Basic Research

#### **Chapter 1**

## Application of Attention Focus in Rehabilitation to Promote Motor Performance and Motor Learning

*Shun Sawai, Shoya Fujikawa, Ryosuke Yamamoto and Hideki Nakano*

#### **Abstract**

Attention focus plays an essential role in promoting motor performance and motor learning. There are two types of attention focus: internal focus and external focus. Internal focus refers to direct attention inside the body while external focus refers to direct attention outside the body. Several studies have reported that external focus positively affects motor performance and motor learning by promoting automatic control. The mechanisms of attention focus have been examined using electromyography (EMG), electroencephalography (EEG), and functional magnetic resonance imaging (fMRI). During rehabilitation, therapists promote patients' movement acquisition and motor learning. This chapter reviews the application of attention focus in rehabilitation to promote motor performance and motor learning in patients.

**Keywords:** attention focus, internal focus, external focus, performance, motor learning, rehabilitation

#### **1. Introduction**

When a person exercises, their attention is somewhere else. Attention focus describes a change in behavior depending on the focus of one's attention. Attention focus can be divided into internal focus and external focus. Internal focus is defined as "instructions related to the learner's own body movements." External focus is defined as "instructions related to the effects of the performer's actions on the environment, for example, the experimental apparatus" [1]. Several studies have reported that external focus is more effective for performance and motor learning than internal focus. The positive effects of external focus are explained by the constrained action hypothesis (CAH). The CAH states that "trying to consciously control one's movements constrains the motor system by interfering with automatic motor control processes that would "normally" regulate the movement" [2]. Based on the CAH, internal focus promotes conscious control of movement by directing attention to inside the body, inhibiting the automatic control of movement, resulting in a negative effect. In contrast, external focus positively inhibits conscious control of movements and promotes automatic control of movements by directing the individual's attention

externally. In this chapter, the effects of internal focus and external focus on changes in performance and motor learning are summarized. In addition, the application of attention focus in the field of rehabilitation is discussed.

#### **1.1 The origin of attention focus**

The first study regarding attention focus was reported by Wulf et al. [1] who examined the effects of internal focus and external focus on motor learning during a slalom movement using a ski simulator. The participants moved rhythmically to the left and right with as wide amplitude as possible. The study was divided into three groups: internal focus, external focus, and a control group who did not receive instructions regarding attention focus. Participants in the internal focus group were instructed to "try to exert force on the outer foot." Participants in the external focus group were instructed to "try to exert force on the outer wheels as long as the platform moved in the respective direction." Therefore, the attention of the participants in the internal focus group was directed to their feet and that in the external focus group was directed to the ski simulator. The amplitude of the movements increased with task performance, and greater learning retention was observed in the external focus group than in the internal focus and control groups. The task performance was the worst in the internal focus group. Although changes in performance due to attention had been examined previously, the classification of attention focus as internal focus and external focus led to the development of studies regarding attention focus. This inaugural study also reported the positive effects of paying attention to the outside of the body (external focus) and the negative effects of paying attention to the inside of the body (internal focus). Subsequently, the effects of attention focus during various tasks have been examined.

#### **1.2 Attention focus during balance control and sports activities**

The effects of attention focus on healthy participants have been examined during several tasks that require accuracy, including balance tasks and sports activities. Several studies have examined the effects of attention focus on performance and motor learning during center of pressure sway (COP) control using a stabilometer. As it is difficult to observe the effect of attention focus during simple tasks [3], studies that include healthy young participants often include difficult postural tasks or tasks performed on rough surfaces. For example, previously-used tasks include posture maintenance while grasping an object [4, 5] and maintaining a single leg standing position on a rough surface [6, 7]. During these tasks, the attention focus can be directed externally via showing the participant the COP cursor measured by the stabilometer or instructing the participant to keep the object as still as possible. In contrast, the attention focus can be directed internally by focusing the grasping hand or the entire body during posture control. A previous study that examined the effects of attention focus during balance tasks reported the positive effects of external focus [8]. The effects of attention focus during postural control tasks have also been examined in elderly participants [9], in which the same positive motor learning effects are observed. Elderly people often suffer fractures due to falls and require rehabilitation [10]. Therefore, it is expected that external focus can promote the improvement of postural control during rehabilitation for fall prevention.

The effects of internal focus and external focus have also been examined during sports activities that do not require open skill, such as golf putting, dart shooting, and

#### *Application of Attention Focus in Rehabilitation to Promote Motor Performance and Motor… DOI: http://dx.doi.org/10.5772/intechopen.105438*

basketball free throws. In golf putting, internal focus directs attention to the arm or the putting motion and external focus directs attention to the golf club or the course of the ball. Several studies have reported more favorable motor learning via external focus than when internal focus or control conditions are used [11, 12]. External focus improves putting accuracy, kinematic parameters [13], and muscle activity as measured by electromyography (EMG) [14], as it smooths the putting motion and decreases muscle activity in the lower extremities. Less muscle activity is required to complete efficient movements. These results indicate that external focus promotes accurate and efficient golf putting. Similar results have been reported regarding the effects of external focus on motor learning during dart shooting and basketball free throws. Internal focus was directed to the participant's wrists and hands, while external focus was directed to the dart trajectory (during dart shooting) or the basket (during basketball free throws). External focus increased movement accuracy, improved kinematic parameters, and decreased muscle activity in both activities [15–17], suggesting that external focus is efficient for motor learning of sports movements that require accuracy and may contribute to the acquisition of more accurate movements. Therefore, verbal instructions regarding external focus may be effective for the rehabilitation of athletes.

#### **1.3 The effects of attention focus on muscle strength and endurance**

The effects of attention focus on muscle strength [18], muscular endurance [19], and tasks requiring accuracy have been reported. Several studies have reported shortterm gains in muscle strength when external focus is used. External focus increased muscle strength during grip strength [20] and squat and deadlift [21] activities. In addition to muscle strength, changes in muscle activity (measured using EMG) have also been reported [22], suggesting that unnecessary muscle activity during movement is reduced by external focus, promoting more efficient movements. These findings also indicate that the use of external focus results in efficient exercises that encourage selective participation of the muscle groups necessary for the movement. Therefore, muscle strengthening training should be conducted using external focus. However, a previous study reported decreased muscle activity but no improvement in muscle strength when the same muscle force was exerted [23]. No study has reported the positive effects of consistent external focus, and there is no clear difference between internal focus and external focus when examining the long-term effects of training. However, when limited to the lower limb, muscle strength training using external focus has resulted in more favorable outcomes. One study [24] reported the positive effects of internal focus. Therefore, although there is currently no evidence to actively recommend external focus, there is a high possibility that the use of external focus provides more favorable muscle strengthening than internal focus. Patients undergoing rehabilitation due to orthopedic, cardiovascular, or other medical diseases often suffer muscle weakness due to disuse, and require efficient muscle strengthening training. Training using external focus is preferred for muscle strengthening training during rehabilitation.

The positive effects of external focus on muscular endurance have also been reported in several studies. Studies including repetitive exercises using the upper extremities, such as push-ups [20] and bench presses [25], and repetitive exercises using the lower extremities, such as squats and deadlifts [22, 26] have been reported. External focus is used to direct attention to the object during tasks that require the use of heavy objects, such as bench presses and squats. For tasks that do not require

the use of an object, such as push-ups, the participants' attention is directed to the external environment, and the participants are instructed to "push on the floor." External focus has been reported to decrease the perception of fatigue and muscle tiredness [27] and it decreases muscle activity when the same muscle force is exerted [22], allowing for more efficient exercise. Increased efficiency prolongs the time to muscle fatigue. The long-term effects of attention focus on improving muscle endurance have not been examined and remain unclear. However, the short-term improvement in muscle endurance when external focus is used allows for more training sessions, resulting in more efficient training for the improvement of muscle strength and endurance. Patients undergoing rehabilitation often have weakened muscular endurance and strength. Therefore, the use of external focus is an efficient method for improving muscle strength and endurance during rehabilitation.

