Fingertip force control during bimanual object lifting in hemiplegic cerebral palsy

Bert Steenbergen, Jeanne Charles, Andrew M Gordon, Bert Steenbergen, Jeanne Charles, Andrew M Gordon

Abstract

In the present study we examined unimanual and bimanual fingertip force control during grasping in children with hemiplegic cerebral palsy (CP). Participants lifted, transported and released an object with one hand or both hands together in order to examine the effect on fingertip force control for each hand separately and to determine whether any benefit exists for the affected hand when it performed the task concurrently with the less-affected hand. Seven children with hemiplegic CP performed the task while their movement and fingertip force control were measured. In the bimanual conditions, the weight of the instrumented objects was equal or unequal. The durations of the all temporal phases for the less-affected hand were prolonged during bimanual control compared to unimanual control. We observed close synchrony of both hands when the task was performed with both hands, despite large differences in duration between both hands when they performed separately. There was a marginal benefit for two of the five force related variables for the affected hand (grip force at onset of load force, and peak grip force) when it transported the object simultaneously with the less-affected hand. Collectively, these results corroborate earlier findings of reaching studies that showed slowing down of the less-affected hand when it moved together with the affected hand. A new finding that extends these studies is that bimanual tasks may have the potential to facilitate force control of the affected hand. The implications of these findings for recent rehabilitative therapies in children with CP that make use of bimanual training are discussed.

Figures

Fig. 1
Fig. 1
Grip force, load force, and position traces from the less-affected hand of a child with CP while performing the task, along with the measures examined: finger difference (T0-T1) preload phase (T1-T2), onset of positive load force increase (T2), loading phase (T2-T3), transport phase T3-T4), replacement phase (T4-5). Total movement time is defined as the duration between T0 and T5 and signifies the duration of the complete grasp, transport and release movement. For elaborate description of the phases, see text
Fig. 2
Fig. 2
Examples of force profiles for the affected hand (left panels) and less-affected hand (rightpanels) in the unimanual conditions (upper panels) and bimanual equal-weight conditions (lowerpanels) when lifting objects of 250 g. T0-T3 represents the isometric force increase, encompassing finger difference, preload, and load phases. T3-T4 represents transport phase, and T4-T5 represents the replacement phase. The total movement time is denoted T0-T5
Fig. 3
Fig. 3
Duration of the different movement phases for the affected and less-affected hand. Shown are the durations in the unimanual conditions (a), bimanual equal-weight conditions (b), and bimanual unequal-weight conditions (c). All durations are calculated relative to object contact (zero). These include load-force onset (a), peak grip-force rate (b), peak load-force rate (c), object lift-off (d), peak grip-force (e), replacement (f), and release (g). Error bars represent standard error
Fig. 4
Fig. 4
Graphical display of the hand × condition interaction that was found for Total Movement Time. Error bars represent standard error
Fig. 5
Fig. 5
Graphical display of the hand × condition interaction that was found for grip force at load force onset. Error bars represent standard error
Fig. 6
Fig. 6
Graphical display of the hand × condition interaction that was found for peak grip force rate. Error bars represent standard error

