Altered brain function during movement programming is linked with motor deficits after stroke: a high temporal resolution study

 I don't see how anything here gets survivors recovered and yes, Steven C. Cramer is a superstar stroke researcher

• Dr. Steven Cramer (22 posts to October 2011)

Altered brain function during movement programming is linked with motor deficits after stroke: a high temporal resolution study

Célia Delcamp^1,2Alexandre Chalard^1,2Ramesh Srinivasan³Steven C. Cramer^1,2*

• ¹Department of Neurology, University of California, Los Angeles, Los Angeles, CA, United States
• ²California Rehabilitation Institute, Los Angeles, CA, United States
• ³Department of Cognitive Sciences, University of California, Irvine, Irvine, CA, United States

Introduction: Stroke leads to motor deficits, requiring rehabilitation therapy that targets mechanisms underlying movement generation. Cortical activity during the planning and execution of motor tasks can be studied using EEG, particularly via the Event Related Desynchronization (ERD). ERD is altered by stroke in a manner that varies with extent of motor deficits. Despite this consensus in the literature, defining precisely the temporality of these alterations during movement preparation and performance may be helpful to better understand motor system pathophysiology and might also inform development of novel therapies that benefit from temporal resolution.

Methods: Patients with chronic hemiparetic post-stroke (n = 27; age 59 ± 14 years) and age-matched healthy right-handed control subjects (n = 23; 59 ± 12 years) were included. They performed a shoulder rotation task following the onset of a stimulus. Cortical activity was recorded using a 256-electrode EEG cap. ERD was calculated in the beta frequency band (15–30 Hz) in ipsilesional sensorimotor cortex, contralateral to movement. The ERD was compared over time between stroke and control subjects using permutation tests. The correlation between upper extremity motor deficits (assessed by the Fugl-Meyer scale) and ERD over time was studied in stroke patients using Spearman and permutation tests.

Results: Patients with stroke showed on average less beta ERD amplitude than control subjects in the time window of −350 to 50 ms relative to movement onset (t(46) = 2.8, p = 0.007, Cohen’s d = 0.31, 95% CI [0.22: 1.40]). Beta-ERD values correlated negatively with the Fugl-Meyer score during the time window −200 to 400 ms relative to movement onset (Spearman’s r = −0.54, p = 0.003, 95% CI [−0.77 to −0.18]).

Discussion: Our results provide new insights into the precise temporal changes of ERD after hemiparetic stroke and the associations they have with motor deficits. After stroke, the average amplitude of cortical activity is reduced as compared to age-matched controls, and the extent of this decrease is correlated with the severity of motor deficits; both were true during motor programming and during motor performance. Understanding how stroke affects the temporal dynamics of cortical preparation and execution of movement paves the way for more precise restorative therapies. Studying the temporal dynamics of the EEG also strengthens the promising interest of ERD as a biomarker of post-stroke motor function.

1 Introduction

Stroke is a leading cause of motor impairment worldwide, with a majority of patients experiencing upper extremity deficits (Rathore et al., 2002). An important direction for stroke rehabilitation targeting these deficits is to understand the mechanisms underlying movement generation. Electroencephalography (EEG) is a non-invasive tool useful for studying and measuring cortical activity during the planning and execution of a motor task by recording the associated electrical activity of the brain. Analysis of EEG data thereby allows for characterization of pathological patterns of cortical activation during movement by patients with stroke.

In humans, the initiation of a motor task is preceded within 500 ms by a slow decrease in EEG amplitude measured over the primary motor cortex. These potentials are known as motor related cortical potentials (MRCP) (Shakeel et al., 2015). MRCP are a consistent across a range of motor behaviors, e.g., being present during self-paced and cued movements (Shibasaki and Hallett, 2006).

Spectral modulations of cortical oscillations in the beta frequency band (13–30 Hz), such as beta event-related desynchronization (ERD), are particularly relevant to motor function and behavior. Cortical oscillations in the beta frequency band over the sensorimotor cortex are heavily involved in motor control. They are present at rest and decrease slightly before, then further during, a movement, and this decrease in beta power defines an ERD (Pfurtscheller and Lopes da Silva, 1999; Pfurtscheller, 2001). This ERD corresponds to increased corticospinal excitability and in most settings is interpreted as an electrophysiological correlate of cortical activations involved in the generation of movement (Takemi et al., 2013a,b). During the execution of a movement by a paretic limb, patients with stroke show an ERD in ipsilesional sensorimotor cortex, measured using EEG or magnetoencephalography, that has a smaller amplitude compared to that of healthy controls (Platz, 2000; Fu et al., 2006, p. 200; Gerloff et al., 2006; Rossiter et al., 2014; Park et al., 2016; Chalard et al., 2020). Some of these studies have studied movement preparation using a priori assumptions regarding choice of temporal window to study, for example, a window between −750 and −500 ms before movement onset (Platz, 2000) and the first 2 s before movement onset (Fu et al., 2006). Studies of the ERD may also be useful to understand how stroke affects motor system function, as ERD amplitude correlates with degree of motor deficits in the subacute (Bartur et al., 2019; Tang et al., 2020) and chronic phase and is reduced compared to healthy controls (Fu et al., 2006).

Defining, without any a priori assumptions, the exact timepoints during the genesis of movement when beta-ERD is altered by stroke, and is related to motor deficits, may be helpful to understand motor system pathophysiology and might also inform development of novel therapies (Fu et al., 2006; Norman et al., 2018), such as brain-machine interfaces and certain forms of brain stimulation. EEG has excellent temporal resolution and so is useful for understanding how alterations in brain function are related to deficits in motor status. We studied 27 patients with hemiparetic stroke and, as an initial step, confirmed that beta-ERD is reduced as compared to age-matched healthy controls, and that this reduction is proportional to the degree of motor deficits. In the current study, we sought to determine: (1) the time window during which beta-ERD differs between patients and controls, hypothesizing that we would observe a lower ERD amplitude for patients during a discrete epoch before movement and exploring whether this extends to the time period after movement is initiated; and (2) the time window during which the amplitude of beta-ERD is reduced in proportion to motor deficits after stroke, hypothesizing that timepoints when patients had reduced ERD compared to controls would be clinically relevant, i.e., that at timepoints with reduced ERD after stroke, ERD would also correlate with deficits in motor performance. In addition, an exploratory analysis examined functional connectivity, measured as EEG coherence, in relation to stroke and motor deficits, to better understand changes in ERD.

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