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Inhibition versus facilitation of contralesional motor cortices in stroke: Deriving a model to tailor brain stimulation
Vishwanath Sankarasubramanian a,
Andre G. Machado b,
Adriana B. Conforto c,d,
Kelsey A. Potter-Baker a,
David A. Cunningham a,e,
Nicole M. Varnerin a,
Xiaofeng Wang f,
Ken Sakaie g,
Ela B. Plow a,b,h,
a Department of Biomedical Engineering, Lerner Research Institute, Cleveland Clinic, Cleveland, OH 44195, USA
b Center for Neurological Restoration, Neurological Institute, Cleveland Clinic, Cleveland, OH 44195, USA
c Neurology Clinical Division, Neurology Department, Hospital das Clinicas, São Paulo University, 05508-090 São Paulo, SP, Brazil
d Hospital Israelita Albert Einstein, 05652-900 São Paulo, SP, Brazil
e School of Biomedical Sciences, Kent State University, Kent, OH 44242, USA
f Department of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic, Cleveland, OH 44195, USA
g Department of Diagnostic Radiology, Imaging Institute, Cleveland Clinic, Cleveland, OH 44195, USA
h Department of Physical Medicine and Rehabilitation, Neurological Institute, Cleveland Clinic, Cleveland, OH 44195, USA
a r t i c l e i n f o
Article history:
Accepted 14 March 2017Available online 21 March 2017
Keywords:
Diffusion tensor imagingMotor cortexPremotor cortexNeuronal plasticityRehabilitationStrokeTranscranial magnetic stimulation
h i g h l i g h t s
Mildly affected chronic stroke patients improved upon paretic upper limb reaching with standardinhibitory 1Hz rTMS of contralesional motor cortex.
Severely affected patients improved with a new method involving facilitatory 5Hz rTMS of contrale-sional dorsal premotor cortex.
A preliminary cut-off level of damage/impairment separated responders to each form of stimulation.
The standard approach to brain stimulation in stroke is based on the premise that ipsilesionalM1(iM1)is important for motor function of the paretic upper limb, while contralesional cortices compete with iM1. Therefore, the approach typically advocates facilitating iM1 and/or inhibiting contralesionalM1 (cM1). But, this approach fails to elicit much improvement in severely affected patients, who on account of extensive damage to ipsilesional pathways, cannot rely on iM1. These patients are believed to instead rely on the undamaged cortices, especially the contralesional dorsal premotor cortex(cPMd), for support of function of the paretic limb. Here, we tested for the first time whether facilitation of cPMd could improve paretic limb function in severely affected patients, and if a cut-off could be identified to separate responders to cPMd from responders to the standard approach to stimulation.
Methods:
In a randomized, sham-controlled crossover study, fifteen patients received the standard approach of stimulation involving inhibition of cM1 and a new approach involving facilitation of cPMdusing repetitive transcranial magnetic stimulation (rTMS). Patients also received rTMS to control areas.At baseline, impairment [Upper Extremity Fugl-Meyer (UEFM PROXIMAL, max=36)] and damage to path-ways [fractional anisotropy (FA)] was measured. We measured changes in time to perform proximal paretic limb reaching, and neurophysiology using TMS.
Results:
Facilitation of cPMd generated more improvement in severely affected patients, who had expe-rienced greater damage and impairment than a cut-off value of FA (0.5) and UEFM PROXIMAL
(26–28). The standard approach instead generated more improvement in mildly affected patients. Responders to cPMd showed alleviation of interhemispheric competition imposed on iM1, while responders to the standard approach showed gains in ipsilesional excitability in association with improvement.
Conclusions:
a Department of Biomedical Engineering, Lerner Research Institute, Cleveland Clinic, Cleveland, OH 44195, USA
b Center for Neurological Restoration, Neurological Institute, Cleveland Clinic, Cleveland, OH 44195, USA
c Neurology Clinical Division, Neurology Department, Hospital das Clinicas, São Paulo University, 05508-090 São Paulo, SP, Brazil
d Hospital Israelita Albert Einstein, 05652-900 São Paulo, SP, Brazil
e School of Biomedical Sciences, Kent State University, Kent, OH 44242, USA
f Department of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic, Cleveland, OH 44195, USA
g Department of Diagnostic Radiology, Imaging Institute, Cleveland Clinic, Cleveland, OH 44195, USA
h Department of Physical Medicine and Rehabilitation, Neurological Institute, Cleveland Clinic, Cleveland, OH 44195, USA
a r t i c l e i n f o
Article history:
Accepted 14 March 2017Available online 21 March 2017
Keywords:
Diffusion tensor imagingMotor cortexPremotor cortexNeuronal plasticityRehabilitationStrokeTranscranial magnetic stimulation
h i g h l i g h t s
Mildly affected chronic stroke patients improved upon paretic upper limb reaching with standardinhibitory 1Hz rTMS of contralesional motor cortex.
Severely affected patients improved with a new method involving facilitatory 5Hz rTMS of contrale-sional dorsal premotor cortex.
A preliminary cut-off level of damage/impairment separated responders to each form of stimulation.
a b s t r a c t
Objective:The standard approach to brain stimulation in stroke is based on the premise that ipsilesionalM1(iM1)is important for motor function of the paretic upper limb, while contralesional cortices compete with iM1. Therefore, the approach typically advocates facilitating iM1 and/or inhibiting contralesionalM1 (cM1). But, this approach fails to elicit much improvement in severely affected patients, who on account of extensive damage to ipsilesional pathways, cannot rely on iM1. These patients are believed to instead rely on the undamaged cortices, especially the contralesional dorsal premotor cortex(cPMd), for support of function of the paretic limb. Here, we tested for the first time whether facilitation of cPMd could improve paretic limb function in severely affected patients, and if a cut-off could be identified to separate responders to cPMd from responders to the standard approach to stimulation.
Methods:
In a randomized, sham-controlled crossover study, fifteen patients received the standard approach of stimulation involving inhibition of cM1 and a new approach involving facilitation of cPMdusing repetitive transcranial magnetic stimulation (rTMS). Patients also received rTMS to control areas.At baseline, impairment [Upper Extremity Fugl-Meyer (UEFM PROXIMAL, max=36)] and damage to path-ways [fractional anisotropy (FA)] was measured. We measured changes in time to perform proximal paretic limb reaching, and neurophysiology using TMS.
Results:
Facilitation of cPMd generated more improvement in severely affected patients, who had expe-rienced greater damage and impairment than a cut-off value of FA (0.5) and UEFM PROXIMAL
(26–28). The standard approach instead generated more improvement in mildly affected patients. Responders to cPMd showed alleviation of interhemispheric competition imposed on iM1, while responders to the standard approach showed gains in ipsilesional excitability in association with improvement.
Conclusions:
A preliminary cut-off level of severity separated responders for standard approach vs. facilitation of cPMd
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