References

    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1007/BF00230856', 'is_inner': False, 'url': 'https://doi.org/10.1007/bf00230856'}, {'type': 'PubMed', 'value': '2257909', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/2257909/'}]}
    2. Aizawa H, Mushiake H, Inase M, Tanji J (1990) An output zone of the monkey primary motor cortex specialized for bilateral hand movement. Exp Brain Res 82:219–221
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1093/brain/96.4.653', 'is_inner': False, 'url': 'https://doi.org/10.1093/brain/96.4.653'}, {'type': 'PubMed', 'value': '4204228', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/4204228/'}]}
    2. Brinkman J, Kuypers HGJ (1973) Cerebral control of contralateral and ipsilateral arm, hand and finger movements in split-brain rhesus-monkey. Brain 96:653–674
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/0028-3932(89)90019-5', 'is_inner': False, 'url': 'https://doi.org/10.1016/0028-3932(89)90019-5'}, {'type': 'PubMed', 'value': '2710320', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/2710320/'}]}
    2. Brown JV, Schumacher U, Rohlman A, Ettlinger G, Schmidt RC, Skreczek W (1989) Aimed movements to visual targets in hemiplegic and normal children: is the “good” hand of children with infantile hemiplegia also normal? Neuropsychologia 27:283–302
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.brainresrev.2005.03.005', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.brainresrev.2005.03.005'}, {'type': 'PubMed', 'value': '15904971', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15904971/'}]}
    2. Carson RG (2005) Neural pathways mediating bilateral interactions between the upper limbs. Brain Res Rev 49(3):641–662
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '15502274', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15502274/'}]}
    2. Cauraugh JH (2004) Coupled rehabilitation protocols and neural plasticity: upper extremity improvements in chronic hemiparesis. Restor Neurol Neurosci 22:337–347
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.pneurobio.2005.04.001', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.pneurobio.2005.04.001'}, {'type': 'PubMed', 'value': '15885874', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15885874/'}]}
    2. Cauraugh JH, Summers JJ (2005) Neural plasticity and bilateral movements: a rehabilitation approach for chronic stroke. Progr Neurobiol 75:309–320
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.clinbiomech.2004.11.015', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.clinbiomech.2004.11.015'}, {'type': 'PubMed', 'value': '15737445', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15737445/'}]}
    2. Chang J, Wu T, Wu W, Su F (2005) Kinematical measure for spastic reaching in children with cerebral palsy. Clinic Biomech 20:381–388
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1155/NP.2005.245', 'is_inner': False, 'url': 'https://doi.org/10.1155/np.2005.245'}, {'type': 'PMC', 'value': 'PMC2565448', 'is_inner': False, 'url': 'http://www.ncbi.nlm.nih.gov/pmc/articles/pmc2565448/'}, {'type': 'PubMed', 'value': '16097492', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16097492/'}]}
    2. Charles J, Gordon AM (2005) A critical review of constraint-induced movement therapy and forced-use in children with hemiplegia. Neural Plast 12:245–262
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1017/S0012162206002039', 'is_inner': False, 'url': 'https://doi.org/10.1017/s0012162206002039'}, {'type': 'PubMed', 'value': '17044964', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/17044964/'}]}
    2. Charles J, Gordon AM (2006) Development of hand-arm bimanual intensive therapy (HABIT) for improving bimanual coordination in children with hemiplegic cerebral palsy. Dev Med Child Neurol 48:931–936
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1093/brain/112.3.749', 'is_inner': False, 'url': 'https://doi.org/10.1093/brain/112.3.749'}, {'type': 'PubMed', 'value': '2731028', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/2731028/'}]}
    2. Colebatch JG, Gandevia SC (1989) The distribution of muscular weakness in upper motor neuron lesions affecting the arm. Brain 112:749–763
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '14577827', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/14577827/'}]}
    2. DeLuca SC, Echols K, Ramey SL, Taub E (2003) Pediatric constraint-induced movement therapy for a young child with cerebral palsy: two episodes of care. Phys Ther 83:1003–1013
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1152/jn.00335.2001', 'is_inner': False, 'url': 'https://doi.org/10.1152/jn.00335.2001'}, {'type': 'PubMed', 'value': '12466464', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/12466464/'}]}
    2. Donchin O, Gribova A, Steinberg O, Mitz AR, Bergman H, Vaadia E (2002) Single-unit activity related to bimanual arm movements in the primary and supplementary motor cortices. J Neurophys 88:3498–3517
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1017/S0012162203001397', 'is_inner': False, 'url': 'https://doi.org/10.1017/s0012162203001397'}, {'type': 'PubMed', 'value': '14580130', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/14580130/'}]}
