Ipsilateral Corticospinal Tract Excitability Contributes to the Severity of Mirror Movements in Unilateral Cerebral Palsy: A Case Series

Tonya L. Rich; Samuel Nemanich; Chao Ying Chen; Ellen N. Sutter; Tim Feyma; Linda E. Krach; Bernadette T. Gillick

doi:10.1177/1550059419899323

Ipsilateral Corticospinal Tract Excitability Contributes to the Severity of Mirror Movements in Unilateral Cerebral Palsy: A Case Series

Tonya L. Rich, Samuel Nemanich, Chao Ying Chen, Ellen N. Sutter, Tim Feyma, Linda E. Krach, Bernadette T. Gillick

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

Mirror movements (MM) can be a clinical manifestation of unilateral cerebral palsy (UCP) causing involuntary movements when attempting to use either hand for functional activities. Atypical development of the corticospinal tract (CST) contributes to impairments in observed motor movements and functional activities. However, little is known about the underlying neurophysiology and contribution of the CST to MM. The current case study characterizes MM in 13 children and young adults with UCP ranging in age from 7 to 19 years and includes clinical and neurophysiologic variables. Clinical profiles included MM of each hand (ie, Woods and Teuber), bimanual coordination and hand use (Assisting Hand Assessment [AHA]), and perception of performance (Canadian Occupational Performance Measure [COPM]). We measured the strength of motor-evoked potentials (MEP) elicited from single-pulse transcranial magnetic stimulation (TMS) of each hemisphere to create a ratio of hemispheric responses. Our sample included three types of CST circuitry: ipsilateral (n = 5), bilateral (n = 3), and contralateral (n = 4). The MEP ratio ranged from 0 to 1.45 (median 0.11) with greater MM observed in participants with ratios greater than 0.5. We observed a positive relationship between the MEP ratio and the more-affected MM score, meaning participants with larger ipsilateral responses from contralesional stimulation (eg, the contralesional hemisphere was stimulated with TMS resulting in an ipsilateral MEP response), as compared with contralateral responses, displayed greater MM than those that did not. There was no relationship between MM and function as measured by the AHA or COPM. These findings suggest a role of the contralesional hemisphere to MM, which could serve as a therapeutic target for interventions.

Original language	English (US)
Pages (from-to)	185-190
Number of pages	6
Journal	Clinical EEG and Neuroscience
Volume	51
Issue number	3
DOIs	https://doi.org/10.1177/1550059419899323
State	Published - May 1 2020

