug 15;43(12):3745-3758. doi: 10.1002/hbm.25881. Epub 2022 Apr 22. Hum Brain Mapp. 2022. PMID: 35451540 Free PMC article.
- HABIT+tDCS: a study protocol of a randomised controlled trial (RCT) investigating the synergistic efficacy of hand-arm bimanual intensive therapy (HABIT) plus targeted non-invasive brain stimulation to improve upper extremity function in school-age children with unilateral cerebral palsy.Gordon AM, Ferre CL, Robert MT, Chin K, Brandao M, Friel KM. Gordon AM, et al. BMJ Open. 2022 Feb 21;12(2):e052409. doi: 10.1136/bmjopen-2021-052409. BMJ Open. 2022. PMID: 35190424 Free PMC article.
- Randomized Controlled Trial
- Analysis of Variance
- Cerebral Palsy / diagnostic imaging
- Cerebral Palsy / pathology*
- Cerebral Palsy / rehabilitation*
- Child
- Evoked Potentials, Motor / physiology
- Female
- Functional Laterality / physiology*
- Hand / physiology
- Humans
- Image Processing, Computer-Assisted
- Magnetic Resonance Imaging
- Male
- Motor Cortex / diagnostic imaging
- Motor Cortex / physiopathology*
- Motor Skills / physiology*
- Physical Therapy Modalities*
- Practice, Psychological
- Transcranial Magnetic Stimulation
- Full Text Sources
- Other Literature Sources
- Medical
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
![Figure 2](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4981562/bin/nihms746149f2.jpg)
![Figure 3](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4981562/bin/nihms746149f3.jpg)
Figure 4
Changes in magnitude of motor…
Figure 4
Changes in magnitude of motor evoked potentials in TMS maps after structured skill…
- Commentary: Skilled Bimanual Training Drives Motor Cortex Plasticity in Children With Unilateral Cerebral Palsy.Serrien DJ. Serrien DJ. Front Hum Neurosci. 2017 Jun 7;11:297. doi: 10.3389/fnhum.2017.00297. eCollection 2017. Front Hum Neurosci. 2017. PMID: 28638332 Free PMC article. No abstract available.
- Comparison of Structured Skill and Unstructured Practice During Intensive Bimanual Training in Children With Unilateral Spastic Cerebral Palsy.Brandão MB, Ferre C, Kuo HC, Rameckers EA, Bleyenheuft Y, Hung YC, Friel K, Gordon AM. Brandão MB, et al. Neurorehabil Neural Repair. 2014 Jun;28(5):452-61. doi: 10.1177/1545968313516871. Epub 2013 Dec 27. Neurorehabil Neural Repair. 2014. PMID: 24376067
- Does Corticospinal Tract Connectivity Influence the Response to Intensive Bimanual Therapy in Children With Unilateral Cerebral Palsy?Smorenburg AR, Gordon AM, Kuo HC, Ferre CL, Brandao M, Bleyenheuft Y, Carmel JB, Friel KM. Smorenburg AR, et al. Neurorehabil Neural Repair. 2017 Mar;31(3):250-260. doi: 10.1177/1545968316675427. Epub 2016 Nov 17. Neurorehabil Neural Repair. 2017. PMID: 27856938 Free PMC article.
- Less-Affected Hand Function in Children With Hemiparetic Unilateral Cerebral Palsy: A Comparison Study With Typically Developing Peers.Rich TL, Menk JS, Rudser KD, Feyma T, Gillick BT. Rich TL, et al. Neurorehabil Neural Repair. 2017 Oct-Nov;31(10-11):965-976. doi: 10.1177/1545968317739997. Epub 2017 Nov 12. Neurorehabil Neural Repair. 2017. PMID: 29130382 Free PMC article.
- Hand-arm bimanual intensive therapy including lower extremities (HABIT-ILE) for children with cerebral palsy.Bleyenheuft Y, Gordon AM. Bleyenheuft Y, et al. Phys Occup Ther Pediatr. 2014 Nov;34(4):390-403. doi: 10.3109/01942638.2014.932884. Epub 2014 Oct 1. Phys Occup Ther Pediatr. 2014. PMID: 25271469 Review.
- To constrain or not to constrain, and other stories of intensive upper extremity training for children with unilateral cerebral palsy.Gordon AM. Gordon AM. Dev Med Child Neurol. 2011 Sep;53 Suppl 4:56-61. doi: 10.1111/j.1469-8749.2011.04066.x. Dev Med Child Neurol. 2011. PMID: 21950396 Review.
- Pediatric Patients With Hemiplegia: A Systematic Review of a Randomized Controlled Trial.Varma A, Khan NR, Varma A, Sharma NS, Vagha JD, Naqvi WM, Besekar S. Varma A, et al. Cureus. 2023 Jan 23;15(1):e34074. doi: 10.7759/cureus.34074. eCollection 2023 Jan. Cureus. 2023. PMID: 36843815 Free PMC article. Review.
- Functional Neuroplasticity and Motor Skill Change Following Gross Motor Interventions for Children With Diplegic Cerebral Palsy.Hilderley AJ, Wright FV, Taylor MJ, Chen JL, Fehlings D. Hilderley AJ, et al. Neurorehabil Neural Repair. 2023 Jan;37(1):16-26. doi: 10.1177/15459683221143503. Epub 2022 Dec 15. Neurorehabil Neural Repair. 2023. PMID: 36524254 Free PMC article. Clinical Trial.
- Active versus resting neuro-navigated robotic transcranial magnetic stimulation motor mapping.Kahl CK, Giuffre A, Wrightson JG, Kirton A, Condliffe EG, MacMaster FP, Zewdie E. Kahl CK, et al. Physiol Rep. 2022 Jun;10(12):e15346. doi: 10.14814/phy2.15346. Physiol Rep. 2022. PMID: 35748041 Free PMC article.
- Robotic mapping of motor cortex in children with perinatal stroke and hemiparesis.Kuo HC, Zewdie E, Giuffre A, Gan LS, Carlson HL, Wrightson J, Kirton A. Kuo HC, et al. Hum Brain Mapp. 2022 Aug 15;43(12):3745-3758. doi: 10.1002/hbm.25881. Epub 2022 Apr 22. Hum Brain Mapp. 2022. PMID: 35451540 Free PMC article.
- HABIT+tDCS: a study protocol of a randomised controlled trial (RCT) investigating the synergistic efficacy of hand-arm bimanual intensive therapy (HABIT) plus targeted non-invasive brain stimulation to improve upper extremity function in school-age children with unilateral cerebral palsy.Gordon AM, Ferre CL, Robert MT, Chin K, Brandao M, Friel KM. Gordon AM, et al. BMJ Open. 2022 Feb 21;12(2):e052409. doi: 10.1136/bmjopen-2021-052409. BMJ Open. 2022. PMID: 35190424 Free PMC article.
- Randomized Controlled Trial
- Analysis of Variance
- Cerebral Palsy / diagnostic imaging
- Cerebral Palsy / pathology*
- Cerebral Palsy / rehabilitation*
- Child
- Evoked Potentials, Motor / physiology
- Female
- Functional Laterality / physiology*
- Hand / physiology
- Humans
- Image Processing, Computer-Assisted
- Magnetic Resonance Imaging
- Male
- Motor Cortex / diagnostic imaging
- Motor Cortex / physiopathology*
- Motor Skills / physiology*
- Physical Therapy Modalities*
- Practice, Psychological
- Transcranial Magnetic Stimulation
- Full Text Sources
- Other Literature Sources
- Medical
![Figure 4](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4981562/bin/nihms746149f4.jpg)
Source: PubMed