#### **1.4 Dominance of attention focus**

The dominance of attention focus has been reported recently as some individuals are internal focus-dominant and others are external focus-dominant. The relationships between abilities and the dominance of attention focus have been examined. Perkins-Ceccato et al. [28] reported that the dominance of attention focus depends on performance during a golf putting task, as a highly-skilled group had a better performance using external focus and a low-skill group had a better performance using internal focus. These results may be due to the fact that the low-skill group must pay attention to each step of the movement to perform it accurately. While beginners need to pay attention to the movement, external focus diverts their attention to the external environment. Participants in the low-skill group may have had insufficient attentional capacity to perform unfamiliar movements when external focus was used, resulting in a worse performance than that of the external focus group. Therefore, internal focus is effective in low-skill groups. Sakurada et al. [29] reported that the dominance of attention focus depends on the motor imagery ability in upper limb tracking tasks. The modality of motor imagery ability includes motor sensory imagery ability and visuomotor imagery ability. Participants with high motor-sensory imagery ability (motor-sensory dominant group) had more favorable motor learning using internal focus while participants with high visual imagery ability (visual dominant group) had more favorable motor learning using external focus. The modality of motor imagery ability and the dominance of attention focus are correlated. Therefore, the effects of internal focus were improved when the polarity of motor sensory dominance was increased. In contrast, the effects of external focus were improved when the polarity of visual dominance was increased. The cortical localization required in motor imagery and attention focus tasks is similar, which may account for the association between the modality of motor imagery ability and the dominance of attention focus. In the previous study, the motor-sensory dominant group had experience in sports that required closed skill, such as swimming and track and field. The visual dominant group had experience in sports that required open skill, such as volleyball and basketball. Therefore, the results of the study may be influenced by the participants' experiences with motor learning and sports training. The visual-dominant group was much larger than the motor-sensory-dominant group [30], suggesting that the observed positive effects of external focus may be due to the difference in group size. Performing tasks with optimal attention strategies leads to better performance, improvement, and promotes motor learning effects. During rehabilitation, therapists are required to tailor interventions to individual patients, and interventions that

*Application of Attention Focus in Rehabilitation to Promote Motor Performance and Motor… DOI: http://dx.doi.org/10.5772/intechopen.105438*

consider the patient's dominance of attention focus may improve the efficiency of rehabilitation. However, few studies regarding the dominance of attention focus have been reported and the results are inconsistent. Therefore, factors that determine the dominance of attention focus should be identified in future studies, and a scale to assess the dominance of attention focus should be developed.

#### **1.5 Summary**

The definitions of internal focus and external focus and the effects of attention focus during various movements based on previous studies that included healthy participants have been described. External focus is thought to be effective to promote the automaticity of movement during rehabilitation. However, the dominance of attention focus requires additional research. The consideration of the optimal attentional focus for patients during rehabilitation interventions will lead to effective and individualized rehabilitation services.

#### **2. Neural basis of internal focus and external focus**

Several studies have reported that brain function is related to performance [31–33] and motor learning [33–35]. Similarly, attention focus, which influences performance and motor learning, is expected to be related to brain function. Recently, encephalography (EEG), functional magnetic resonance imaging (fMRI), and functional near-infrared spectroscopy (fNIRS) have been used to examine the neural basis of attention focus. An understanding of the neural basis will not only clarify the existence of attention focus but will also be useful to consider new intervention methods for the modulation of brain activity via neuromodulation and other techniques.

#### **2.1 Neural basis of attention focus**

The neural basis of attention focus remains unclear. However, several reports have considered differences in brain functions as related to information processing and cognitive control. Raisbeck et al. [36] used fMRI to examine the effects of attention focus and the differences between internal focus and external focus during knee flexion and extension movements and found that internal focus activates motor-related areas (primary motor cortex and primary somatosensory cortex) and the cerebellar folium vermis. The use of internal focus increases the processing of somatosensory information and the activation of motor-sensory areas. The cerebellar folium vermis is active in internal cognition [37]. The activation of the cerebellar folium vermis may indicate increased cognitive demands. Internal focus increases cognitive demands as it promotes conscious control of the body. In contrast, activation of the anterior part of the lingual gyrus, occipital pole, occipital spindle gyrus, and parahippocampal gyrus was observed when external focus was used. The lingual gyrus and occipital pole are located in the occipital lobe and are involved in the processing of visual information [38]. The occipital spindle gyrus is involved in object recognition. The activation of these three regions indicates an increase in visual information due to the use of external focus. Furthermore, the parahippocampal gyrus is associated with visual memory [39], indicating visually dominant control with external focus. Another study that used EEG reported that external focus activates visual areas [40]. However, additional studies [40, 41] have reported that external focus activates motor-sensory areas, which

is inconsistent with the results of the study by Raisbeck et al. [36]. The activation of motor-sensory areas by external focus is caused by the integration of visual and somatosensory information. The increase in visual information due to the use of external focus further increases the somatosensory information, activating the motor-sensory area during the processing of this information. This effect is related to the improvement of performance. Another area associated with this cognitive control is the activity of the frontal region. High theta wave activity in the frontal region of the EEG (FMθ) has been observed during concentration in cognitive tasks [42]. FMθ is also observed when external focus is used [40] and may reflect the effects of attention focus.

The neural basis of attention focus is based on previous studies that have considered the brain regions activated by internal focus and external focus to support function. However, several studies have suggested that the inactivation of brain regions or brain activity similar to that at rest may be efficient. Kuhn et al. [43] used transcranial magnetic stimulation (TMS) to examine the effects of attention focus and the intracortical inhibition of the primary motor cortex and found that external focus improves performance and activates inhibitory circuits in the primary motor cortex. The activity of the intracortical inhibitory circuits indicates the suppression of cortical activity, which may indicate that the suppression of unnecessary brain activity when external focus is used leads to the efficient execution of locally-activated cortical movements. Intracortical inhibition has also been shown to affect motor control, including coordinated movements [44]. Intracortical inhibition may represent the difference in motor control during internal focus and external focus. Therefore, both the activation and inactivation of brain regions may represent the neural basis of attention focus.

#### **2.2 Neural basis of the dominance of attention focus**

The neural basis of the dominance of attention focus has also been studied as differences in brain activity due to differences in optimal attention focus existing among individuals. Brain activity in participants using internal focus and those using external focus differed in a study in which participants were divided into internal focusdominant and external focus-dominant groups based on their performance during an attention-focused task. The neural basis for the dominance of attention focus is related to information processing, cognitive processes, and the neural basis for attention focus. In a study using fNIRS, Sakurada et al. [45] reported that the right dorsolateral prefrontal cortex and somatosensory association cortex were less active in the internal focus-dominant and external focus-dominant groups when performing tasks at optimal attention focus (**Figure 1**). Participants with higher motor skills are able to perform movements with less neural activity than those with lower motor skills [46]. The dorsolateral prefrontal cortex and somatosensory association cortex are responsible for the integration of information and had low activity in this study, suggesting that the optimal attentional strategy enabled movement with less neural activity and less information processing, which indicate efficient brain activity. Furthermore, validation studies regarding event-related potentials using tactile and visual stimuli [47] and fNIRS [48] reported a relationship between the dominance of attention focus and processing of visual and tactile information, supporting the association between information processing and attention focus. In another study [49], EEG was used to examine the neural basis of the dominance of attention focus during a standing, postural control task (**Figure 2**). When internal focus was used, the left parietal lobe

*Application of Attention Focus in Rehabilitation to Promote Motor Performance and Motor… DOI: http://dx.doi.org/10.5772/intechopen.105438*

#### **Figure 1.**

*Differences in brain activity in the optimal attentional strategy [45]. The red area in the parietal lobe, indicated by 4, is the somatosensory association cortex. The red area in the frontal lobe, indicated by 11, is the right dorsolateral prefrontal cortex. These two regions showed inactivity during optimal attentional focus.*

#### **Figure 2.**

*Differences in EEG activity between the internal focus-dominant group and the external focus-dominant group [49]. The red area is activated in participants in the internal focus-dominant group, while the blue area is activated in participants in the external focus-dominant group. When internal focus is used, the left parietal lobe is hyperactive in the internal focus-dominant group (a). When external focus is used, the left frontal lobe is highly active in the external focus-dominant group (b).*

of participants in the internal focus-dominant group had higher theta wave activity. In contrast, the left frontal lobe of participants in the external focus group had higher theta wave activity when external focus was used. High theta wave activity in the parietal lobe has been reported to be associated with the processing of proprioceptive and superficial sensory information [50] and with attentional control [51]. Therefore, the internal focus-dominant group may have increased superficial sensory processing when internal focus is used and may have higher attentional control when directing attention to the inside of the body. In contrast, high theta wave activity in the frontal lobe has been reported to be associated with error detection [52] and cognitive control [53]. Therefore, the external focus-dominant group is more likely to selectively pay attention to the outside of the body when external focus is used and may perform postural control by error detection based on visual information. Studies regarding the neural basis of the dominance of attention focus indicate that sensory processing and cognitive processes are involved.

The results of these studies are contradictory as to whether higher or lower brain activity is more favorable. Some studies have reported that higher brain activity improves information processing [54] and cognitive control [55] by activating more neurons. However, during motor learning [56] and movement mastery [46], lower brain activity has been reported to imply more efficient neural activity. These studies also reported that optimal attentional strategies generated less brain activity and efficient neural activity, while greater neural activity resulted in better performance. Although it is clear that there is a difference in brain activity, further research is needed.

#### **2.3 Summary**

The neural bases of attention focus and attention focus dominance involve sensory information processing and cognitive processes. Changes in performance and motor learning due to attention focus occur in the same environment. Therefore, performance and brain activity change based on how information is processed and perceived. The ability to process information and cognitive control may determine the effects of attentional focus.

