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Altered Corticomuscular Coherence (CMCoh) Pattern in the Upper Limb During Finger Movements After Stroke
Ziqi Guo
Qiuyang Qian
Kiufung Wong
Hanlin Zhu
Yanhuan Huang
Xiaoling Hu
Yongping Zheng- Department of Biomedical Engineering, The Hong Kong Polytechnic University, Kowloon, Hong Kong
Background:
Proximal compensation to
the distal movements is commonly observed in the affected upper
extremity (UE) of patients with chronic stroke. However, the cortical
origin of this compensation has not been well-understood. In this study,
corticomuscular coherence (CMCoh) and electromyography (EMG) analysis
were adopted to investigate the corticomuscular coordinating pattern of
proximal UE compensatory activities when conducting distal UE movements
in chronic stroke.
Method:
Fourteen chronic stroke
subjects and 10 age-matched unimpaired controls conducted isometric
finger extensions and flexions at 20 and 40% of maximal voluntary
contractions. Electroencephalogram (EEG) data were recorded from the
sensorimotor area and EMG signals were captured from extensor digitorum
(ED), flexor digitorum (FD), triceps brachii (TRI), and biceps brachii
(BIC) to investigate the CMCoh peak values in the Beta band. EMG
parameters, i.e., the EMG activation level and co-contraction index
(CI), were analyzed to evaluate the compensatory muscular patterns in
the upper limb.
Result:
The peak CMCoh with statistical significance (P
< 0.05) was found shifted from the ipsilesional side to the
contralesional side in the proximal UE muscles, while to the central
regions in the distal UE muscle in chronic strokes. Significant
differences (P < 0.05) were observed in both peak ED and FD
CMCohs during finger extensions between the two groups. The unimpaired
controls exhibited significant intragroup differences between 20 and 40%
levels in extensions for peak ED and FD CMCohs (P < 0.05). The stroke subjects showed significant differences in peak TRI and BIC CMCohs (P
< 0.01). No significant inter- or intra-group difference was
observed in peak CMCoh during finger flexions. EMG parameters showed
higher EMG activation levels in TRI and BIC muscles (P <
0.05), and higher CI values in the muscle pairs involving TRI and BIC
during all the extension and flexion tasks in the stroke group than
those in the control group (P < 0.05).
Conclusion:
The post-stroke proximal
muscular compensations from the elbow to the finger movements were
cortically originated, with the center mainly located in the
contralesional hemisphere.
Introduction
Post-stroke motor recovery is usually associated with the cortical reorganization and adaptive learning experiences (1).
Cerebral plasticity is the process by which the human body reorganizes
neural networks and pathways after a stroke. Existing studies have found
that the majority of motor recovery observed via cerebral plasticity
reaches a plateau within the first 6 months after the onset (2, 3).
Patients with chronic stroke (first onset over 6 months) regain the
independence of the activities of daily living but always sustain upper
extremity (UE) motor dysfunctions, e.g., muscle weakness, spasticity,
and discoordination (4).
Specifically, patients' distal UE segments, e.g., fingers and wrist,
usually exhibit poorer functional recovery than the proximal elbow and
shoulder parts (5). In our previous study (6, 7),
we found that the dyscoordination observed following chronic stroke was
particularly evident during distal UE joint motion tasks, and that
stroke patients frequently relied on compensatory contractions from
proximal UE muscles to substitute for a loss or reduction in hand
function. However, Jones concluded that proximal compensations can be
mistaken for recovery and constrain the potential motor restoration at
the distal segments, leading to “learned non-use” or “learned dis-use” (8).
Although such post-stroke behavioral deviation can further exacerbate
motor impairments, the interaction between the cortical plasticity in
chronic stroke and the dynamic muscular coordination in the upper limb
has not yet been well-investigated.
Previous neuroimaging studies on motor restoration after
stroke using positron emission tomography (PET), functional magnetic
resonance (fMRI) imaging, and transcranial magnetic stimulation (TMS)
have identified that post-stroke patients exhibit a reduction in brain
activities at the lesioned side and a propensity to recruit the
contralesional motor cortex when conducting tasks involving the arms (9–11).
However, these methods were limited by the low temporal resolutions to
reveal the transient relationship between the cortical and muscular
dynamics in the investigation of the post-stroke compensatory mechanism
to activate proximal muscle contractions in compensation for distal
movements in the upper limb.
Electroencephalogram (EEG) and electromyogram (EMG) can
capture faster dynamics in the cortex and peripheral muscles,
respectively, comparing with the imaging techniques mentioned above.
Furthermore, previous studies have found that the coherence between the
two parameters can result in the demonstration of time-based functional
connections in the neuromuscular pathways when subjects perform specific
motion tasks (12, 13).
This also makes it possible to identify the location of cortical
sources and trace the neuroplasticity after stroke according to the
coherence topography (14). The coherence between EEG and EMG was first described by Salenius et al. (15) and Gerloff et al. (16),
who referred to it as corticomuscular coherence (CMCoh) to reflect
voluntary descending control from the primary motor cortex to the
effector muscles. Coherence can be calculated using both EEG and EMG
signals, and it is typically observed within the frequency range of
13–30 Hz (Beta band) during the execution of steady-state isometric
contraction and phasic movements (17).
The maximum value (i.e., the peak CMCoh) denotes the most significant
neuromuscular coupling of the coherent activities and location of the
central generator over the whole motor cortex (18, 19). Mima et al. (20)
first reported the topographical shift of CMCoh from the lesional side
to the contralesional side observed among chronic stroke patients, which
may be due to the contribution of lateral and/or medial premotor area
control made to the muscles, as suggested by previous PET and
electrocorticographic studies (21–23).
Furthermore, the neuromuscular coupling between cortical commands and
consequent muscle activities indicated by CMCoh values is usually not
evident immediately after a stroke; rather, it seems to increase
throughout the course of the recovery process gradually. Fang et al. (24) and Larsen et al. (25)
reported that the CMCoh values in patients with acute and subacute
stroke were weaker than those observed in unimpaired controls, while
Chen and colleagues (26)
found patients with chronic stroke demonstrated higher CMCoh values
from the UE flexors than those in a control group. These studies have
consistently indicated that data pertaining to the intensity and
location of peak coherence could be employed to estimate the muscle
representation areas after neural reorganization following stroke.
However, most of the CMCoh studies on stroke patients to date
investigating the cerebral-derived control on distal UE segments have
been limited to EMG recording from distal muscles, e.g., the extensor
carpi radialis muscle (19) or its antagonist muscle flexor carpi radialis (27)
in wrist extension at the affected side. Rare studies have employed
CMCoh to investigate the contractions of proximal muscles to compensate
for distal motions, which could be traced back to a cortical-originated
alteration in muscular discoordination at the peripheral.
The purpose of this study was to investigate the
corticomuscular coordination pattern in the upper limb muscles during
distal finger movements at the affected side of patients with chronic
stroke, via a combination of EEG and EMG measurements.
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