Bibliographical note

Funding Information:
https://orcid.org/0000-0002-9419-7259 Rich Tonya L. 1 Nemanich Samuel 1 Chen Chao-Ying 2 Sutter Ellen N. 3 Feyma Tim 4 Krach Linda E. 4 5 Gillick Bernadette T. 1 3 1 Department of Rehabilitation Medicine, Division of Rehabilitation Science, University of Minnesota, Minneapolis, MN, USA 2 Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong 3 Division of Physical Therapy, University of Minnesota, Minneapolis, MN, USA 4 Gillette Children’s Specialty Healthcare, St. Paul, MN, USA 5 Department of Rehabilitation Medicine, University of Minnesota, Minneapolis, MN, USA Tonya L. Rich, Department of Rehabilitation Medicine, Division of Rehabilitation Science, Medical School, University of Minnesota, 420 Delaware Street SE, MMC 388, Minneapolis, MN 55455, USA. Email: rich1038@umn.edu 1 2020 1550059419899323 29 7 2019 28 10 2019 27 11 2019 © EEG and Clinical Neuroscience Society (ECNS) 2020 2020 EEG and Clinical Neuroscience Society Mirror movements (MM) can be a clinical manifestation of unilateral cerebral palsy (UCP) causing involuntary movements when attempting to use either hand for functional activities. Atypical development of the corticospinal tract (CST) contributes to impairments in observed motor movements and functional activities. However, little is known about the underlying neurophysiology and contribution of the CST to MM. The current case study characterizes MM in 13 children and young adults with UCP ranging in age from 7 to 19 years and includes clinical and neurophysiologic variables. Clinical profiles included MM of each hand (ie, Woods and Teuber), bimanual coordination and hand use (Assisting Hand Assessment [AHA]), and perception of performance (Canadian Occupational Performance Measure [COPM]). We measured the strength of motor-evoked potentials (MEP) elicited from single-pulse transcranial magnetic stimulation (TMS) of each hemisphere to create a ratio of hemispheric responses. Our sample included three types of CST circuitry: ipsilateral (n = 5), bilateral (n = 3), and contralateral (n = 4). The MEP ratio ranged from 0 to 1.45 (median 0.11) with greater MM observed in participants with ratios greater than 0.5. We observed a positive relationship between the MEP ratio and the more-affected MM score, meaning participants with larger ipsilateral responses from contralesional stimulation (eg, the contralesional hemisphere was stimulated with TMS resulting in an ipsilateral MEP response), as compared with contralateral responses, displayed greater MM than those that did not. There was no relationship between MM and function as measured by the AHA or COPM. These findings suggest a role of the contralesional hemisphere to MM, which could serve as a therapeutic target for interventions. neonate pediatric noninvasive brain stimulation mirror movements corticospinal tract cerebral palsy American Academy of Cerebral Palsy and Developmental Medicine Travel Awards University of Minnesota https://doi.org/10.13039/100007249 MnDRIVE Fellowship Foundation for Physical Therapy https://doi.org/10.13039/100009713 Magistro Family Foundation Research Grant Eunice Kennedy Shriver National Institute of Child Health and Human Development https://doi.org/10.13039/100009633 1K01HD078484-01A1 edited-state corrected-proof typesetter ts1 We are grateful to the caregivers and children in our studies that made this work, and knowledge, possible. Author Contributions TLR: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval; agrees to be accountable for all aspects of work ensuring integrity and accuracy. SN: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval. C-YC: contributed to acquisition and interpretation; critically revised manuscript; gave final approval. ENS: contributed to analysis and interpretation; drafted manuscript; critically revised manuscript; gave final approval. TF: contributed to conception; critically revised manuscript; gave final approval. LEK: contributed to conception; critically revised manuscript; gave final approval. BTG: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval; agrees to be accountable for all aspects of work ensuring integrity and accuracy. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Funding sources are NIH NICHD 1K01HD078484-01A1 (BTG), Foundation for Physical Therapy (BTG), Cerebral Palsy Foundation (BTG), AACPDM Student Travel award (TR), and UMN MnDRIVE Fellowship (TR and STN). ORCID iD Tonya L. Rich https://orcid.org/0000-0002-9419-7259

Funding Information:
We are grateful to the caregivers and children in our studies that made this work, and knowledge, possible. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Funding sources are NIH NICHD 1K01HD078484-01A1 (BTG), Foundation for Physical Therapy (BTG), Cerebral Palsy Foundation (BTG), AACPDM Student Travel award (TR), and UMN MnDRIVE Fellowship (TR and STN).

Publisher Copyright:
© EEG and Clinical Neuroscience Society (ECNS) 2020.

Keywords

cerebral palsy
corticospinal tract
mirror movements
neonate
noninvasive brain stimulation
pediatric

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10.1177/1550059419899323

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@article{08b3604536b14875ba0b59c520ec902a,

title = "Ipsilateral Corticospinal Tract Excitability Contributes to the Severity of Mirror Movements in Unilateral Cerebral Palsy: A Case Series",

abstract = "Mirror movements (MM) can be a clinical manifestation of unilateral cerebral palsy (UCP) causing involuntary movements when attempting to use either hand for functional activities. Atypical development of the corticospinal tract (CST) contributes to impairments in observed motor movements and functional activities. However, little is known about the underlying neurophysiology and contribution of the CST to MM. The current case study characterizes MM in 13 children and young adults with UCP ranging in age from 7 to 19 years and includes clinical and neurophysiologic variables. Clinical profiles included MM of each hand (ie, Woods and Teuber), bimanual coordination and hand use (Assisting Hand Assessment [AHA]), and perception of performance (Canadian Occupational Performance Measure [COPM]). We measured the strength of motor-evoked potentials (MEP) elicited from single-pulse transcranial magnetic stimulation (TMS) of each hemisphere to create a ratio of hemispheric responses. Our sample included three types of CST circuitry: ipsilateral (n = 5), bilateral (n = 3), and contralateral (n = 4). The MEP ratio ranged from 0 to 1.45 (median 0.11) with greater MM observed in participants with ratios greater than 0.5. We observed a positive relationship between the MEP ratio and the more-affected MM score, meaning participants with larger ipsilateral responses from contralesional stimulation (eg, the contralesional hemisphere was stimulated with TMS resulting in an ipsilateral MEP response), as compared with contralateral responses, displayed greater MM than those that did not. There was no relationship between MM and function as measured by the AHA or COPM. These findings suggest a role of the contralesional hemisphere to MM, which could serve as a therapeutic target for interventions.",

keywords = "cerebral palsy, corticospinal tract, mirror movements, neonate, noninvasive brain stimulation, pediatric",

