Progressive recruitment of contralesional cortico‐reticulospinal pathways drives motor impairment post stroke
Key points Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy. It has been proposed that flexion synergy expression is related to re...
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| Published in | The Journal of physiology Vol. 596; no. 7; pp. 1211 - 1225 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Wiley Subscription Services, Inc
01.04.2018
John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0022-3751 1469-7793 1469-7793 |
| DOI | 10.1113/JP274968 |
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| Abstract | Key points
Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy.
It has been proposed that flexion synergy expression is related to reduced output from ipsilesional motor cortex and corticospinal pathways.
In this human subjects study, we provide evidence that the magnitude of flexion synergy expression is instead related to a progressive, task‐dependent recruitment of contralesional cortex.
We also provide evidence that recruitment of contralesional cortex may induce excessive activation of ipsilateral reticulospinal descending motor pathways that cannot produce discrete movements, leading to flexion synergy expression.
We interpret these findings as an adaptive strategy that preserves low‐level motor control at the cost of fine motor control.
A hallmark of hemiparetic stroke is the loss of fine motor control in the contralesional arm and hand and the constraint to a grouped movement pattern known as the flexion synergy. In the flexion synergy, increasing shoulder abductor activation drives progressive, involuntary increases in elbow, wrist and finger flexion. The neural mechanisms underlying this phenomenon remain unclear. Here, across 25 adults with moderate to severe hemiparesis following chronic stroke and 18 adults without neurological injury, we test the overall hypothesis that two inter‐related mechanisms are necessary for flexion synergy expression: increased task‐dependent activation of the intact, contralesional cortex and recruitment of contralesional motor pathways via ipsilateral reticulospinal projections. First, we imaged brain activation in real time during reaching motions progressively constrained by flexion synergy expression. Using this approach, we found that cortical activity indeed shifts towards the contralesional hemisphere in direct proportion to the degree of shoulder abduction loading in the contralesional arm. We then leveraged the post‐stroke reemergence of a developmental brainstem reflex to show that anatomically diffuse reticulospinal motor pathways are active during synergy expression. We interpret this progressive recruitment of contralesional cortico‐reticulospinal pathways as an adaptive strategy that preserves low‐level motor control at the cost of fine motor control.
Key points
Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy.
It has been proposed that flexion synergy expression is related to reduced output from ipsilesional motor cortex and corticospinal pathways.
In this human subjects study, we provide evidence that the magnitude of flexion synergy expression is instead related to a progressive, task‐dependent recruitment of contralesional cortex.
We also provide evidence that recruitment of contralesional cortex may induce excessive activation of ipsilateral reticulospinal descending motor pathways that cannot produce discrete movements, leading to flexion synergy expression.
We interpret these findings as an adaptive strategy that preserves low‐level motor control at the cost of fine motor control. |
|---|---|
| AbstractList | Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy.
It has been proposed that flexion synergy expression is related to reduced output from ipsilesional motor cortex and corticospinal pathways.
In this human subjects study, we provide evidence that the magnitude of flexion synergy expression is instead related to a progressive, task‐dependent recruitment of contralesional cortex.
We also provide evidence that recruitment of contralesional cortex may induce excessive activation of ipsilateral reticulospinal descending motor pathways that cannot produce discrete movements, leading to flexion synergy expression.
