Cortical beta oscillations and motor thresholds differ across the spectrum of post-stroke motor impairment, a preliminary MEG and TMS study

Shiner, Christine T.; Tang, Hua; Johnson, Blake W.; McNulty, Penelope A.

doi:10.1016/j.brainres.2015.09.037

Cited by 46 publications

(54 citation statements)

References 74 publications

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“…The strength of the beta rhythm rebound after sensory stimulation and passive movements of the affected hand is related to motor impairment and recovery therefrom. During active movements of the affected hand, a smaller beta desynchronization in contralateral M1 has consistently been found in chronic stroke patients that is related to the degree of impairment . Our longitudinal recordings demonstrate that this reduced level of movement‐related beta desynchronization is already present at the acute stage.…”

Section: Discussionsupporting

confidence: 72%

“…During active movements of the affected hand, a smaller beta desynchronization in contralateral M1 has consistently been found in chronic stroke patients that is related to the degree of impairment. 23,29,49,50 Our longitudinal recordings demonstrate that this reduced level of movement-related beta desynchronization is already present at the acute stage. This indicates that reduced beta modulation is not the result of poststroke plasticity but likely contingent on altered homeostasis between excitatory and inhibitory circuits already early after stroke.…”

Section: Diminishment Of Movement-related Lfos In Stroke Pathophysiologymentioning

confidence: 55%

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Low‐Frequency Brain Oscillations Track Motor Recovery in Human Stroke

Bönstrup

Krawinkel

Schulz

et al. 2019

Annals of Neurology

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Objective The majority of patients with stroke survive the acute episode and live with enduring disability. Effective therapies to support recovery of motor function after stroke are yet to be developed. Key to this development is the identification of neurophysiologic signals that mark recovery and are suitable and susceptible to interventional therapies. Movement preparatory low‐frequency oscillations (LFOs) play a key role in cortical control of movement. Recent animal data point to a mechanistic role of motor cortical LFOs in stroke motor deficits and demonstrate neuromodulation intervention with therapeutic benefit. Their relevance in human stroke pathophysiology is unknown. Methods We studied the relationship between movement‐preparatory LFOs during the performance of a visuomotor grip task and motor function in a longitudinal (<5 days, 1 and 3 months) cohort study of 33 patients with motor stroke and in 19 healthy volunteers. Results Acute stroke–lesioned brains fail to generate the LFO signal. Whereas in healthy humans, a transient occurrence of LFOs preceded movement onset at predominantly contralateral frontoparietal motor regions, recordings in patients revealed that movement‐preparatory LFOs were substantially diminished to a level of 38% after acute stroke. LFOs progressively increased at 1 and 3 months. This re‐emergence closely tracked the recovery of motor function across several movement qualities including grip strength, fine motor skills, and synergies and was frequency band specific. Interpretation Our results provide the first human evidence for a link between movement‐preparatory LFOs and functional recovery after stroke, promoting their relevance for movement control. These results suggest that it may be interesting to explore targeted, LFOs‐restorative brain stimulation therapy in human stroke patients. ANN NEUROL 2019;86:853–865

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Section: Discussionsupporting

confidence: 72%

Section: Diminishment Of Movement-related Lfos In Stroke Pathophysiologymentioning

confidence: 55%

Low‐Frequency Brain Oscillations Track Motor Recovery in Human Stroke

Bönstrup

Krawinkel

Schulz

et al. 2019

Annals of Neurology

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“…We propose that, on an individual level, the primary motor cortices may have an absolute threshold of beta power that must be reached in order to adequately execute a movement, and that an inability to reduce beta power to this threshold results in an increase in movement duration. Recent MEG studies of movement disorders such as cerebral palsy (Kurz et al, 2014), Parkinson’s disease (Heinrichs-Graham et al, 2014b; Pollok et al, 2012), and stroke (Rossiter et al, 2014a; Shiner et al, 2015; Wilson et al, 2011a) have demonstrated aberrant movement-related beta oscillatory activity within these populations. Future work should examine the relationship between resting beta activity and movement-related beta oscillations in the context of these movement disorders.…”

Section: Discussionmentioning

confidence: 99%

“…Further, a multitude of studies examining the neurophysiology of movement disorders, such as Parkinson’s disease (Brown, 2007; Cassidy et al, 2002; Heinrichs-Graham et al, 2014a; Heinrichs-Graham et al, 2014b; Little and Brown, 2014; Pollok et al, 2012; Weinberger et al, 2006), cerebral palsy (Kurz et al, 2014), Tourette syndrome (Franzkowiak et al, 2010; Niccolai et al, 2015; Tinaz et al, 2014), dystonia (Hinkley et al, 2012), and stroke (Rossiter et al, 2014a; Shiner et al, 2015; Wilson et al, 2011a) have shown aberrant sensorimotor beta power at rest and/or during movement. These beta aberrations are often correlated with symptom severity, which suggests that the degree of motor impairment is closely tied to beta activity in the motor cortices.…”