    2. Duff SV, Gordon AM (2003) Learning of grasp control in children with hemiplegic cerebral palsy. Dev Med Child Neurol 45:746–757
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '1916022', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/1916022/'}]}
    2. Eliasson AC, Gordon AM, Forssberg H (1991) Basic co-ordination of manipulative forces of children with cerebral palsy. Dev Med Child Neurol 33:661–670
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '1559601', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/1559601/'}]}
    2. Eliasson AC, Gordon AM, Forssberg H (1992) Impaired anticipatory control of isometric forces during grasping by children with cerebral palsy. Dev Med Child Neurol 34(3):216–225
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1017/S0012162205000502', 'is_inner': False, 'url': 'https://doi.org/10.1017/s0012162205000502'}, {'type': 'PubMed', 'value': '15832550', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15832550/'}]}
    2. Eliasson AC, Krumlinde-Sundholm L, Shaw K, Wang C (2005) Effects of constraint-induced movement therapy in young children with hemiplegic cerebral palsy: an adapted model. Dev Med Child Neurol 47:266–275
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1006/jecp.2000.2623', 'is_inner': False, 'url': 'https://doi.org/10.1006/jecp.2000.2623'}, {'type': 'PubMed', 'value': '11511132', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11511132/'}]}
    2. Fagard J, Hardy-Léger I, Kervella C, Marks A (2001) Changes in interhemispheric transfer rate and the development of bimanual coordination during childhood. J Exp Child Psychol 80:1–22
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1093/brain/122.6.1157', 'is_inner': False, 'url': 'https://doi.org/10.1093/brain/122.6.1157'}, {'type': 'PubMed', 'value': '10356067', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/10356067/'}]}
    2. Forssberg H, Eliasson AC, Redon-Zouitenn C, Mercuri E, Dubowitz L (1999) Impaired grip-lift synergy in children with unilateral brain lesions. Brain 122:1157–1168
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '17979861', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/17979861/'}]}
    2. Gordon AM, Schneider JA, Chinnan A, Charles J (2007) Efficacy of Hand-arm bimanual intensive therapy (HABIT) in children with cerebral palsy. Dev Med Child Neurol 49:830–838
    1. Gordon AM, Steenbergen B (in press) Bimanual coordination in children with cerebral palsy. In: Eliasson AC, Burtner P (eds) Child with cerebral palsy: management of the upper extremity. Clinics in Developmental Medicine. MacKeith Press, London
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1017/S0012162299000365', 'is_inner': False, 'url': 'https://doi.org/10.1017/s0012162299000365'}, {'type': 'PubMed', 'value': '10210250', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/10210250/'}]}
    2. Gordon AM, Charles J, Duff SV (1999) Fingertip forces during object manipulation in children with hemiplegic cerebral palsy. II: bilateral coordination. Dev Med Child Neurol 41:176–185
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1017/S0012162299001231', 'is_inner': False, 'url': 'https://doi.org/10.1017/s0012162299001231'}, {'type': 'PubMed', 'value': '10503916', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/10503916/'}]}
    2. Gordon AM, Duff SV (1999) Relation between clinical measures and fine manipulative control in children with hemiplegic cerebral palsy. Dev Med Child Neurol 41:586–591
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1203/01.pdr.0000242370.41469.74', 'is_inner': False, 'url': 'https://doi.org/10.1203/01.pdr.0000242370.41469.74'}, {'type': 'PubMed', 'value': '16988186', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16988186/'}]}
    2. Gordon AM, Charles J, Steenbergen B (2006a) Fingertip force planning during grasp is disrupted by impaired sensorimotor integration in children with hemiplegic cerebral palsy. Ped Res 60:587–591
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1542/peds.2005-1009', 'is_inner': False, 'url': 'https://doi.org/10.1542/peds.2005-1009'}, {'type': 'PubMed', 'value': '16510616', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16510616/'}]}
    2. Gordon AM, Charles J, Wolf SL (2006b) Efficacy of contraint-induced movement therapy on more-affected upper-extremity use in children with hemiplegic cerebral palsy is not age-dependent. Pediatrics 117:363–373
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '5788487', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/5788487/'}]}
    2. Jebsen RH, Taylor N, Trieschmann RB (1969) Objective and standardized test of hand function. Arch Phys Med Rehab (Chicago) 50:311
    1. None
    2. Jeeves MA, Silver PH, Milne AB (1988) Role of the corpus callosum in the development of a bimanual motor skill. Dev Neuropsych 4(4):305–323
    1. None
    2. Kaufman AS, Kaufman NL (1990) Kaufman brief intelligence test. American Guidance Services, Circle Pines, MN
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1126/science.424729', 'is_inner': False, 'url': 'https://doi.org/10.1126/science.424729'}, {'type': 'PubMed', 'value': '424729', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/424729/'}]}
    2. Kelso JAS, Southard DL, Goodman D (1979) On the nature of human interlimb coordination. Science 203:1029–1031
    1. None