author = "Rich, {Tonya L.} and Samuel Nemanich and Chen, {Chao Ying} and Sutter, {Ellen N.} and Tim Feyma and Krach, {Linda E.} and Gillick, {Bernadette T.}",

note = "Funding Information: https://orcid.org/0000-0002-9419-7259 Rich Tonya L. 1 Nemanich Samuel 1 Chen Chao-Ying 2 Sutter Ellen N. 3 Feyma Tim 4 Krach Linda E. 4 5 Gillick Bernadette T. 1 3 1 Department of Rehabilitation Medicine, Division of Rehabilitation Science, University of Minnesota, Minneapolis, MN, USA 2 Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong 3 Division of Physical Therapy, University of Minnesota, Minneapolis, MN, USA 4 Gillette Children{\textquoteright}s Specialty Healthcare, St. Paul, MN, USA 5 Department of Rehabilitation Medicine, University of Minnesota, Minneapolis, MN, USA Tonya L. Rich, Department of Rehabilitation Medicine, Division of Rehabilitation Science, Medical School, University of Minnesota, 420 Delaware Street SE, MMC 388, Minneapolis, MN 55455, USA. Email: rich1038@umn.edu 1 2020 1550059419899323 29 7 2019 28 10 2019 27 11 2019 {\textcopyright} EEG and Clinical Neuroscience Society (ECNS) 2020 2020 EEG and Clinical Neuroscience Society Mirror movements (MM) can be a clinical manifestation of unilateral cerebral palsy (UCP) causing involuntary movements when attempting to use either hand for functional activities. Atypical development of the corticospinal tract (CST) contributes to impairments in observed motor movements and functional activities. However, little is known about the underlying neurophysiology and contribution of the CST to MM. The current case study characterizes MM in 13 children and young adults with UCP ranging in age from 7 to 19 years and includes clinical and neurophysiologic variables. Clinical profiles included MM of each hand (ie, Woods and Teuber), bimanual coordination and hand use (Assisting Hand Assessment [AHA]), and perception of performance (Canadian Occupational Performance Measure [COPM]). We measured the strength of motor-evoked potentials (MEP) elicited from single-pulse transcranial magnetic stimulation (TMS) of each hemisphere to create a ratio of hemispheric responses. Our sample included three types of CST circuitry: ipsilateral (n = 5), bilateral (n = 3), and contralateral (n = 4). The MEP ratio ranged from 0 to 1.45 (median 0.11) with greater MM observed in participants with ratios greater than 0.5. We observed a positive relationship between the MEP ratio and the more-affected MM score, meaning participants with larger ipsilateral responses from contralesional stimulation (eg, the contralesional hemisphere was stimulated with TMS resulting in an ipsilateral MEP response), as compared with contralateral responses, displayed greater MM than those that did not. There was no relationship between MM and function as measured by the AHA or COPM. These findings suggest a role of the contralesional hemisphere to MM, which could serve as a therapeutic target for interventions. neonate pediatric noninvasive brain stimulation mirror movements corticospinal tract cerebral palsy American Academy of Cerebral Palsy and Developmental Medicine Travel Awards University of Minnesota https://doi.org/10.13039/100007249 MnDRIVE Fellowship Foundation for Physical Therapy https://doi.org/10.13039/100009713 Magistro Family Foundation Research Grant Eunice Kennedy Shriver National Institute of Child Health and Human Development https://doi.org/10.13039/100009633 1K01HD078484-01A1 edited-state corrected-proof typesetter ts1 We are grateful to the caregivers and children in our studies that made this work, and knowledge, possible. Author Contributions TLR: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval; agrees to be accountable for all aspects of work ensuring integrity and accuracy. SN: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval. C-YC: contributed to acquisition and interpretation; critically revised manuscript; gave final approval. ENS: contributed to analysis and interpretation; drafted manuscript; critically revised manuscript; gave final approval. TF: contributed to conception; critically revised manuscript; gave final approval. LEK: contributed to conception; critically revised manuscript; gave final approval. BTG: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval; agrees to be accountable for all aspects of work ensuring integrity and accuracy. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Funding sources are NIH NICHD 1K01HD078484-01A1 (BTG), Foundation for Physical Therapy (BTG), Cerebral Palsy Foundation (BTG), AACPDM Student Travel award (TR), and UMN MnDRIVE Fellowship (TR and STN). ORCID iD Tonya L. Rich https://orcid.org/0000-0002-9419-7259 Funding Information: We are grateful to the caregivers and children in our studies that made this work, and knowledge, possible. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Funding sources are NIH NICHD 1K01HD078484-01A1 (BTG), Foundation for Physical Therapy (BTG), Cerebral Palsy Foundation (BTG), AACPDM Student Travel award (TR), and UMN MnDRIVE Fellowship (TR and STN). Publisher Copyright: {\textcopyright} EEG and Clinical Neuroscience Society (ECNS) 2020.",