#### **3. Attention focus during rehabilitation**

The use of attention focus to improve performance and promote motor learning does not require specific equipment, making it extremely easy to implement in clinical trials. However, there is a high induction to internal focus during stroke rehabilitation [57], especially with feedback to patients, which is mainly internal focus [58, 59]. Therefore, attention focus may not be considered during rehabilitation. In addition to basic research regarding attention focus, clinical research has shown how rehabilitation can be conducted more effectively via the incorporation of attention focus. In this section, the effects of attention focus on patients with specific diseases are described.

#### **3.1 Attention focus in patients with stroke**

The effects of attention focus in patients with stroke have been examined during tasks such as upper limb movement, gait, and postural control. These tasks are related to movements that are impaired by stroke and that impede the return to home and

#### *Application of Attention Focus in Rehabilitation to Promote Motor Performance and Motor… DOI: http://dx.doi.org/10.5772/intechopen.105438*

social reintegration. The effects of attention focus have been examined during some accuracy-requiring tasks. More clinical studies have been conducted in patients with stroke with impaired dexterity than in patients with other diseases, and external focus has been reported as effective for patients with stroke. Gomes et al. [60] examined the effects of attention focus during upper limb tasks performed by patients with stroke. The temporal data acquisition instrument (TDAI) [61], an upper limb function test for patients with stroke, was used. The patients' upper limb movements were captured using a camera, and the upper limb movement time, speed, and peak speed were calculated. The results indicate that internal focus and external focus promote motor learning compared to no instructions regarding attention focus in these patients. However, there were no differences in motor learning effects when internal focus or external focus were used. Patient performance is improved when external focus is performed after internal focus as patients with stroke are more likely to exercise conscious control of their movements [62]. Conversely, there was no improvement in performance when internal focus was used after external focus. This indicates that external focus suppresses conscious control of movement and improves performance. A negative correlation between conscious control and motor function has been reported in patients with stroke, and patient function improves when the patients depart from conscious control. As internal focus promotes the conscious control of movements [63, 64], it may be effective during early rehabilitation in patients with stroke who tend to exercise conscious control. Therefore, no differences in motor learning were found when internal focus or external focus were used. However, no reports regarding the relationship between the stage and severity of stroke and the dominance of attention focus have been reported. As the benefits of verbally instructing patients with stroke to pay attention during upper limb movements are clear, these patients should be instructed to pay attention to their upper limbs and the environment, instead of simply performing repetitive movements.

Kim et al. [65] reported that external focus increased step and stride lengths, walking speed, and load on the paralyzed leg when employed during walking in stroke patients. In this study, the subjects' attention was directed to their lower limbs in the internal focus condition and to a line drawn on the floor in the external focus condition. The results indicate that external focus not only improves gait parameters such as step length, but also promote loading of the paralyzed lower extremity. This may be due to the fact that external focus promotes automatic gait control, resulting in a gait pattern similar to normal gait, which in turn promotes loading of the paralyzed lower limb. This is also important for the acquisition of symmetrical and stable gait [66], and the gait speed may have been improved by adopting a gait pattern similar to normal gait. In the rehabilitation of stroke patients, walking ability is an important factor that determines the outcome [67] and the patient's level of living [68]. In addition, it has been reported that gait training for chronic stroke patients does not produce sufficient evidence for functional recovery [69], and efficient improvement of walking ability during the recovery phase is required. Furthermore, it is necessary to acquire automaticity of movements by various tasks for walking in stroke patients [68], and we believe that automating movements with external focus based on the restricted action hypothesis (CAH) is effective. Based on the above, we recommend an efficient intervention with external focus to improve walking ability in stroke patients.

Aloraini et al. [70] compared kinematic data obtained via motion capture and physiological data obtained via EMG during a step postural control task performed by patients with stroke using attention focus. The step task was performed under

various step distance and step landing area conditions. When external focus was used, the body movement time, higher peak velocity, and time to peak velocity were shorter and the sway in the final position was smaller. The timing of muscle contraction was faster and the muscle contractions were smaller when external focus was used. Smaller muscle contractions indicate more efficient movements. These results indicate that external focus is effective for postural control in patients with stroke.

The effects of attention focus on motor learning during postural control tasks have also been reported. Kal et al. [71] examined the long-term effects of attention focus during postural control tasks in patients with stroke and found that although external focus improves performance in the short term, there were no significant differences between the long-term effects of internal focus and external focus. However, external focus was effective for patients with stroke who had improved balance, good sensory function, and a small attention capacity, indicating that the interventions should be tailored to individuals based on their optimal attention focus. These results agree with those of Perkins-Ceccato [28], who reported that external focus is effective in patients with high ability, and in an additional study [49] that reported that an internal focus-dominant group has high attentional control ability based on EEG activity. However, few studies have examined the long-term effects of attention focus, and sufficient evidence has not been obtained. More research is necessary. In addition, the symptoms of stroke vary according to the location of the lesion, and the effects and dominance of attention focus may differ based on the stroke symptoms. Therefore, more studies regarding the effects of attention focus in patients with different stroke symptoms are needed. Patients with stroke often suffer from impaired balance due to trunk dysfunction [72], and rehabilitation often includes interventions to improve balance ability [73]. Recently, virtual reality (VR) training [74–76] and electrical stimulation [77] have been investigated as new intervention methods for postural control in patients with stroke. Although these new intervention methods have been reported as effective, they require specific equipment and are difficult to implement in some situations. In comparison, attention focus can improve the postural control using only verbal instruction from therapists and requires no equipment or cost. Therefore, attention focus is clinically useful, and interventions should be conducted to promote performance and motor learning while seeking the optimal attention focus for postural control in patients with stroke.

The effects of attention focus on patients with stroke are not consistent. However, no studies have reported more favorable results without the use of attention focus compared to with the use of attention focus. Therefore, not considering the patient's attention focus may impede performance improvement. The use of the patient's optimal attention focus may lead to improved performance during the rehabilitation of patients with stroke.

#### **3.2 Attention focus in patients with Parkinson's disease**

The effects of attention focus in patients with Parkinson's disease have been examined during postural control and gait tasks. The main symptoms of Parkinson's disease are tremors, rigidity, immobility, and impaired postural reflexes [78]. Impaired postural reflexes lead to decreased gait ability, resulting in decreased activities of daily living (ADL) [79]. Therefore, effective treatment methods for postural control and gait are essential for patients with Parkinson's disease. Paradoxical gait [80] triggered by auditory or visual information is a well-known characteristic of Parkinson's disease. Therefore, the performance of patients with Parkinson's disease

#### *Application of Attention Focus in Rehabilitation to Promote Motor Performance and Motor… DOI: http://dx.doi.org/10.5772/intechopen.105438*

can be improved via exercises based on information from the environment. The use of external focus has positive effects in patients with Parkinson's disease. Wulf et al. [81] studied the effects of attention focus during a standing posture control task on an unstable surface performed by patients with Parkinson's disease and found that the use of external focus reduced postural sway compared to the control condition and the use of internal focus. Patients with Parkinson's disease may have impaired endogenous regulation derived from the basal ganglia [82], resulting in poor performance during the use of internal focus. Therefore, the use of external focus is recommended for postural control training in patients with Parkinson's disease during rehabilitation.

Beck et al. [83] also examined the effects of attention focus on gait during a dual-task in patients with Parkinson's disease. The use of external focus decreased the step time, while the use of internal focus decreased the step length and gait speed, suggesting that external focus promotes automaticity during dual-task gait and that internal focus impairs the dual-task gait. The unified Parkinson's disease rating scale motor section (UPDRS subsection III) was lower when external focus was used, indicating that external focus improves motor dysfunction caused by Parkinson's disease. However, another study [84] reported increase in walking speed and stride length when internal focus was used, and that these improvements occurred without compromising the performance of the dual-task. The positive effects of internal focus are related to the pathogenesis of Parkinson's disease. Parkinson's disease causes a loss of automaticity in learned movements due to damage to the basal ganglia. Therefore, the use of external focus is less effective as it attempts to use reduced automaticity to perform movements, and conscious control (the use of internal focus) may be effective as a compensation for the loss of automaticity. In summary, both internal focus and external focus have been reported to be effective to improve gait in patients with Parkinson's disease, even when the pathophysiology of Parkinson's disease is considered. However, it is interesting to note that performance is changed by attention focus. It is necessary to clarify whether attention focus should be used to improve lost abilities or to promote the compensatory use of remaining abilities in patients with Parkinson's disease.

The effects of attention focus on patients with Parkinson's disease remain unclear. The relationship between attention focus and brain function requires further research. The effects of attention focus on patients with Parkinson's disease may be revealed via future basic research as Parkinson's disease is a neurodegenerative disease.