    2. Krumlinde-Sundholm L, Eliasson AC (2003) Development of the assisting hand assessment: a Rasch-built measure intended for children with unilateral upper limb impairments. Dev Med Child Neurol 10:16
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '17376135', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/17376135/'}]}
    2. Krumlinde-Sundholm L, Holmefur M, Kottorp A, Eliasson AC (2007) The assisting hand assessment: current evidence of validity, reliability, and responsiveness to change. Dev Med Child Neurol 49:259–264
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1017/S0012162200001353', 'is_inner': False, 'url': 'https://doi.org/10.1017/s0012162200001353'}, {'type': 'PubMed', 'value': '11104343', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11104343/'}]}
    2. Kuhtz-Buschbeck JP, Sundholm LK, Eliasson AC, Forssberg H (2000) Quantitative assessment of mirror movements in children and adolescents with hemiplegic cerebral palsy. Dev Med Child Neurol 42(11):728–736
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1001/jama.292.15.1853', 'is_inner': False, 'url': 'https://doi.org/10.1001/jama.292.15.1853'}, {'type': 'PMC', 'value': 'PMC2930817', 'is_inner': False, 'url': 'http://www.ncbi.nlm.nih.gov/pmc/articles/pmc2930817/'}, {'type': 'PubMed', 'value': '15494583', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15494583/'}]}
    2. 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(15):1853–1861
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '4078279', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/4078279/'}]}
    2. Mackinnon SE, Dellon AL (1985) Two-point discrimination tester. J Hand Surg [Am] 10:906–907
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '10661755', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/10661755/'}]}
    2. Mudie MH, Matyas TA (2000) Can simultaneous bilateral movement involve the undamaged hemisphere in reconstruction of neural networks damaged by stroke? Dis Reh 22(1–2):23–37
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1007/s00221-005-0327-0', 'is_inner': False, 'url': 'https://doi.org/10.1007/s00221-005-0327-0'}, {'type': 'PubMed', 'value': '16538378', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16538378/'}]}
    2. Mutsaarts M, Steenbergen B, Bekkering H (2006) Anticipatory planning deficits and task context effects in hemiparetic cerebral palsy. Exp Brain Res 172(2):151–162
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1093/brain/96.3.471', 'is_inner': False, 'url': 'https://doi.org/10.1093/brain/96.3.471'}, {'type': 'PubMed', 'value': '4517841', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/4517841/'}]}
    2. Nathan PW, Smith MC (1973) Effects of 2 unilateral cordotomies on motility of lower limbs. Brain 96:471–494
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S0387-7604(98)00094-1', 'is_inner': False, 'url': 'https://doi.org/10.1016/s0387-7604(98)00094-1'}, {'type': 'PubMed', 'value': '10372901', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/10372901/'}]}
    2. Nezu A, Kimura S, Takeshita S, Tanaka M (1999) Functional recovery in hemiplegic cerebral palsy: ipsilateral electromyographic responses to focal transcranial magnetic stimulation. Brain Dev 21(3):162–165
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '3771300', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/3771300/'}]}
    2. Njiokiktjien C, Driessen M, Habraken L (1986) Development of supination-pronation movements in normal children. Hum Neurobiol 5:199–203
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '9233360', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/9233360/'}]}
    2. Okumura A, Kato T, Kuno K, Hayakawa F, Watanabe K (1997) MRI findings in patients with spastic cerebral palsy. 2. Correlation with type of cerebral palsy. Dev Med Child Neurol 39:369–372
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1007/s00221-003-1716-x', 'is_inner': False, 'url': 'https://doi.org/10.1007/s00221-003-1716-x'}, {'type': 'PubMed', 'value': '14689146', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/14689146/'}]}
    2. Roon van D, Steenbergen B, Meulenbroek RGJ (2004) Trunk recruitment during spoon use in tetraparetic cerebral palsy. Exp Brain Res 155:186–195
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '7698522', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/7698522/'}]}
    2. Sugden D, Utley A (1995) Interlimb coupling in children with hemiplegic cerebral palsy. Dev Med Child Neurol 37:293–309
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1002/ana.20297', 'is_inner': False, 'url': 'https://doi.org/10.1002/ana.20297'}, {'type': 'PubMed', 'value': '15562409', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15562409/'}]}
    2. 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 56:854–863
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1007/BF00241378', 'is_inner': False, 'url': 'https://doi.org/10.1007/bf00241378'}, {'type': 'PubMed', 'value': '8817260', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/8817260/'}]}
    2. Steenbergen B, Hulstijn W, de Vries A, Berger M (1996) Bimanual movement coordination in spastic hemiparesis. Exp Brain Res 110:91-98
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S0167-9457(00)00006-3', 'is_inner': False, 'url': 'https://doi.org/10.1016/s0167-9457(00)00006-3'}]}
