Mirror Neuron System to Treat Gait: History
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Subjects: Rehabilitation
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Gait is affected from the early stages of the disease and its worsening runs parallel to the progression of the pathology where three phases could be established. Treatment of gait are focused on medication, brain surgery, and physiotherapy. The more used medication is levodopa, and regarding brain surgery, deep brain stimulation (DBS) in the subthalamic nuclei is the most used option. Both treatments lead to an improvement in spatiotemporal parameters of gait and freezing of gait (FOG), obtaining good results from the beginning up to two years after the intervention, but becoming less evident with the progression of PD.

  • Parkinson’s disease
  • mirror neurons
  • gait
  • action observation

1. Introduction

It is important to consider the cognitive performance level of the patient, as his or her learning from practice will be influenced by feedback, attentional demands, and motivation to perform the task [18,20,21]. In this sense, the motor plan elaborated in the motor cortex can be accessed through the memory circuits.
It is worth highlighting the existing evidence that shows how therapy based on external sensory signals (auditory and visual) [22,23,24] and visuo-motor training help in the process of ideation and motor planning [12,15,18,20,21], emphasizing their participation in FOG improvement.
Action observation (AO) and motor imagery (MI) are two of the most important visuo-motor training strategies, being based on the activation of the mirror neuron system (MNS) to facilitate motor learning [18].
The MNS is a specialized group of neurons located in parietofrontal and limbic systems [25]. The parietofrontal MNS involves premotor cortex, parietal lobe, and the caudal part of the inferior frontal gyrus. The limbic system involves the insula and the anterior mesial frontal cortex. Other structures have been described like supplementary motor area, cerebellum, and primary and secondary somatosensory cortex. The MNS is characterized by being excited when the individual performs an action and when he observes another individual performing or imagining himself performing the action. Several studies have determined that the MNS is made up of visuomotor, audiovisual, and sensory neurons, which are activated when performing the action and through vision, hearing, and proprioception [25,26,27,28,29,30].
The characteristics of the MNS make it possible to establish its role in the understanding and intentionality of the actions of other individuals by comparing them with one’s own experience [26,27,28,31]. As a result of these cognitive processes, motor planning and motor learning or relearning take place [32].
The usefulness of the MNS in physiotherapy treatment lies in the fact that its activity precedes the non-mirror neurons. This makes it possible to predict both the goal of the action and the possible sequence of steps to reach that goal. Non-mirror neurons are only activated during the execution of the action [31].
Recent studies have been able to establish the relationship between the application of AO and MI techniques, with an improvement in the PD patient’s clinical condition in terms of motor relearning [33,34,35].
AO therapy is based on the observation of videos in which actions performed by an individual are presented and observed by the patient. This viewing is usually followed by the execution of the same action, although this last step may not be performed [36]. The person in the video performing the action may be the patient himself or a third party. The videos are usually recorded from different perspectives [32,37,38,39] and the most appropriate application protocol has not been established [36], although applications do not exceed 30 min.
Motor imagery (MI) is based on the patient imagining himself performing an action, preferably in the first person (in the absence of muscular movement) and subsequently executing this action [40,41,42,43]. This technique favors motor learning through the activation of the MNS, and there is scientific evidence that shows that when the time of imagination and execution of the action is similar, neuroplasticity is favored [44]. Furthermore, during the execution of the technique, ANS signs can be observed, such as an increase in respiratory rate or heart rate, which are related to the magnitude of the imagined effort [45]. As for AO therapy, MI has not got a main application protocol, although long applications deal with mental fatigue [33,46].
AO and MI have important advantages: they are non-invasive, safe, low-cost therapies and they can be performed at home [33].