Section: Introductionmentioning

confidence: 99%

Is an absolute level of cortical beta suppression required for proper movement? Magnetoencephalographic evidence from healthy aging

2016

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Previous research has connected a specific pattern of beta oscillatory activity to proper motor execution, but no study to date has directly examined how resting beta levels affect motor-related beta oscillatory activity in the motor cortex. Understanding this relationship is imperative to determining the basic mechanisms of motor control, as well as the impact of pathological beta oscillations on movement execution. In the current study, we used magnetoencephalography (MEG) and a complex movement paradigm to quantify resting beta activity and movement-related beta oscillations in the context of healthy aging. We chose healthy aging as a model because preliminary evidence suggests that beta activity is elevated in older adults, and thus by examining older and younger adults we were able to naturally vary resting beta levels. To this end, healthy younger and older participants were recorded during motor performance and at rest. Using beamforming, we imaged the peri-movement beta event-related desynchronization (ERD) and extracted virtual sensors from the peak voxels, which enabled absolute and relative beta power to be assessed. Interestingly, absolute beta power during the pre-movement baseline was much stronger in older relative to younger adults, and older adults also exhibited proportionally large beta desynchronization (ERD) responses during motor planning and execution compared to younger adults. Crucially, we found a significant relationship between spontaneous (resting) beta power and beta ERD magnitude in both primary motor cortices, above and beyond the effects of age. A similar link was found between beta ERD magnitude and movement duration. These findings suggest a direct linkage between beta reduction during movement and spontaneous activity in the motor cortex, such that as spontaneous beta power increases, a greater reduction in beta activity is required to execute movement. We propose that, on an individual level, the primary motor cortices have an absolute threshold of beta power that must be reached in order to move, and that an inability to suppress beta power to this threshold results in an increase in movement duration.

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“…In the recovery of motor function following stroke, for example, the duration of movement-induced beta-desynchronization and post-movement synchronization were correlated with the patients’ motor function scores (Shiner et al 2015), indicating that the temporal dimension provided by EEG contributes to the understanding of motor recovery. Similarly, neuroplasticity indexed by spectral and evoked potential changes in working memory and attention has been observed after strokes in lateral frontal cortex (Voytek et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Neuroplasticity of language in left‐hemisphere stroke: Evidence linking subsecond electrophysiology and structural connections

Piai

Meyer

Dronkers

et al. 2017

Human Brain Mapping

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Our understanding of neuroplasticity following stroke is predominantly based on neuroimaging measures that cannot address the subsecond neurodynamics of impaired language processing. We combined behavioral and electrophysiological measures and structural-connectivity estimates to characterize neuroplasticity underlying successful compensation of language abilities after left-hemispheric stroke. We recorded the electroencephalogram from patients with stroke lesions to the left temporal lobe and matched controls during context-driven word retrieval. Participants heard lead-in sentences that either constrained the final word (“He locked the door with the”) or not (“She walked in here with the”). The last word was shown as a picture to be named. We conducted individual-participant analyses and focused on oscillatory power as a subsecond indicator of a brain region’s functional neurophysiological computations. All participants named pictures faster following constrained than unconstrained sentences, except for two patients, who had extensive damage to the left temporal lobe. Left-lateralized alpha-beta oscillatory power decreased in controls pre-picture presentation for constrained relative to unconstrained contexts. In patients, the alpha-beta power decreases were observed with the same time course as in controls but were lateralized to the intact right hemisphere. The right lateralization depended on the probability of white-matter connections between the bilateral temporal lobes. The two patients who performed poorly behaviorally showed no alpha-beta power decreases. Our findings suggest that incorporating direct measures of neural activity into investigations of neuroplasticity can provide important neural markers to help predict language recovery, assess the progress of neurorehabilitation, and delineate targets for therapeutic neuromodulation.

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Cortical beta oscillations and motor thresholds differ across the spectrum of post-stroke motor impairment, a preliminary MEG and TMS study

Cited by 46 publications

References 74 publications

Low‐Frequency Brain Oscillations Track Motor Recovery in Human Stroke

Low‐Frequency Brain Oscillations Track Motor Recovery in Human Stroke

Is an absolute level of cortical beta suppression required for proper movement? Magnetoencephalographic evidence from healthy aging

Neuroplasticity of language in left‐hemisphere stroke: Evidence linking subsecond electrophysiology and structural connections

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