#### **3.3 Attention focus in patients with orthopedic diseases**

The effects of attention focus on patients with orthopedic diseases have been examined mainly in patients with anterior cruciate ligament (ACL) injuries [85]. ACL injuries are classified into contact and non-contact types. The non-contact type is caused by the force exerted on the knee joint during movements such as landing a jump or stepping [86–89] and accounts for 70–75% of ACL injuries [90]. In patients with non-contact ACL injuries, safe landing is effective in preventing re-tears. The appropriate motor acquisition through motor learning is necessary after a non-contact ACL injury, and improving the efficiency of motor learning using attention focus is of great significance in the rehabilitation of patients with ACL injuries. Gokeler et al. [91] investigated the effects of attention focus on kinematic indices for single-leg jumping movements in patients after ACL reconstruction (ACLR) and found that safe landing movements (including the knee flexion angle at contact; peak knee flexion angle; total range of motion of the hip, knee, and ankle joints in the sagittal plane;

and time to peak knee flexion angle) were significantly higher when external focus was used. However, this study examined temporary performance, and the motor learning effects are not clear. Appropriate movements are necessary for motor learning, and these movements are acquired through repetition. Therefore, movement training with the use of external focus is recommended during the rehabilitation of patients after ACLR.

Attention focus can also be used for ACL injury prevention [92, 93]. ACL injury prevention training reduces the risk of ACL injury [94] and improves the training of soccer players. The effects of attention focus on ACL injury prevention can be inferred from the kinematic effects of squatting in healthy participants. Benjaminse et al. [95] recommended interventions using external focus during single-leg squat and lunge movements. External focus has been shown to result in less knee joint eversion that can lead to ACL injuries. The use of repetitive movements that do not cause knee joint eversion may contribute to ACL injury prevention.

The effects of external focus are clearer in patients with musculoskeletal diseases than in patients with neurological diseases [96]. The contradictory findings regarding the use of attention focus in patients with neurological diseases may be related to brain function in attention focus. The lack of direct brain damage in patients with orthopedic injuries may account for similar effects of attention focus in these patients and in healthy participants. Although the effects of attention focus should be carefully examined and implemented in clinical practice, interventions using external focus are recommended, especially for patients with musculoskeletal disorders.

#### **3.4 Attention focus in patients with developmental disabilities**

The effects of attention focus in patients with developmental disabilities have been examined mainly in patients with developmental coordination disorder (DCD). DCD cannot be explained by general intellectual disabilities or specific congenital or acquired neurological disorders alone [97, 98]. Although several studies have shown the effectiveness of exercise therapy for patients with DCD [99–102], there are reports of a lack of automaticity in movement [103], and additional intervention methods are needed. Jarus et al. [104] examined the effects of attention focus on motor learning effects in patients with DCD and in normally-developing children and found that normally-developing children had good retention of learning when external focus was used, though no significant difference was found between the use of internal focus and external focus in patients with DCD. These findings may be due to the fact that patients with DCD are unable to follow instructions accurately and have a lack of concentration and interest and do not indicate that attention focus is ineffective for patients with DCD. Internal focus and external focus may not be used appropriately in these patients as it is difficult for them to pay attention to a forced motor learning task, and patients with DCD are more likely to experience decreased concentration and effort due to repeated failures [105]. Therefore, experimental tasks such as repetitive movements may not be performed appropriately, and the effects of attention focus are difficult to study. Additional studies [106, 107] have reported that the use of external focus is as effective in patients with DCD as in normally-developing children. However, the data of patients DCD and normally-developing children were combined in these studies and were not verified using the data of patients with DCD alone. Therefore, the effects of attention focus on patients with DCD remain unclear and should be reexamined in future studies. The effects of attention focus on motor learning that can improve the motor skills of patients with DCD must also be investigated.

*Application of Attention Focus in Rehabilitation to Promote Motor Performance and Motor… DOI: http://dx.doi.org/10.5772/intechopen.105438*

#### **3.5 Summary**

The effects of attention focus on patients with various disease have been studied. During rehabilitation, it is necessary to improve the movement ability and to promote motor learning. The clinical usefulness of attention focus to change those abilities is apparent. However, the study findings were inconsistent and should be interpreted with care. Further research is needed to clarify whether attention focus is diseasedependent or homeostatic.

#### **4. Conclusion**

In this chapter, the effects of internal focus and external focus on brain activity, performance, and motor learning are summarized. The effects of attention focus are unclear. However, the use of attention focus has the potential to improve patient performance during rehabilitation without the need for special equipment. Based on conflicting findings, both internal focus and external focus should be implemented during rehabilitation, and the most optimal attention focus for individual patients should be considered. The inclusion of attention focus during rehabilitation will make physical therapists' interventions more effective.

#### **Acknowledgements**

We would like to thank Editage (www.editage.com) for English language editing. This work was supported by the Yuumi Memorial Foundation for Home Health Care and JSPS KAKENHI Grant Number JP20K11173.

#### **Conflict of interest**

The authors declare no conflicts of interest.

#### **Appendices and nomenclature**


*Neurorehabilitation and Physical Therapy*

### **Author details**

Shun Sawai1,2, Shoya Fujikawa3 , Ryosuke Yamamoto4 and Hideki Nakano1 \*

1 Neurorehabilitation Laboratory, Graduate School of Health Sciences, Kyoto Tachibana University, Kyoto, Japan

2 Department of Rehabilitation, Kyoto Kuno Hospital, Kyoto, Japan

3 Neurorehabilitation Laboratory, Faculty of Health Sciences, Department of Physical Therapy, Kyoto Tachibana University, Kyoto, Japan

4 Department of Rehabilitation, Tesseikai Neurosurgical Hospital, Osaka, Japan

\*Address all correspondence to: nakano-h@tachibana-u.ac.jp

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Application of Attention Focus in Rehabilitation to Promote Motor Performance and Motor… DOI: http://dx.doi.org/10.5772/intechopen.105438*

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#### **Chapter 2**

## Potential Applications of Motor Imagery for Improving Standing Posture Balance in Rehabilitation

*Shoya Fujikawa, Chihiro Ohsumi, Ryu Ushio, Kousuke Tamura, Shun Sawai, Ryosuke Yamamoto and Hideki Nakano*

#### **Abstract**

Improving standing posture balance is an essential role of rehabilitation to prevent falls in the elderly and stroke victims. Recently, motor imagery has been reported to be an effective method to improve standing posture balance. Motor imagery is a simulation of a movement in the brain without actual movement. Motor imagery is believed to have a common neural basis with actual movement and is effective in reconstructing motor functions. Recently, it has also been shown that motor imagery can be enhanced through use in combination with neuromodulation techniques. In this chapter, motor imagery contributing to the improvement of standing postural balance and its combination with neuromodulation techniques are reviewed.

**Keywords:** motor imagery, kinesthetic imagery, visual imagery, standing balance, posture control, neuromodulation, neurofeedback, transcranial electrical stimulation, transcranial magnetic stimulation

#### **1. Introduction**

An important role of rehabilitation is to improve the standing postural balance of the elderly and stroke victims to prevent falls. Recently, motor imagery has been reported to effectively improve standing postural balance and facilitate the effects of neuromodulation techniques. This chapter outlines how motor imagery contributes to the improvement of standing postural balance and reviews how this method can be used in combination with neuromodulation techniques.

#### **2. Motor imagery**

Motor imagery is the simulation of motion in the brain without actual motion [1]. According to the PubMed database, 3853 articles on motor imagery were reviewed from 1979 to 2021, and the number is increasing every year. In addition, 1178 articles on rehabilitation using motor imagery were reviewed from 1999 to 2021, and the number of articles in this subtopic is also increasing, indicating that the application

of motor imagery in rehabilitation has been attracting attention in recent years (**Figure 1**). In addition, motor imagery has a common neural basis with actual movement and is considered to be effective in reconstructing motor function. Therefore, clarification of brain activity during motor imagery will enhance the validity of motor function reconstruction by comparing it with brain activity during the actual exercise. In this section, we review the neural basis and mechanisms of motor imagery based on previous studies.

#### **2.1 Brain function studies on motor imagery**

In 1977, Ingvar and Philipson [2] introduced the first method for displaying the mean blood flow distribution in the brain as a two-dimensional color map in the study of brain function during motor imagery. They used this method to measure and compare regional cerebral blood flow at rest, during motor imagery, and during actual movement. Subjects performed a task in which they were asked to imagine a rhythmical clasping movement of the right hand during motor imagery and then perform a rhythmical movement of the right hand during actual movement. The measurement procedure in this study was the same for all subjects, with the resting state being measured first, followed by the motor imagery, and finally the actual exercise. The results showed that motor imagery increased blood flow in the entire frontal lobe, including the supraorbital region, as well as the parietal and temporal lobe regions. However, the actual movement of the right hand increased blood flow mainly in the central sulcus. Thus, the results of this study suggest that the centers of motor imagery are located in a different region of the cerebrum than the centers that control actual hand movements. However, medical science and technology have made

#### **Figure 1.**

*Progression of the number of publications on motor imagery and the number of publications on motor imagery and rehabilitation. The red line shows the number of publications on motor imagery from 1977 to 2021. The blue line shows the number of publications on motor imagery and rehabilitation from 1999 to 2021. Data were collected from the PubMed database (https://pubmed.ncbi.nlm.nih.gov/) by online searches with the terms "motor imagery" for the red lines and "motor imagery" and "rehabilitation" for the blue lines.*