We interpret these findings as an adaptive strategy that preserves low‐level motor control at the cost of fine motor control. Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy. It has been proposed that flexion synergy expression is related to reduced output from ipsilesional motor cortex and corticospinal pathways. In this human subjects study, we provide evidence that the magnitude of flexion synergy expression is instead related to a progressive, task-dependent recruitment of contralesional cortex. We also provide evidence that recruitment of contralesional cortex may induce excessive activation of ipsilateral reticulospinal descending motor pathways that cannot produce discrete movements, leading to flexion synergy expression. We interpret these findings as an adaptive strategy that preserves low-level motor control at the cost of fine motor control.KEY POINTSActivation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy. It has been proposed that flexion synergy expression is related to reduced output from ipsilesional motor cortex and corticospinal pathways. In this human subjects study, we provide evidence that the magnitude of flexion synergy expression is instead related to a progressive, task-dependent recruitment of contralesional cortex. We also provide evidence that recruitment of contralesional cortex may induce excessive activation of ipsilateral reticulospinal descending motor pathways that cannot produce discrete movements, leading to flexion synergy expression. We interpret these findings as an adaptive strategy that preserves low-level motor control at the cost of fine motor control.A hallmark of hemiparetic stroke is the loss of fine motor control in the contralesional arm and hand and the constraint to a grouped movement pattern known as the flexion synergy. In the flexion synergy, increasing shoulder abductor activation drives progressive, involuntary increases in elbow, wrist and finger flexion. The neural mechanisms underlying this phenomenon remain unclear. Here, across 25 adults with moderate to severe hemiparesis following chronic stroke and 18 adults without neurological injury, we test the overall hypothesis that two inter-related mechanisms are necessary for flexion synergy expression: increased task-dependent activation of the intact, contralesional cortex and recruitment of contralesional motor pathways via ipsilateral reticulospinal projections. First, we imaged brain activation in real time during reaching motions progressively constrained by flexion synergy expression. Using this approach, we found that cortical activity indeed shifts towards the contralesional hemisphere in direct proportion to the degree of shoulder abduction loading in the contralesional arm. We then leveraged the post-stroke reemergence of a developmental brainstem reflex to show that anatomically diffuse reticulospinal motor pathways are active during synergy expression. We interpret this progressive recruitment of contralesional cortico-reticulospinal pathways as an adaptive strategy that preserves low-level motor control at the cost of fine motor control.ABSTRACTA hallmark of hemiparetic stroke is the loss of fine motor control in the contralesional arm and hand and the constraint to a grouped movement pattern known as the flexion synergy. In the flexion synergy, increasing shoulder abductor activation drives progressive, involuntary increases in elbow, wrist and finger flexion. The neural mechanisms underlying this phenomenon remain unclear. Here, across 25 adults with moderate to severe hemiparesis following chronic stroke and 18 adults without neurological injury, we test the overall hypothesis that two inter-related mechanisms are necessary for flexion synergy expression: increased task-dependent activation of the intact, contralesional cortex and recruitment of contralesional motor pathways via ipsilateral reticulospinal projections. First, we imaged brain activation in real time during reaching motions progressively constrained by flexion synergy expression. Using this approach, we found that cortical activity indeed shifts towards the contralesional hemisphere in direct proportion to the degree of shoulder abduction loading in the contralesional arm. We then leveraged the post-stroke reemergence of a developmental brainstem reflex to show that anatomically diffuse reticulospinal motor pathways are active during synergy expression. We interpret this progressive recruitment of contralesional cortico-reticulospinal pathways as an adaptive strategy that preserves low-level motor control at the cost of fine motor control. A hallmark of hemiparetic stroke is the loss of fine motor control in the contralesional arm and hand and the constraint to a grouped movement pattern known as the flexion synergy. In the flexion synergy, increasing shoulder abductor activation drives progressive, involuntary increases in elbow, wrist and finger flexion. The neural mechanisms underlying this phenomenon remain unclear. Here, across 25 adults with moderate to severe hemiparesis following chronic stroke and 18 adults without neurological injury, we test the overall hypothesis that two inter‐related mechanisms are necessary for flexion synergy expression: increased task‐dependent