    2. Steenbergen B, Van Thiel E, Hulstijn W, Meulenbroek RGJ (2000) The coordination of reaching and grasping in spastic hemiparesis. Hum Mov Sci 19:75–105
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1017/S0012162206001666', 'is_inner': False, 'url': 'https://doi.org/10.1017/s0012162206001666'}, {'type': 'PubMed', 'value': '16904028', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16904028/'}]}
    2. Steenbergen B, Gordon AM (2006) Activity limitation in hemiplegic cerebral palsy: evidence for disorders in motor planning. Dev Med Child Neurol 48:780–783
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.jns.2006.01.005', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.jns.2006.01.005'}, {'type': 'PubMed', 'value': '16476449', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16476449/'}]}
    2. Stewart KC, Cauraugh JH, Summers JJ (2006) Bilateral movement training and stroke rehabilitation: a systematic review and meta-analysis. J Neurol Sci 244(1–2):89–95
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '27620374', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/27620374/'}]}
    2. Taub E, Wolf SL (1997) Constraint induction techniques to facilitate upper extremity use in stroke patients. Top Stroke Rehab 3:38–61
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '10659807', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/10659807/'}]}
    2. Taub E, Uswatte G, Pidikiti R (1999) Constraint-induced movement therapy: a new family of techniques with broad application to physical reahbilitation—a clinical review. J Rehab Res Dev 36:237–251
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1542/peds.113.2.305', 'is_inner': False, 'url': 'https://doi.org/10.1542/peds.113.2.305'}, {'type': 'PubMed', 'value': '14754942', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/14754942/'}]}
    2. Taub E, Ramey SL, DeLuca S, Echols K (2004) Efficacy of constraint-induced movement therapy for children with cerebral palsy with asymmetric motor impairment. Pediatrics 113:305–312
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '11303111', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11303111/'}]}
    2. Thiel van E, Steenbergen B (2001) Shoulder and hand displacements during hitting, reaching, and grasping movements in hemiparetic cerebral palsy. Mot Control 2:72–88
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S0028-3932(01)00075-6', 'is_inner': False, 'url': 'https://doi.org/10.1016/s0028-3932(01)00075-6'}, {'type': 'PubMed', 'value': '11595259', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11595259/'}]}
    2. Thiel van E, Meulenbroek RGJ, Smeets JBJ, Hulstijn W (2002) Fast adjustments of ongoing movements in hemiparetic cerebral palsy. Neuropsychologia 40:16–27
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '9652781', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/9652781/'}]}
    2. Utley A, Sugden DA (1998) Interlimb coupling in children with hemiplegic cerebral palsy during reaching and grasping at speed. Dev Med Child Neurol 40:396–404
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1080/13638490500155573', 'is_inner': False, 'url': 'https://doi.org/10.1080/13638490500155573'}, {'type': 'PubMed', 'value': '16449071', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16449071/'}]}
    2. Utley A, Steenbergen B (2006) Discrete bimanual co-ordination in children and young adolescents with hemiparetic cerebral palsy: recent findings, implications and future research directions. Ped Rehab 9(2):127–136
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S0001-6918(02)00041-0', 'is_inner': False, 'url': 'https://doi.org/10.1016/s0001-6918(02)00041-0'}, {'type': 'PubMed', 'value': '12102113', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/12102113/'}]}
    2. Volman MJM, Wijnroks A, Vermeer A (2002) Bimanual circle drawing in children with spastic hemiparesis: effect of coupling modes on the performance of the impaired and unimpaired arms. Acta Psychol 110(2–3):339–356
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1002/ana.10686', 'is_inner': False, 'url': 'https://doi.org/10.1002/ana.10686'}, {'type': 'PubMed', 'value': '14520658', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/14520658/'}]}
    2. Werhahn KJ, Conforto AB, Kadom N, Hallet M, Cohen LG (2003) Contribution of the ipsilateral motor cortex to recovery after chronic stroke. Ann Neurol 54:464–472
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '11022069', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11022069/'}]}
    2. Whitall J, Waller SM, Silver KHC, et al (2000) Repetitive bilateral arm training with rhythmic auditory cueing improves motor function in chronic hemiparetic stroke. Stroke 31(10):2390–2395
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1001/jama.296.17.2095', 'is_inner': False, 'url': 'https://doi.org/10.1001/jama.296.17.2095'}, {'type': 'PubMed', 'value': '17077374', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/17077374/'}]}
    2. Wolf SL, Winstein CJ, Miller JP, Taub E, Uswatte G, Morris D, Giuliani C, Light KE, Nichols-Larsen D (2006) Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. J Am Med Assoc 296:2095–2104

Source: PubMed

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