Elsevier

Clinical Neurophysiology

Volume 128, Issue 11, November 2017, Pages 2217-2226
Clinical Neurophysiology

Corticomuscular coherence in the acute and subacute phase after stroke

https://doi.org/10.1016/j.clinph.2017.08.033Get rights and content

Highlights

  • Corticomuscular coherence (CMC) and intermuscular coherence (IMC) were reduced in acute and subacute stroke compared to healthy controls.

  • CMC was localized above the contralateral sensorimotor cortex in both patients and controls.

  • Improvement of hand motor performance did not require changes in CMC or IMC.

Abstract

Objective

Stroke is one of the leading causes of physical disability due to damage of the motor cortex or the corticospinal tract. In the present study we set out to investigate the role of adaptations in the corticospinal pathway for motor recovery during the subacute phase after stroke.

Methods

We examined 19 patients with clinically diagnosed stroke and 18 controls. The patients had unilateral mild to moderate weakness of the hand. Each patient attended two sessions at approximately 3 days (acute) and 38 days post stroke (subacute). Task-related changes in the communication between motor cortex and muscles were evaluated from coupling in the frequency domain between EEG and EMG during movement of the paretic hand.

Results

Corticomuscular coherence (CMC) and intermuscular coherence (IMC) were reduced in patients as compared to controls. Paretic hand motor performance improved within 4–6 weeks after stroke, but no change was observed in CMC or IMC.

Conclusions

CMC and IMC were reduced in patients in the early phase after stroke. However, changes in coherence do not appear to be an efficient marker for early recovery of hand function following stroke.

Significance

This is the first study to demonstrate sustained reduced coherence in acute and subacute stroke.

Introduction

Stroke results from critically reduced blood flow to the brain tissue due to bleeding or obstruction of arteries. Globally, stroke remains a major cause of disability despite advances in preventive treatment and in acute management (Hankey, 2017). The most common impairment caused by stroke is motor disability affecting approximately 80% of the patients, most frequently seen as hemiparesis (Langhorne et al., 2009). Spontaneous recovery may occur in the following weeks and months after stroke and can be facilitated through rehabilitation involving exercise (Maulden et al., 2005). Despite of this, upper limb motor impairments are often persistent and disabling (Lai et al., 2002) and no rehabilitation program has been proven superior to other programs (Pollock et al., 2014). Strategies aiming at enhancing rehabilitation programs require a greater understanding of the mechanisms of recovery. In the present study we set out to investigate the role of adaptations in the corticospinal tract (CST) for motor recovery of the affected hand during the subacute phase after stroke.

Studies performed in monkeys have demonstrated severe deficits in precise finger movements following selective lesion to the CST (Lawrence and Kuypers, 1968) and diffusion-tensor imaging studies have consistently shown a relation between damaged CST fibres and motor deficits (Stinear et al., 2007, Schulz et al., 2012). In primates most of the neurons in the CST originate in the primary motor cortex (M1) and a subset of these makes direct, cortico-motoneuronal connections with spinal motoneurons especially towards distal finger muscles (Porter and Lemon, 1993). Evidence suggest that these direct connections play a key role in fractionated finger movements, which are important for manipulation of small objects (Lemon et al., 2004). It is believed that the direct connections work in parallel with the more indirect connections by adding the final spatiotemporal excitation patterns in order to produce appropriate levels of motoneuronal recruitment and discharge (Lemon et al., 2004). Disconnection of direct and indirect connections in the CST is assumed to be a major cause of impaired hand and finger motor function after stroke (Lemon, 2008).

Estimates of task-related corticospinal connections can be noninvasively determined during finger movements from coherence analysis in human subjects. This measurement allows a statistical analysis to be performed to characterize the functional coupling in the frequency domain (coherence) between cortical oscillatory activity (measured by EEG) and motor activity (measured by EMG) during a task (Halliday et al., 1995). I addition, coherence analysis of surface EMG within and between muscles provides a complementary means of measuring and detecting changes in the CST (Grosse et al., 2002). Previously cross-sectional studies have demonstrated that corticomuscular coherence (CMC) is reduced in the chronic phase after stroke (Mima et al., 2001, Braun et al., 2007, Fang et al., 2009, Rossiter et al., 2013) and furthermore that CMC can increase in the chronic phase after training (Belardinelli et al., 2017), with peripheral electrical stimulation (Lai et al., 2016) and with time (von Carlowitz-Ghori et al., 2014). However the adaptations in the CST during the first 4–6 weeks post-stroke, where the most dramatic improvements occur, have not been investigated. We hypothesized that CMC will be reduced in stroke patients and will increase in parallel to the stroke patient’s improvement in functional performance during early recovery.

Section snippets

Participants

We examined 19 patients (mean age 61 years, range 31–86 years, 2 females, 1 left-handed) with clinically diagnosed stroke and 18 control participants with no history of stroke (mean age 65 years, range 33–88 years, 5 females, 0 left-handed). The stroke patients had unilateral mild to moderate motor weakness of the hand (7 dominant hand affected). We excluded patients with hemorrhagic stroke, those unable to perform the pinch grip task and those with language/cognitive deficits sufficient to impair

Results

Nineteen patients were recruited for this study. Four patients were excluded for statistical analysis: One due to an error in hardware settings, one who could not co-operate to the dynamic pinch task and two patients had a medical history of previous stroke. Baseline characteristics for the 15 remaining patients are shown in Table 1. Two patients cancelled their second recording day due to psychological and physiological tiredness caused by the stroke.

From T1 to T2 patients improved their MVC

Discussion

In this study, simultaneous EEG and EMG recordings were obtained from cortex and affected finger muscles during an isometric pinch grip to investigate the task-related coupling in the early phase after stroke. The results provide evidence that both CMC and IMC are reduced in the acute phase after stroke with no significant change within the following 4–6 weeks despite improved behavioral performance in the dynamic pinch task, MVC and pegboard score.

CMC is a marker of the corticospinal pathway

Conclusion

To our knowledge this is the first study to investigate CMC and IMC during the early recovery phase after stroke. The distribution of significant CMC above the contralateral (ipsilesional) sensorimotor cortex was similar to the distribution of control participants but the amount of both CMC and IMC was persistently reduced and CMC occurred at somewhat lower frequencies after stroke. No significant correlation was found between the amount of coherence and the level of functional recovery.

Acknowledgements

The study was supported by the research program “Physical activity and nutrition for improvement of health” funded by the University of Copenhagen Excellence Programme for Interdisciplinary Research.

Conflict of interest

None of the authors have potential conflicts of interest to be disclosed.

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