#### *Potential Applications of Motor Imagery for Improving Standing Posture Balance in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105779*

obvious progress since 1977, and new techniques, such as functional magnetic resonance imaging (fMRI) [3] and positron emission tomography (PET) [4], have been used to detect brain activity. Moreover, Hétu et al. [5] performed an activation likelihood estimation (ALE) meta-analysis of 75 studies measuring brain activity during motor imagery using fMRI or PET reported up to 2011. They were the first to examine quantitative maps of structures activated during motor imagery. The results revealed that motor imagery depends on a network that includes motor-related areas, such as frontoparietal and subcortical structures. Therefore, studies from recent years have supported the view that motor imagery and actual movement share a common neural basis. In addition, a study from 2018 [6] that compared brain activity during motor imagery and actual movement in detail reported that there is effective connectivity between motor and cognitive networks. In that study, 20 healthy subjects were tested in a series of finger tapping trials, and electroencephalography (EEG) data throughout the task were validated using dynamic causal modeling. The results demonstrated effective connectivity between the dorsolateral prefrontal cortex (DLPFC) and secondary motor areas (M2), and between primary motor areas (M1) and M2, both during motor imagery and motor execution. Furthermore, DLPFC-premotor cortex (PMC) connectivity was more strongly activated during motor imagery than during actual movement. Additionally, PMC-supplementary motor areas (SMA) connectivity and M1-PMC connectivity were more strongly activated during motor imagery than during actual movement. Thus, in addition to supporting the recent view that motor imagery and actual movement share a common neural basis, the results of that study also suggest that although they share a common neural basis, they are distinct processes. In light of the above, reports on motor imagery are increasing annually, and subsequent studies are expected to elucidate brain activity during motor imagery.

#### **2.2 Classification of motor imagery**

Motor imagery can be divided into two types—muscular sensory imagery (KI) and visual imagery (VI). Because these methods of imagery differ, resulting in differing brain activity and training effects [7], the characteristics of each method must be understood to flexibly introduce motor imagery training in rehabilitation and elicit its effects. Guillot et al. [8] used fMRI to determine whether the neural networks formed by KI and VI are equivalent. In this study, 13 subjects were given a finger movement as a motor imagery task. The results of the comparison between KI and VI showed that movement-related structures and the inferior parietal lobule (IPL) were activated in KI, whereas the occipital lobule and superior parietal lobule (SPL) were mainly activated in VI. **Figure 2** shows the results of the evoked responses obtained for KI and VI during the 5 s of the test using a FASTRAK digitizer (Polhemus, Colchester, Vermont, USA), based on the neurophysiological data measured by the magnetoencephalography system. From the figure, it can be seen that KI results in outstanding PMC activity, while VI results in an activated occipital lobe. In addition, **Figure 3** shows the power spectra of brain activity measured by EEG for four activities—kinesthetic motor imagery (KMI), visual motor imagery (VMI), motor execution (ME), and visual observation (VO). Panel (a) shows that the normalized power of the KMI and VMI conditions was similar in the alpha and beta frequency bands. Panel (b) demonstrates that the neural networks were similar in KMI and ME due to their high connectivity to regions of interest (ROI) in the sensorimotor cortex. Furthermore, VMI and VO networks were similar, with a large number of networks distributed in the DLPFC and PMC. Moreover, Hétu et al. [5] reported in detail the brain regions

#### **Figure 2.**

*Typical induced responses in KI and VI [9]. Right: induced response in KI. Left: induced response in VI.*

#### **Figure 3.**

*Power spectra and connectivity in ME, KMI, VMI, and VO brain activity [10]. (a) Grand average power spectra of the four groups. Each line represents the grand average of the normalized power of each group with all seven subjects and ROIs. (b) The average of the maximum 20% connectivity in each of the four frequency bands. The line represents the functional connectivity calculated from the mutual information, and the thickness of the edge represents the strength of the connectivity. The node represents the location of the ROI, and the size of the node represents the connectivity with other ROIs.*

that are consistently activated during KI and VI execution. KI showed consistent activation of the SMA, IPL, precentral gyrus (PcG), cerebellum (CB), left inferior frontal gyrus (IFG), supramarginal gyrus (SMG), temporal pole, putamen, anterior insula, right Rolandic operculum, angular gyrus, and pallidum. VI showed consistent activation of the bilateral SMA, left PcG, lingual gyrus, CB, light middle frontal gyrus (MFG), and postcentral gyrus (PocG). When KI and VI were combined, the left PcG, SMA, anterior insula, and bilateral putamen were consistently activated. Therefore, KI is employed during the execution of real movements, while VI is activated in the visual cortex, which processes visual information.

#### **3. Motor imagery and standing postural balance**

Improvement of standing postural balance consists of muscle strength [11, 12]; joint range of motion [13]; and somatosensory [14], visual [15], and brain function [16]. Moreover, standing postural balance and fall prevention are correlated, and

*Potential Applications of Motor Imagery for Improving Standing Posture Balance in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105779*

it has been shown that control of lateral stability is significant for fall prevention interventions [17, 18]. Recently, motor imagery has been attracting attention as an intervention to improve balance function and the effects of motor imagery on standing postural balance have been reported in healthy subjects, the elderly, patients with stroke, and those with Parkinson's disease, among others. In this section, we review the effects of motor imagery on standing postural balance compared by subject based on previous studies.

#### **3.1 Motor imagery and standing postural balance in healthy and elderly subjects**

In a study on healthy subjects, Jahn et al. [19] examined the activation/deactivation patterns of each brain region during motor imagery using fMRI in imagery tasks of standing posture, walking, running, and supine posture. In this study, 13 healthy adults with an average age of 27.3 years performed the above-mentioned four motor imagery tasks for 20 s each in the supine position with closed eyes. The results showed that different activation/deactivation patterns were detected in the three conditions of standing, walking, and running, respectively. During motor imagery of the standing posture, the thalamus, basal ganglia, and cerebellar mediastinum were activated. During motor imagery of walking, the parahippocampal gyrus and cuneiform gyrus, occipital visual area, and CB were significantly activated. Moreover, during motor imagery of running, the cerebellar vermis and adjacent cerebellar hemispheres in the CB were activated six times more than during motor imagery in the standing and walking conditions, while the parahippocampal gyrus and cuneus gyrus were not activated compared to the walking condition. These results support the concept of hierarchical organization of posture and movement and suggest that motor imagery activates low-intensity CB activity that controls standing postural balance and the sensory-motor control through the thalamus and basal ganglia. In addition, a study has examined the effects of nonphysical training on standing postural balance from the perspective of brain activity [20]. The intervention involved 16 healthy adults with an average age of 27.5 years. The study was conducted under three conditions: (1) a combination of action observation and motor imagery in which the subjects watched a video of a balance task being performed, (2) simple action observation in which they watched a video, and (3) simple motor imagery in which they imagined walking with their eyes closed. Two balance tasks were performed under each condition: static standing and dynamic standing with internal and external perturbations, which were measured four times for static trials and four times for dynamic trials in a randomly determined order. The results showed that the intervention of motor imagery during the dynamic balance task predominantly activated the putamen, CB, SMA, and M1, and the combination of action observation and motor imagery activated the PMC in addition to the brain regions activated in motor imagery alone. However, intervention with action observation did not significantly activate these brain regions. In other words, this study suggests that motor imagery training may be effective in controlling standing posture in the medial and lateral directions.

In a study of older adults, Oh et al. [21] examined the potential for effective training adaptations for fall prevention by assessing static and dynamic balance and fear of falling in older adults who have a history of falls, before and after motor imagery training or task-oriented training. This study included 34 elderly subjects aged 65 years or older, randomly assigned to three groups: a motor imagery (11 subjects), task-oriented training (11 subjects), and a control group (12 subjects). In motor imagery training, the subjects sat in a sitting posture with their eyes closed during a 10-min relaxation period. Then, they imagined movements to protect themselves in the event of a fall for

20 min. In task-oriented training, balance training focusing on daily activities was conducted. The results showed that dynamic balance and fear of falling were significantly improved in the motor imagery group compared to the other two groups. Therefore, motor imagery training for the elderly and those without disease improved balance function, suggesting that it is highly effective as an intervention for fall prevention.

#### **3.2 Motor imagery and standing postural balance in stroke patients**

In 2005, a systematic review of seven databases on the effectiveness of motor imagery interventions in stroke patients [22] revealed a significant effect of motor imagery training in the Fugl-Meyer Stroke Assessment (FMA). In another study, a 30-minute motor imagery task of daily activities was performed on the paralyzed upper limbs, and changes in the cortex were verified by fMRI after 10 weeks of intervention [23]. This study revealed significant activation in the bilateral PMC and M1, as well as in the superior parietal lobe of the paralyzed side for flexion or extension movements of the wrist on the paralyzed side. These studies suggest that intervention with motor imagery training is effective for improving function in stroke patients.