year = "2020",

month = may,

day = "1",

doi = "10.1177/1550059419899323",

language = "English (US)",

volume = "51",

pages = "185--190",

journal = "Clinical EEG and Neuroscience",

issn = "1550-0594",

publisher = "EEG and Clinical Neuroscience Society (ECNS)",

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TY - JOUR

T1 - Ipsilateral Corticospinal Tract Excitability Contributes to the Severity of Mirror Movements in Unilateral Cerebral Palsy

T2 - A Case Series

AU - Rich, Tonya L.

AU - Nemanich, Samuel

AU - Chen, Chao Ying

AU - Sutter, Ellen N.

AU - Feyma, Tim

AU - Krach, Linda E.

AU - Gillick, Bernadette T.

N1 - Funding Information: https://orcid.org/0000-0002-9419-7259 Rich Tonya L. 1 Nemanich Samuel 1 Chen Chao-Ying 2 Sutter Ellen N. 3 Feyma Tim 4 Krach Linda E. 4 5 Gillick Bernadette T. 1 3 1 Department of Rehabilitation Medicine, Division of Rehabilitation Science, University of Minnesota, Minneapolis, MN, USA 2 Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong 3 Division of Physical Therapy, University of Minnesota, Minneapolis, MN, USA 4 Gillette Children’s Specialty Healthcare, St. Paul, MN, USA 5 Department of Rehabilitation Medicine, University of Minnesota, Minneapolis, MN, USA Tonya L. Rich, Department of Rehabilitation Medicine, Division of Rehabilitation Science, Medical School, University of Minnesota, 420 Delaware Street SE, MMC 388, Minneapolis, MN 55455, USA. Email: rich1038@umn.edu 1 2020 1550059419899323 29 7 2019 28 10 2019 27 11 2019 © EEG and Clinical Neuroscience Society (ECNS) 2020 2020 EEG and Clinical Neuroscience Society Mirror movements (MM) can be a clinical manifestation of unilateral cerebral palsy (UCP) causing involuntary movements when attempting to use either hand for functional activities. Atypical development of the corticospinal tract (CST) contributes to impairments in observed motor movements and functional activities. However, little is known about the underlying neurophysiology and contribution of the CST to MM. The current case study characterizes MM in 13 children and young adults with UCP ranging in age from 7 to 19 years and includes clinical and neurophysiologic variables. Clinical profiles included MM of each hand (ie, Woods and Teuber), bimanual coordination and hand use (Assisting Hand Assessment [AHA]), and perception of performance (Canadian Occupational Performance Measure [COPM]). We measured the strength of motor-evoked potentials (MEP) elicited from single-pulse transcranial magnetic stimulation (TMS) of each hemisphere to create a ratio of hemispheric responses. Our sample included three types of CST circuitry: ipsilateral (n = 5), bilateral (n = 3), and contralateral (n = 4). The MEP ratio ranged from 0 to 1.45 (median 0.11) with greater MM observed in participants with ratios greater than 0.5. We observed a positive relationship between the MEP ratio and the more-affected MM score, meaning participants with larger ipsilateral responses from contralesional stimulation (eg, the contralesional hemisphere was stimulated with TMS resulting in an ipsilateral MEP response), as compared with contralateral responses, displayed greater MM than those that did not. There was no relationship between MM and function as measured by the AHA or COPM. These findings suggest a role of the contralesional hemisphere to MM, which could serve as a therapeutic target for interventions. neonate pediatric noninvasive brain stimulation mirror movements corticospinal tract cerebral palsy American Academy of Cerebral Palsy and Developmental Medicine Travel Awards University of Minnesota https://doi.org/10.13039/100007249 MnDRIVE Fellowship Foundation for Physical Therapy https://doi.org/10.13039/100009713 Magistro Family Foundation Research Grant Eunice Kennedy Shriver National Institute of Child Health and Human Development https://doi.org/10.13039/100009633 1K01HD078484-01A1 edited-state corrected-proof typesetter ts1 We are grateful to the caregivers and children in our studies that made this work, and knowledge, possible. Author Contributions TLR: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval; agrees to be accountable for all aspects of work ensuring integrity and accuracy. SN: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval. C-YC: contributed to acquisition and interpretation; critically revised manuscript; gave final approval. ENS: contributed to analysis and interpretation; drafted manuscript; critically revised manuscript; gave final approval. TF: contributed to conception; critically revised manuscript; gave final approval. LEK: contributed to conception; critically revised manuscript; gave final approval. BTG: contributed to conception and design; contributed to acquisition, analysis, and interpretation; drafted manuscript; critically revised manuscript; gave final approval; agrees to be accountable for all aspects of work ensuring integrity and accuracy. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Funding sources are NIH NICHD 1K01HD078484-01A1 (BTG), Foundation for Physical Therapy (BTG), Cerebral Palsy Foundation (BTG), AACPDM Student Travel award (TR), and UMN MnDRIVE Fellowship (TR and STN). ORCID iD Tonya L. Rich https://orcid.org/0000-0002-9419-7259 Funding Information: We are grateful to the caregivers and children in our studies that made this work, and knowledge, possible. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Funding sources are NIH NICHD 1K01HD078484-01A1 (BTG), Foundation for Physical Therapy (BTG), Cerebral Palsy Foundation (BTG), AACPDM Student Travel award (TR), and UMN MnDRIVE Fellowship (TR and STN). Publisher Copyright: © EEG and Clinical Neuroscience Society (ECNS) 2020.