2. Effectiveness of Therapies Based on Mirror Neuron System to Treat Gait in Patients with Parkinson’s Disease

After assessing the methodological quality of the studies using the PEDro scale, two studies were of fair quality [52,54] and one of poor quality [50]. The review by Ryan et al. [36] also included the study by Pelosin et al. [54], concluding, through the Cochrane Risk of Bias (RoB) 2.0 tool, whose methodological quality is good. Regarding the study by Mezzarobba et al. [50], its low methodological quality according to the PEDro scale was because it refers to the original article to explain the methodology [49]. Considering that the methodological quality of the original article was 8/10, this result can be extrapolated to the low-scoring article [50]. Therefore, it would be interesting to use several tools to assess the risk of bias of the review articles.
According to Ryan et al. [36], there is level 1 evidence to support AO intervention for the improvement of balance, FOGt, disease severity, and other motor and non-motor skills (aerobic capacity). However, the studies included in this review [36] do not provide the same level of evidence for the improvement of spatiotemporal gait parameters in PD patients. Taking this into account, it would be interesting to prioritize the performance of RCTs of high methodological quality that would allow good evidence to be obtained and strong recommendations to be made.
This review does not include studies assessing the long-term effects of MI in isolation. In a previous review, studies evaluating the long-term effects of MI in PD patients were found [33]. Braun et al. [55] concluded that the combination of MI with physiotherapy did not produce significant improvements in any of the study variables (including gait) compared to the CG in which a combination of physiotherapy and relaxation was applied. Therefore, it would be interesting to follow this line of work to corroborate these results or to add new evidence to the existing one.
The analysis carried out in this review shows promising results in all the variables under study, but there are also certain controversies. The significant improvement in the variables to be analyzed in the EG (disease severity, quality of life, balance, and gait) is evident in all the studies in which they were evaluated with different assessment scales [49,50,51,52,53,54]. When analyzing the EG and CG of the studies separately, significant results were obtained in both for the variables under study at the end of treatment. However, these significant results were maintained at follow-up only in the EG, which leads us to believe that all included interventions based on the MNS allow for long-term improvements in disease severity, quality of life, balance, and gait.
Analyzing the comparison between the EG and CG of the studies in the review, the results were significant in favor of the EG for the variables of disease severity, quality of life, and gait in all the studies. Balance was the only variable that showed differences between studies, so it cannot be generalized that AO and MI interventions lead to a significant improvement in balance compared to conventional physiotherapy treatment in the group comparison. The studies that obtained significant improvements in EG in the group comparison were those of Pelosin et al. [54] and Sarasso et al. [53]. It would be interesting to pursue both lines of research; on the one hand, to explore the effectiveness of MI in group interventions, and on the other hand, interventions could be focused on the use of dual tasks in combination with MI and AO in group interventions.
Regarding the results obtained on FOG, all the studies in which it is evaluated (FOG-Q, NFOG-Q) achieved significant improvements in long-term EG scores [49,51,53,54]. These significant improvements only occurred in group comparisons in the study by Mezzarobba et al. [49]. On the other side, it was demonstrated that PD patients with cognitive function impairment have more risks to develop neuropsychiatric symptoms, depression, and anxiety compared with healthy controls. For that reason, motor symptoms could be a predictor of FOG [56].
Three studies [49,50,51] used auditory cues during AO. Because the use of cues improves kinematics and FOG, sonification is presented as an alternative to visual cues, which generate more dependence, as well as standard auditory cues (metronome), which are less effective in regulating patient coordination [49]. The process of sonification is based on the transformation of kinematic data, of a movement visible in a video, into sounds. This could add additional information of the movement to the patient, so that they could reproduce it in a better spatio-temporal way. A research proposal would be to perform a combined MI protocol with sonification or even AO − MI + sonification.
Sarasso et al. [53] conducted the first study on the effects of joint application of AO and MI in long-term treatment and follow-up in patients with PD. The use of both tools together enhances their effect on the activation of the MNS (motor learning benefits) [35]. In addition, the implementation with a double task (motor-cognitive) allowed for the improvement of cognitive functions such as attention and working memory (which are usually affected in PD from early stages) [57,58]. This evidence opens the door to new intervention protocols that would be interesting to explore.

This entry is adapted from the peer-reviewed paper 10.3390/jcm11144236

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