activation of the intact, contralesional cortex and recruitment of contralesional motor pathways via ipsilateral reticulospinal projections. First, we imaged brain activation in real time during reaching motions progressively constrained by flexion synergy expression. Using this approach, we found that cortical activity indeed shifts towards the contralesional hemisphere in direct proportion to the degree of shoulder abduction loading in the contralesional arm. We then leveraged the post‐stroke reemergence of a developmental brainstem reflex to show that anatomically diffuse reticulospinal motor pathways are active during synergy expression. We interpret this progressive recruitment of contralesional cortico‐reticulospinal pathways as an adaptive strategy that preserves low‐level motor control at the cost of fine motor control. Key points Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy. It has been proposed that flexion synergy expression is related to reduced output from ipsilesional motor cortex and corticospinal pathways. In this human subjects study, we provide evidence that the magnitude of flexion synergy expression is instead related to a progressive, task‐dependent recruitment of contralesional cortex. We also provide evidence that recruitment of contralesional cortex may induce excessive activation of ipsilateral reticulospinal descending motor pathways that cannot produce discrete movements, leading to flexion synergy expression. We interpret these findings as an adaptive strategy that preserves low‐level motor control at the cost of fine motor control. A hallmark of hemiparetic stroke is the loss of fine motor control in the contralesional arm and hand and the constraint to a grouped movement pattern known as the flexion synergy. In the flexion synergy, increasing shoulder abductor activation drives progressive, involuntary increases in elbow, wrist and finger flexion. The neural mechanisms underlying this phenomenon remain unclear. Here, across 25 adults with moderate to severe hemiparesis following chronic stroke and 18 adults without neurological injury, we test the overall hypothesis that two inter‐related mechanisms are necessary for flexion synergy expression: increased task‐dependent activation of the intact, contralesional cortex and recruitment of contralesional motor pathways via ipsilateral reticulospinal projections. First, we imaged brain activation in real time during reaching motions progressively constrained by flexion synergy expression. Using this approach, we found that cortical activity indeed shifts towards the contralesional hemisphere in direct proportion to the degree of shoulder abduction loading in the contralesional arm. We then leveraged the post‐stroke reemergence of a developmental brainstem reflex to show that anatomically diffuse reticulospinal motor pathways are active during synergy expression. We interpret this progressive recruitment of contralesional cortico‐reticulospinal pathways as an adaptive strategy that preserves low‐level motor control at the cost of fine motor control. Key points Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy. It has been proposed that flexion synergy expression is related to reduced output from ipsilesional motor cortex and corticospinal pathways. In this human subjects study, we provide evidence that the magnitude of flexion synergy expression is instead related to a progressive, task‐dependent recruitment of contralesional cortex. We also provide evidence that recruitment of contralesional cortex may induce excessive activation of ipsilateral reticulospinal descending motor pathways that cannot produce discrete movements, leading to flexion synergy expression. We interpret these findings as an adaptive strategy that preserves low‐level motor control at the cost of fine motor control. Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in the same arm, a phenomenon referred to as the flexion synergy. It has been proposed that flexion synergy expression is related to reduced output from ipsilesional motor cortex and corticospinal pathways. In this human subjects study, we provide evidence that the magnitude of flexion synergy expression is instead related to a progressive, task-dependent recruitment of contralesional cortex. We also provide evidence that recruitment of contralesional cortex may induce excessive activation of ipsilateral reticulospinal descending motor pathways that cannot produce discrete movements, leading to flexion synergy expression. We interpret these findings as an adaptive strategy that preserves low-level motor control at the cost of fine motor control. A hallmark of hemiparetic stroke is the loss of fine motor control in the contralesional arm and hand and the constraint to a grouped movement pattern known as the flexion synergy. In the flexion synergy, increasing shoulder abductor activation drives progressive, involuntary increases in elbow, wrist and finger flexion. The neural mechanisms underlying this phenomenon remain unclear. Here, across 25 adults with moderate to severe hemiparesis following chronic stroke and 18 adults without neurological injury, we test the overall hypothesis that two inter-related mechanisms are necessary for flexion synergy