In addition, a meta-analysis of balance function in stroke patients was performed in 2016 by extracting randomized controlled trials of motor imagery intervention for gait ability and balance in stroke patients from 12 electronic databases [24]. This study reported that intervention with motor imagery is effective in improving gait performance, but no statistical difference was found concerning balance function. According to Oostra et al. [25], poor motor imagery after stroke is associated with lesions of the left putamen, left ventral premotor cortex (PMv), and long association fibers connecting the parietooccipital region and the DLPFC. In other words, the effect of motor imagery is less clearly defined when the frontoparietal network is impaired. It has also been reported that the effect of motor imagery in stroke patients depends on their ability to maintain and manipulate information in working memory [26]. Moreover, the working memory involves the frontoparietal network [27], and it is highly likely that the basal ganglia and PMC have a strong influence on motor imagery. Additionally, the frontoparietal network has been reported to be the same brain region that is activated in actual movement [5]. Thus, a part of the frontoparietal network that is related to motor imagery as well as the actual movement was impaired, which affected the result that balance function was not significantly improved in the stroke patients. However, many studies have reported statistically significant effects on walking ability and upper limb function, suggesting that screening for motor imagery effectiveness based on lesion localization is necessary.

#### **3.3 Motor imagery and standing postural balance in patients with Parkinson's disease**

Parkinson's disease (PD) presents with movement [28], cognitive [29], and psychiatric symptoms [30]. PD can be clinically classified into a tremor-dominant subtype and a postural instability gait disorder subtype, and it has been reported that balance function is more impaired and the risk of falling is higher in the postural instability gait disorder subtype than in the tremor-dominant subtype [31, 32]. In addition, the severity of the postural instability gait disturbance is a useful indicator of PD severity and prognosis [33], suggesting that improvement in balance function and walking ability may be attributed to a favorable prognosis.

#### *Potential Applications of Motor Imagery for Improving Standing Posture Balance in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105779*

Motor imagery interventions for PD have been reported in many studies. For example, Thobois et al. used PET to compare the brain activity of normal subjects and immobilized PD subjects who imagined continuous hand movements [34]. The results showed that the prefrontal cortex, SMA, superior parietal lobe, IFG, and CB were activated during motor imagery in normal healthy subjects, while M1 activation was only observed during the dominant hand trials. Furthermore, in PD patients, motor imagery of the immobile hand showed a lack of activation in the contralateral primary somatosensory cortex and CB, persistent activation in the SMA, and bilateral activation in the superior parietal lobes. Based on these results, this study reports that PD patients with immobility show abnormal brain activation during motor imagery and that ideal brain activation depends on the state of the imagery hand.

Another symptom of PD is the altered timing of continuous movements. It has been shown that movement timing in internally generated continuous movements is selectively deficient, and the defects can lead to problems in movement planning [35]. This symptom may limit the conduct and potential effectiveness of motor imagery in rehabilitation for PD patients. Therefore, Heremans et al. validated the effects of a goal-directed motor imagery task using visual and auditory cues [36]. The results showed that the motor imagery task with visual cues significantly reduced bradykinesia. Moreover, the results suggest that the effectiveness of motor imagery for restoring function in PD patients can be enhanced by employing VI, while the effectiveness of KI is low. A study of VI intervention in PD patients examined the effects on standing postural balance and walking ability [37]. In this study, VO and motor imagery were administered as VI for 6 weeks. The results showed improved balance function and gait velocity in PD patients with postural instability and gait impairment. Thus, the addition of VI to standing postural balance training in PD patients promoted specific functional reorganization of brain regions involved in motor control and executiveattentional abilities, which is expected to have a long-term effect.

#### **4. Neuromodulation techniques facilitated motor imagery effects**

Motor imagery can be easily introduced into clinical practice because it can improve performance without special equipment. However, mental practice using motor imagery is limited in that the quality of the motor imagery being performed is not feedbacked to the subject [38], which causes individual differences in the motor imagery effects [39]. Neuromodulation technology has recently attracted attention as a method to solve this problem. Neuromodulation is a technique used to regulate the nervous system by electrical or scientific measures and is applied for many diseases [40]. Using this technology to provide feedback to the subject on the quality of motor imagery may be effective in improving movement performance. In this section, we review various neuromodulation techniques that facilitate motor imagery.

#### **4.1 Combined motor imagery and neurofeedback**

Neurofeedback is a noninvasive tool for purposeful modulation of human brain function that has the potential to dramatically impact neuroscience and clinical treatment of neuropsychiatric disorders [41]. Boe et al. [42] investigated whether the combined use of neurofeedback during motor imagery tasks could modulate brain activity. In this study, 18 healthy subjects (eight males, ten females, 24.7 ± 3.8 years old) were randomly assigned to a neurofeedback group or a control group. The motor imagery task was a KI activity in which the subject continuously pressed buttons with the ineffective hand. Neurofeedback was based on event-related synchronization/desynchronization (ERS/ERD) in the β-band of the sensorimotor cortex and was provided in real-time during motor imagery from a bar graph on a projector. The results showed that neurofeedback from bilateral sensory-motor cortices increased the contralateral pattern of brain activity associated with motor imagery with each successive session compared to the control group. Thus, this study suggests that the provision of neurofeedback provides significant information about motor imagery training and an opportunity for patients to modulate their own regional brain activation. In addition, neurofeedback approaches have a background of dependence on a single brain imaging modality such as EEG or fMRI. However, a study validated breaking away from this dependency system by reporting the effects of bimodal neurofeedback with simultaneous EEG and fMRI feedback [43]. In this study, the effects of unimodal EEG- and fMRI-neurofeedback were compared with those of bimodal EEG-fMRI-neurofeedback. The results showed that EEG-fMRI-neurofeedback significantly modulated activity in the movement domain compared to the two groups of short-peaked neurofeedback, and specific mechanisms and their additional value were found. Other studies have examined the effects of EEG-fMRI-neurofeedback on motor imagery, and all have shown that neurofeedback can modulate brain activity better than unimodal neurofeedback [44, 45]. In conclusion, neurofeedback during motor imagery can modulate brain activity and improve performance. Furthermore, incorporating multimodal techniques, such as bimodal neurofeedback instead of unimodal neurofeedback, may enhance the effects obtained from motor imagery.

#### **4.2 Motor imagery and tES**

Transcranial electrical stimulation (tES) aims to noninvasively modulate brain function by applying current from the current source [46]. Cranial electro-stimulation therapy (CET), cranial electrotherapy stimulation (CES), and transcranial pulsed current noise stimulation (tRNS) are several methods of tES used as clinical treatment [47]. Several previous studies have reported the use of tES, especially transcranial direct current stimulation (tDCS) and transcranial alternating current stimulation in combination with motor imagery. Moreover, Xie et al. [48] examined the effects of tES on brain activity during motor imagery. The results showed that ERD of μ and β rhythms during a motor imagery task was significantly enhanced by the combined use of tDCS with motor imagery. In addition, a study that examined the modulation of motor learning by transcranial alternating current stimulation [tACS] [49] suggested that 70 Hz tACS enhances motor learning ability by intermodulation activity in the β-wave band. Thus, tDCS and tACS are potential approaches to modulate brain activity during motor imagery and enhance effective functions to improve performance.

#### **4.3 Motor imagery and rTMS**

Transcranial magnetic stimulation (TMS) is a technique that noninvasively modulates brain activity through the induction of currents by rapidly changing magnetic field pulses [50]. In addition, by reviewing the literature through 2018, guidelines were established for treatment with repetitive transcranial magnetic stimulation (rTMS) in Europe in 2020. The guidelines established rTMS as a clinical treatment modality, although its efficacy has not reached Level A/B evidence.

*Potential Applications of Motor Imagery for Improving Standing Posture Balance in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105779*

Moreover, rTMS can be divided into high frequency (HF) and low frequency (LF) rTMS. LF rTMS decreases the excitability of the nonaffected hemisphere [51], while HF rTMS increases it [52].

Many previous studies in which motor imagery and rTMS were combined have verified the therapeutic effects on upper limb function in stroke victims [53, 54]. For example, Pan et al. [54] investigated the effects of motor imagery and LF rTMS on upper limb motor function during stroke rehabilitation. They applied 1 Hz rTMS to the M1 of the nonaffected hemisphere; 10 sessions of 30 min were performed during a two-week intervention period. The results showed that upper limb motor function was significantly improved in the group that received motor imagery and LF rTMS in the second and fourth weeks after the intervention compared to the control group (LF rTMS-only group). Moreover, a study in which motor imagery was combined with HF rTMS [55] also revealed a significant improvement in pre- and post-stimulation performance. These results suggest that rTMS can enhance the effects obtained from motor imagery in subjects such as stroke survivors. Finally, it was suggested that there is no difference between high and low rTMS frequencies in terms of performance improvement.

