Relationship between resting-state functional connectivity and change in motor function after motor imagery intervention in patients with stroke: a scoping review

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Relationship between resting-state functional connectivity and change in motor function after motor imagery intervention in patients with stroke: a scoping review

• Kenya Tanamachi,
• Wataru Kuwahara,
• Megumi Okawada,
• Shun Sasaki &
• Fuminari Kaneko 

Journal of NeuroEngineering and Rehabilitation volume 20, Article number: 159 (2023) Cite this article

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Abstract

Background

In clinical practice, motor imagery has been proposed as a treatment modality for stroke owing to its feasibility in patients with severe motor impairment. Motor imagery-based interventions can be categorized as open- or closed-loop. Closed-loop intervention is based on voluntary motor imagery and induced peripheral sensory afferent (e.g., Brain Computer Interface (BCI)-based interventions). Meanwhile, open-loop interventions include methods without voluntary motor imagery or sensory afferent. Resting-state functional connectivity (rs-FC) is defined as a significant temporal correlated signal among functionally related brain regions without any stimulus. rs-FC is a powerful tool for exploring the baseline characteristics of brain connectivity. Previous studies reported changes in rs-FC after motor imagery interventions. Systematic reviews also reported the effects of motor imagery-based interventions at the behavioral level. This study aimed to review and describe the relationship between the improvement in motor function and changes in rs-FC after motor imagery in patients with stroke.

Review process

The literature review was based on Arksey and O’Malley’s framework. PubMed, Ovid MEDLINE, Cochrane Central Register of Controlled Trials, and Web of Science were searched up to September 30, 2023. The included studies covered the following topics: illusion without voluntary action, motor imagery, action imitation, and BCI-based interventions. The correlation between rs-FC and motor function before and after the intervention was analyzed. After screening by two independent researchers, 13 studies on BCI-based intervention, motor imagery intervention, and kinesthetic illusion induced by visual stimulation therapy were included.

Conclusion

All studies relating to motor imagery in this review reported improvement in motor function post-intervention. Furthermore, all those studies demonstrated a significant relationship between the change in motor function and rs-FC (e.g., sensorimotor network and parietal cortex).

Background

Stroke is one of the most prevalent neurological diseases worldwide. Importantly, it induces motor dysfunction and hinders the performance of activities of daily living. Up to 85% of survivors experience hemiparesis immediately after the stroke, resulting in impaired upper extremity function. In addition, 55 to 75% of survivors continue to experience limitations in upper extremity function, even at 3–6 months after the event, further leading to a decline in health-related quality of life [1, 2].

Motor imagery involves as the mental presentation of an action without voluntary body movement [3]. The physiological effect was first represented as the regional cerebral blood flow during rest and planning of voluntary movement reported by Roland et al. [4] They reported that motor imagery activates central sites involved in normal voluntary movements. After more than 10 years, Yahagi and Kasai reported that the primary motor cortex excitability increased during motor imagery without gain modulation in the spinal reflex, using transcranial magnetic stimulation (TMS) [5, 6]. After their reports using TMS, a number of studies concerning the physiological effects of motor imagery have since reported [7,8,9,10]. In 2011, Aoyama demonstrated that the facilitatory effect depends on the voluntary effort level of the motor image in the soleus muscle without a change in H-reflex gain [11]. We previously demonstrated the negative effect of sustained rest during joint immobilization on facilitatory function of motor imagery [12]. In that research, we demonstrated that the facilitation effect in which the motor evoked potentials (MEP) during motor imagery was suppressed after immobilization along parallel with decreased muscular output. Furthermore, when the voluntary muscular activity level recovered to that of before the immobilization, MEP was restored to the normal level. These previous findings of the physiological effects indicate the potential use of motor imagery as a clinical treatment, including in stroke. Systematic reviews reported the effects of motor imagery for corticomotoneuronal excitability. In 2019, Dilena et al. [13] indicated that the excitability of the corticomotoneuronal system was enhanced by the kinesthetic illusion, which was induced through visual and tendon vibration.

An advantage of motor imagery intervention is that it may be feasible in patients with severely impaired motor function. Zimmermann-Schlatter et al. [14] conducted a systematic review in 2008 on the efficacy of motor imagery intervention in post-stroke rehabilitation. They found that an improvement in motor imagery, as evidenced by the Fugl-Meyer Assessment (FMA), can confer additional benefits to conventional therapy. Biosignal-based brain-computer interface (BCI) hold great potential for the motor rehabilitation of patients with stroke. Systematic reviews and meta-analyses reported the effects of BCI-based interventions. In 2017, Monge-Pereira et al. [15] indicated that BCI may be potentially beneficial in improving motor outcome measures, such as FMA, Action Research Arm Test (ARAT), and Wolf Motor Function Test (WMFT), in patients with stroke. Carvalho et al. [16] also reported in 2019 that BCI-based intervention, in conjunction with physical practice (conventional or robot-assisted therapy), can enhance upper limb functional recovery. BCI-based intervention can categorize as a closed-loop intervention. In closed-loop intervention, voluntary motor imagery is examined through electroencephalography (EEG). The EEG-based BCI system uses this signal to drive exoskeletal robots and induces peripheral sensory afferent. Meanwhile, open-loop intervention involves methods without voluntary effort to reproduce motor imagery and/ or the absence of sensory afferent. Motor imagery interventions have been shown to be effective in improving motor function [17, 18].

Resting-state functional connectivity (rs-FC) is a powerful tool for exploring the baseline characteristics of brain connectivity. rs-FC is a significantly temporal correlated signal between functionally-related brain regions in the absence of any stimulus or task [19]. rs-FC measurable through functional magnetic resonance imaging (fMRI), EEG, and magnetoencephalography (MEG). According to previous studies, the intensity of rs-FC was related to behavioral measures, and repetition of a specific task modified the rs-FC between brain regions closely related to that task after stroke [20,21,22,23].

Previous studies investigating motor imagery intervention reported that the inter-and intra-hemispheric rs-FC differs in patients depending on stroke severity, becoming weak in patients with severe stroke [24]. Patients in the subacute-to-chronic phase after stroke exhibit diminished rs-FC between the primary motor cortex (PMC) of each hemisphere compared to the healthy controls [25]. The index of asymmetry was significantly correlated with motor function deficits, and the rs-FC between postcentral gyrus (S1) and other regions indicated an asymmetrical difference [26], while rs-FC was increased in the ipsilesional (ipsi-) sensorimotor cortex during the neurofeedback intervention [27]. We investigated that relationship between rs-FC and motor function [28]. This study indicated indicate a linear relationship between rs-FC and improvement of motor function. Investigating the relationship between improvements in motor function and changes in rs-FC through motor imagery intervention can provide valuable insights into understanding this relationship. We hypothesized that resting-state brain function coupling underlies the improvement in motor function with motor imagery intervention. However, our hypothesis has not been reviewed. Therefore, the present review aimed to review and describe the status of these studies.

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