expression: increased task-dependent activation of the intact, contralesional cortex and recruitment of contralesional motor pathways via ipsilateral reticulospinal projections. First, we imaged brain activation in real time during reaching motions progressively constrained by flexion synergy expression. Using this approach, we found that cortical activity indeed shifts towards the contralesional hemisphere in direct proportion to the degree of shoulder abduction loading in the contralesional arm. We then leveraged the post-stroke reemergence of a developmental brainstem reflex to show that anatomically diffuse reticulospinal motor pathways are active during synergy expression. We interpret this progressive recruitment of contralesional cortico-reticulospinal pathways as an adaptive strategy that preserves low-level motor control at the cost of fine motor control. |
| Author | Dewald, Julius P. A. Yao, Jun Heckman, C. J. McPherson, Jacob G. Chen, Albert Ellis, Michael D. |
| AuthorAffiliation | 3 Feinberg School of Medicine, Department of Physical Medicine and Rehabilitation Northwestern University 345 East Superior Street Chicago IL 60611 USA 2 Department of Biomedical Engineering Florida International University 10555 West Flagler Street, EC 2600 Miami FL 33174 USA 4 Feinberg School of Medicine, Department of Physiology Northwestern University 303 East Chicago Ave, M211 Chicago IL 60611 USA 5 McCormick School of Engineering, Department of Biomedical Engineering Northwestern University 2145 Sheridan Road Evanston IL 60208 USA 1 Feinberg School of Medicine Department of Physical Therapy and Human Movement Sciences Northwestern University 645 N Michigan Ave, Suite 1100 Chicago IL 60611 USA |
| AuthorAffiliation_xml | – name: 4 Feinberg School of Medicine, Department of Physiology Northwestern University 303 East Chicago Ave, M211 Chicago IL 60611 USA – name: 1 Feinberg School of Medicine Department of Physical Therapy and Human Movement Sciences Northwestern University 645 N Michigan Ave, Suite 1100 Chicago IL 60611 USA – name: 5 McCormick School of Engineering, Department of Biomedical Engineering Northwestern University 2145 Sheridan Road Evanston IL 60208 USA – name: 3 Feinberg School of Medicine, Department of Physical Medicine and Rehabilitation Northwestern University 345 East Superior Street Chicago IL 60611 USA – name: 2 Department of Biomedical Engineering Florida International University 10555 West Flagler Street, EC 2600 Miami FL 33174 USA |
| Author_xml | – sequence: 1 givenname: Jacob G. orcidid: 0000-0002-4554-7531 surname: McPherson fullname: McPherson, Jacob G. organization: Florida International University – sequence: 2 givenname: Albert surname: Chen fullname: Chen, Albert organization: Northwestern University – sequence: 3 givenname: Michael D. surname: Ellis fullname: Ellis, Michael D. organization: Northwestern University – sequence: 4 givenname: Jun surname: Yao fullname: Yao, Jun organization: Northwestern University – sequence: 5 givenname: C. J. surname: Heckman fullname: Heckman, C. J. organization: Northwestern University – sequence: 6 givenname: Julius P. A. surname: Dewald fullname: Dewald, Julius P. A. email: j-dewald@northwestern.edu organization: Northwestern University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29457651$$D View this record in MEDLINE/PubMed |
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| Copyright | 2018 Northwestern University. The Journal of Physiology © 2018 The Physiological Society 2018 Northwestern University. The Journal of Physiology © 2018 The Physiological Society. Journal compilation © 2018 The Physiological Society |
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| Issue | 7 |
| Keywords | neural plasticity motor control stroke |
| Language | English |
| License | http://onlinelibrary.wiley.com/termsAndConditions#vor 2018 Northwestern University. The Journal of Physiology © 2018 The Physiological Society. |
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| Notes | Edited by: Janet Taylor & Richard Carson J. G. McPherson and A. Chen contributed equally to this work. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
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Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger... Activation of the shoulder abductor muscles in the arm opposite a unilateral brain injury causes involuntary increases in elbow, wrist and finger flexion in... A hallmark of hemiparetic stroke is the loss of fine motor control in the contralesional arm and hand and the constraint to a grouped movement pattern known as... |
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| SubjectTerms | Adult Aged Aged, 80 and over Arm Brain stem Elbow Female Humans Male Middle Aged Molecular and Cellular motor control Motor Cortex - pathology Motor task performance Muscle Weakness neural plasticity Paresis Paresis - etiology Paresis - pathology Pyramidal Tracts - pathology Recruitment Reflex Research Paper Reticular Formation - pathology Shoulder Spinal Cord - pathology Stroke Stroke - complications Wrist |
| Title | Progressive recruitment of contralesional cortico‐reticulospinal pathways drives motor impairment post stroke |
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