#### **5. Conclusion**

In this chapter, we outlined motor imagery effects that contribute to the improvement of standing postural balance and the effects that can result from use in combination with neuromodulation techniques. We further discussed the consequences for healthy subjects and those with illnesses. Recently, the view that motor imagery constitutes the same neural basis as actual movement is gaining ground, and the main effects of motor imagery in improving standing postural balance have been demonstrated. In addition, neuromodulation technology has the potential to improve the effects of motor imagery and is expected to further contribute to rehabilitation. Thus, the combination of neuromodulation techniques with motor imagery training will be significant in improving the quality of rehabilitation.

#### **Acknowledgements**

This work was supported by the Yuumi Memorial Foundation for Home Health Care and JSPS KAKENHI Grant Number JP20K11173.

#### **Conflict of interest**

The authors declare no conflict of interest.

#### **Appendices and nomenclature**



*Potential Applications of Motor Imagery for Improving Standing Posture Balance in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105779*

#### **Author details**

Shoya Fujikawa1 , Chihiro Ohsumi1 , Ryu Ushio1 , Kousuke Tamura1 , Shun Sawai2,3, Ryosuke Yamamoto4 and Hideki Nakano1,2\*

1 Faculty of Health Sciences, Neurorehabilitation Laboratory, Department of Physical Therapy, Kyoto Tachibana University, Kyoto, Japan

2 Neurorehabilitation Laboratory, Graduate School of Health Sciences, Kyoto Tachibana University, Kyoto, Japan

3 Department of Rehabilitation, Kyoto Kuno Hospital, Kyoto, Japan

4 Department of Rehabilitation, Tesseikai Neurosurgical Hospital, Osaka, Japan

\*Address all correspondence to: nakano-h@tachibana-u.ac.jp

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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#### **Chapter 3**

## Clinical Application of Repetitive Peripheral Magnetic Stimulation in Rehabilitation

*Ryu Ushio, Kousuke Tamura, Shoya Fujikawa, Chihiro Ohsumi, Shun Sawai, Ryosuke Yamamoto and Hideki Nakano*

#### **Abstract**

Repetitive peripheral magnetic stimulation (rPMS) is a noninvasive method involving the repetitive magnetic stimulation of peripheral nerves and muscles. Recently, its potential as a new neuromodulation technique for sensory motor disorders has been recognized. Its advantages include less pain than with electrical stimulation and that neuromuscular stimulation can be performed over clothing. These advantages make it a practical and straightforward adjunct tool widely used in clinical practice. In particular, the combination of rPMS and general rehabilitation reportedly promotes functional improvement in stroke patients with difficult involuntary contractions. This chapter reviews rPMS and its potential clinical applications in rehabilitation.

**Keywords:** repetitive peripheral magnetic stimulation, motor imagery, muscle strengthening, spasticity, stroke, motor recovery, rehabilitation, physical therapy

#### **1. Introduction**

Magnetic stimulation is the application of "electrode-free electrical stimulation" using induced current from a pulsed magnetic field. The magnetic field generated by the stimulation coil induces an electromagnetic-induced overcurrent in the body that resultantly depolarizes nerves and muscles' cell membranes, thereby stimulating the brain, nerves, and muscles. Repetitive peripheral magnetic stimulation (rPMS) is applied as a treatment method that noninvasively delivers repetitive magnetic stimulation to peripheral nerves and muscles. It has attracted attention as a new means of rehabilitation, especially for sensory and motor disorders [1].

To date, neuromuscular electrical stimulation (NMES) has been widely used as a similar tool. NMES is an electrical stimulation therapy primarily performed to improve motor function, such as suppressing muscle hypertonia associated with upper-motor neuron damage, preventing and improving muscle atrophy associated with peripheral neuropathy, and increasing muscle strength. However, this therapy is associated with pain and discomfort caused by electrical stimulation. Compared with NMES, rPMS does not cause discomfort due to pain and can stimulate deep

muscles [2]. NMES evokes cutaneous receptors and may generate noisy signals, whereas rPMS generates intrinsic receptive information during muscle contraction that affects brain reversibility [3].

Furthermore, rPMS does not require the application of electrodes and can be stimulated over clothing. Similar to NMES, however, rPMS is contraindicated for pacemakers and implantable medical devices. In addition, rPMS is larger in size and more expensive than NMES, making its widespread use a challenge. However, rPMS is expected to improve functional recovery in stroke patients because of its ability to safely stimulate deeper layers and improve muscle areas without pain [4].

#### **2. rPMS studies in healthy subjects**

#### **2.1 Physiological changes in rPMS**

rPMS can improve motor function in central nervous system (CNS) diseases. How, then, would the induction of CNS plasticity be altered by the parameters of rPMS? Nito et al. [5] studied the effects of rPMS on wrist extensor muscles in terms of neuroplasticity and motor performance in 26 healthy subjects (HS). Motor-evoked potential (MEP), intracortical inhibition (ICI), intracortical facilitation (ICF), M-wave, and Hoffman reflex were measured before and after the application of rPMS, and the effects of rPMS on wrist extensor movements were examined.

First, rPMS was applied to the wrist extensor muscles at different frequencies (50, 25, and 10 Hz), with the total number of stimuli set constant to examine the physical effects of stimulus frequency. MEPs of the wrist extensors increased significantly with rPMS at 50 and 25 Hz but remained unchanged at 10 Hz. In the next experiment, in which the number of stimuli was increased and the time required to induce plasticity was examined, at least 15 minutes of rPMS were required for 50- and 25-Hz rPMS. Based on these parameters, the sustained effect of 50- or 25-Hz rPMS was evaluated after 15 minutes of rPMS. Significant increases in MEP were observed up to 60 minutes after 50- and 25-Hz rPMS were administered. Similarly, attenuation of ICI and enhancement of ICF were also observed.

In addition, the maximal M-wave and Hoffman reflex were unchanged, suggesting that the imposition of rPMS does not directly stimulate the centrifugal nerves and excite the muscles but that the increase in MEP is caused by the plastic changes in the motor cortex. In addition, an increase in force and EMG during wrist extension movements was observed after the application of rPMS at 50 and 25 Hz. These results suggest that the application of rPMS at 25 Hz or higher for 15 minutes can increase cortical excitability at the irradiated site and improve motor output from the motor cortex, rather than changing the excitability of the spinal cord circuitry.

Recent studies have also reported the effects of rPMS in combination with noninvasive brain stimulation techniques and on regions other than the periphery. Kumru et al. [6] examined the effects of paired associative stimulation (PAS), in which paired stimuli of repetitive transcranial magnetic stimulation (rTMS) and rPMS are repeatedly applied. PAS is an effective method to induce plasticity in the human motor cortex. Three stimulus conditions were applied to 11 HS for 10 minutes each. In the rPMS alone condition, rPMS at 10 Hz was applied to the extensor carpi radialis (ECR) five times every 10 seconds for 60 trials. In the rTMS alone condition, rTMS was applied to the contralateral primary motor cortex region of the ECR at a frequency of 0.1 Hz (60 stimuli) and an intensity of 120% of the ECR threshold. In the PAS condition, rPMS

#### *Clinical Application of Repetitive Peripheral Magnetic Stimulation in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105787*

and rTMS described above were performed with paired stimuli. The results showed that the PAS condition increased MEP amplitude and decreased ICI in the ECR. This suggests that PAS stimulation effectively increases corticospinal tract excitability and decreases ICI. Krause et al. [7] studied the effects of repetitive magnetic stimulation (rMS) to the right cervical nerve root (C7/C8) on corticospinal excitability in HS. The right cervical nerve root (C7/C8) innervating the test muscle, the right first dorsal interosseous muscle, was stimulated at a frequency of 20 Hz for 10 seconds with an intensity of 120% of resting motor threshold for a total of 10 trials. The results showed that rMS caused a significantly longer cortical silent period, increased ICI, and increased MEP amplitude. These changes were not confirmed contralaterally. This study confirmed that rMS increased MEP amplitude in the right first dorsal interosseous muscle without altering the left dorsal interosseous muscle. These results indicate that rMS affects motor cortex excitability similar to electrical stimulation; this suggests that rMS is applicable in spastic and central paraplegia rehabilitation.

As described above, physiological changes in rPMS have been reported in HS, and based on these studies, various clinical application studies have been conducted in the recent years.

#### **2.2 Changes in rPMS and motor imagery in combination**

Motor imagery (MI) is the simulation of movement in the brain without actual movement and is widely used in clinical practice as a tool for evaluation and treatment. Recently, the combined effects of MI and rPMS have been reported.

Asao et al. [8] examined the effects of rPMS combined with MI (rPMS+MI) on corticospinal excitability. The rPMS+MI condition and rPMS alone condition were performed on HS. In the rPMS+MI condition, rPMS was administered simultaneously with a cue for a MI task of dorsiflexion of the right wrist joint. The test muscle was the right ECR. The rPMS frequency was 25 Hz, stimulus duration was 2 s, and stimulus intensity was 1.5 times the motor threshold. In the rPMS alone condition, rPMS was administered under the same stimulation conditions as in the rPMS+MI condition. The results showed that the pre- and post-stimulus MEP ratios were more significant in the rPMS+MI condition than in the rPMS alone-intense condition, which was associated with Movement Imagery Questionnaire-Revised scores. This study suggests that an intervention combining rPMS and MI can induce more corticospinal excitation than rPMS alone.