PY - 2020/5/1

Y1 - 2020/5/1

N2 - Mirror movements (MM) can be a clinical manifestation of unilateral cerebral palsy (UCP) causing involuntary movements when attempting to use either hand for functional activities. Atypical development of the corticospinal tract (CST) contributes to impairments in observed motor movements and functional activities. However, little is known about the underlying neurophysiology and contribution of the CST to MM. The current case study characterizes MM in 13 children and young adults with UCP ranging in age from 7 to 19 years and includes clinical and neurophysiologic variables. Clinical profiles included MM of each hand (ie, Woods and Teuber), bimanual coordination and hand use (Assisting Hand Assessment [AHA]), and perception of performance (Canadian Occupational Performance Measure [COPM]). We measured the strength of motor-evoked potentials (MEP) elicited from single-pulse transcranial magnetic stimulation (TMS) of each hemisphere to create a ratio of hemispheric responses. Our sample included three types of CST circuitry: ipsilateral (n = 5), bilateral (n = 3), and contralateral (n = 4). The MEP ratio ranged from 0 to 1.45 (median 0.11) with greater MM observed in participants with ratios greater than 0.5. We observed a positive relationship between the MEP ratio and the more-affected MM score, meaning participants with larger ipsilateral responses from contralesional stimulation (eg, the contralesional hemisphere was stimulated with TMS resulting in an ipsilateral MEP response), as compared with contralateral responses, displayed greater MM than those that did not. There was no relationship between MM and function as measured by the AHA or COPM. These findings suggest a role of the contralesional hemisphere to MM, which could serve as a therapeutic target for interventions.

AB - Mirror movements (MM) can be a clinical manifestation of unilateral cerebral palsy (UCP) causing involuntary movements when attempting to use either hand for functional activities. Atypical development of the corticospinal tract (CST) contributes to impairments in observed motor movements and functional activities. However, little is known about the underlying neurophysiology and contribution of the CST to MM. The current case study characterizes MM in 13 children and young adults with UCP ranging in age from 7 to 19 years and includes clinical and neurophysiologic variables. Clinical profiles included MM of each hand (ie, Woods and Teuber), bimanual coordination and hand use (Assisting Hand Assessment [AHA]), and perception of performance (Canadian Occupational Performance Measure [COPM]). We measured the strength of motor-evoked potentials (MEP) elicited from single-pulse transcranial magnetic stimulation (TMS) of each hemisphere to create a ratio of hemispheric responses. Our sample included three types of CST circuitry: ipsilateral (n = 5), bilateral (n = 3), and contralateral (n = 4). The MEP ratio ranged from 0 to 1.45 (median 0.11) with greater MM observed in participants with ratios greater than 0.5. We observed a positive relationship between the MEP ratio and the more-affected MM score, meaning participants with larger ipsilateral responses from contralesional stimulation (eg, the contralesional hemisphere was stimulated with TMS resulting in an ipsilateral MEP response), as compared with contralateral responses, displayed greater MM than those that did not. There was no relationship between MM and function as measured by the AHA or COPM. These findings suggest a role of the contralesional hemisphere to MM, which could serve as a therapeutic target for interventions.

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Ipsilateral Corticospinal Tract Excitability Contributes to the Severity of Mirror Movements in Unilateral Cerebral Palsy: A Case Series

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