The studies above did not clarify the effective length of intervention period for the combination of rPMS and MI to promote corticospinal excitability. Therefore, the time course changes in corticospinal excitability when rPMS and MI are used in combination have been examined [9]. rPMS alone, MI alone, and rPMS and MI combination conditions have been performed on HS. In the rPMS alone and rPMS+MI conditions, the ECR was stimulated with rPMS at 25 Hz for 2 seconds at a stimulus intensity of 1.5 times the motor threshold. In addition, the MI and rPMS+MI groups were asked to perform MI of wrist dorsiflexion for 2 seconds.

Consequently, the MEP amplitude increase of the ECR in the rPMS+MI group was observed after 10 minutes. In addition, the MEP amplitude after 20 minutes was more significant in the rPMS+MI group than in the rPMS alone group. This study suggests that the combination of rPMS and MI over 10 minutes increases corticospinal excitation and that the combined effect is more significant than rPMS alone. Overall, the combination of rPMS and MI may induce plasticity in the CNS and promote motor function recovery.

#### **3. Clinical applications of rPMS**

#### **3.1 Muscle-strengthening effects of rPMS**

One of the clinical applications of rPMS is its muscle-strengthening effect. It has been reported that rPMS promotes muscle strengthening in animals and humans without causing pain.

Yang et al. [10] investigated the effects of neuromuscular magnetic stimulation (NMMS) on strength, cross-sectional area, and thickness of the quadriceps muscle in HS. NMMS was performed on the quadriceps femoris muscle at a frequency of 10 Hz and at the maximum tolerable intensity that could be tolerated for 15 minutes, thrice weekly for 5 weeks. The results showed that maximal isometric torque and mean peak torque increased significantly after intervention, but there was no change in crosssectional area or thickness. This study suggests that NMMS effectively trains large or skeletal muscles such as the quadriceps.

Stolting et al. [11] showed that magnetic stimulation of a mouse muscle injury model caused post-traumatic muscle hypertrophy, but the effects of rPMS on human subjects remained unclear. Therefore, Hirono et al. [12] examined the acute changes in skeletal muscle thickness induced by rPMS after low-intensity exercise for clinical application of rPMS. rPMS was applied to the vastus lateralis muscle at the maximum intensity of the rPMS device after an HS performed three sets of 10 isometric knee extension exercises at 30% of maximum muscle strength. The results showed that the muscle thickness of the rectus femoris and vastus lateralis muscles after exercise increased over baseline values, with significant increases only in the vastus lateralis after rPMS. This study suggests that post-exercise rPMS induces muscle expansion *via* repetitive muscle contractions. Acute changes such as skeletal muscle expansion that occur immediately after exercise also reportedly play a significant role in subsequent muscle hypertrophy [13, 14].

rPMS has the advantage of not causing pain and has been used in clinical practice with the expectation of functional recovery in some cases. Beck et al. [15] studied the effect of early intervention with rPMS on the vastus lateralis muscle after hip replacement surgery. The subjects were patients who underwent hip replacement after a proximal femur fracture. The experimental group received 10 Hz rPMS on the vastus lateralis muscle for 15 sessions daily, five times weekly for 3 weeks, whereas the control group received sham stimulation. The results showed that the root-mean-square value of the electromyogram during the maximum voluntary contraction of the vastus lateralis muscle after rPMS was significantly improved. Tandem rise time and normal walking speed in the rPMS group also improved. This study suggests that early intervention with rPMS on the lateral vastus muscle after hip arthroplasty improves muscle strength, standing balance, and gait function. This study also indicates that rPMS can be applied to patients with pain and wounds and is expected to be widely applied in clinical practice in the future.

As described above, rPMS, which promotes muscle strengthening without causing pain, has excellent potential for clinical applications.

#### **3.2 Application of rPMS in stroke rehabilitation**

Post-stroke hemiplegia occurs in more than 85% of individuals and 55–75% have residual upper limb dysfunction [16]. After stroke, the recovery rate to a practical

#### *Clinical Application of Repetitive Peripheral Magnetic Stimulation in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105787*

level is approximately 60% for lower limb function and approximately 20% for upper limb function [17]. The effectiveness of rehabilitation and physical therapy for stroke has been reported in many cases. In this context, the effectiveness of rPMS for stroke has been reported in recent years.

rPMS is a noninvasive method of activating peripheral nerves at the stimulation site and improving muscle strength and has the advantage of being performed without causing pain. Jiang et al. [18] applied rPMS in the early subacute phase of stroke and studied its effect on severe upper limb disability. In the intervention group, rPMS of 20 Hz, totaling 2400 pulses, was applied daily for 2 weeks to the triceps brachii and extensor digitorum brevis muscles. The results showed that the rPMS group showed significant improvements in the upper limb, Barthel Index, upper limb muscle strength, and root mean square on the Fugl-Meyer Assessment compared with those in the control group. This study demonstrates that rPMS for the upper extremity after stroke improves upper extremity function and muscle strength.

Fernandez-Lobera et al. [19] studied the efficacy of rPMS as a tool to assess wrist spasticity in stroke patients. The subjects were HS, acute stroke patients without spasticity (AS), and chronic stroke patients with spasticity (CS). Spasticity was assessed by calculating the index of movement restriction (iMR) from the difference between the maximum passive movement range of the wrist joint and the evoked movement range by rPMS. The stimulation intensity of rPMS was set at 70% of the maximum output of the stimulator, frequency at 25 Hz, and stimulation duration at 2 seconds. The results showed that the amplitude, velocity, and acceleration of rPMS-induced movements were reduced in the CS compared with those in the HS and AS. The iMR values were 2.8 for HS, 13.0 for AS, and 59.2 for CS, with CS having the highest iMR value. Furthermore, the iMR value for CS decreased to 41.1 after treatment with botulinum neurotoxin.

Shoulder joint subluxation is one of the many complications following stroke and is an inhibitor of motor function recovery [20]. In particular, shoulder joint subluxation causes pain in the shoulder joint and has a significant impact on activities of daily living. Therefore, Fujimura et al. [21] investigated the effect of rPMS on shoulder joint dislocation caused by stroke. The subjects were patients who presented with shoulder joint subluxation after stroke. rPMS was performed repetitively on the supraspinatus, posterior deltoid, and infraspinatus muscles. Stimulation intensity was the maximum tolerable intensity and was performed at 30 Hz for 2 seconds for 100 sessions. Results showed that the acromion-humerus interval was significantly reduced after treatment. That shoulder joint pain, shoulder abduction range of motion, and upper extremity scores on the Fugl-Meyer Assessment also improved. This study demonstrates that rPMS for post-stroke shoulder dislocation decreases the degree of shoulder subluxation and pain and improves upper extremity motor function.

Krewer et al. [22] examined the short- and long-term effects of rPMS on spasticity and motor function in stroke patients. rPMS involved a total of 5000 stimuli at 25 Hz and a stimulus intensity of 110% of the resting motor threshold. Stimulation was applied to the extensor and flexor muscles of the upper arm and forearm twice daily for 2 weeks. Results showed short-term effects on wrist flexor spasticity (immediately after the intervention) and long-term effects on elbow extensor spasticity (2 weeks after the intervention) in the rPMS group. In addition, the rPMS group showed an improvement in sensory function. This study demonstrates that rPMS reduces spasticity and improves sensory function in stroke patients in both short and long terms.

Kinoshita et al. [23] investigated the effects of rPMS on the lower limb of chronic stroke patients on gait function. The subjects were stroke patients with lower limb hemiplegia and gait disturbance. The stimulation sites of rPMS were the gluteus maximus, vastus medialis, hamstrings, quadriceps, gastrocnemius, and soleus muscles of the paralyzed lower limb. rPMS was performed twice daily for 15 days at a frequency of 20 Hz for 3 s, 4800 pulses, and a stimulus intensity of 110% of the motor threshold. The results showed that walking speed, walking ability, and balance ability were significantly improved after the intervention. This study suggests that rPMS effectively restores gait function in stroke patients with gait disturbance.

Beaulieu et al. [24] studied the effect of rPMS on lower limb dysfunction in chronic stroke. The stimulation site of rPMS was the anterior tibialis muscle of the paralyzed lower extremity. rPMS was performed at a theta-burst frequency (three 50 Hz pulses each, delivered in 5-Hz bursts) for 190 s at 42% of maximum stimulation intensity. The results showed that the rPMS group increased ankle dorsiflexion range of motion and maximum isometric muscle strength after the intervention and decreased resistance to ankle flexor stretch. The results also suggested that these changes are related to residual corticospinal tracts. This study demonstrates that rPMS improves lower limb dysfunction in chronic stroke patients.

In conclusion, rPMS improves upper and lower limb dysfunction in stroke patients. Therefore, we believe that rPMS is a highly effective tool for evaluation and treatment in stroke rehabilitation.

#### **4. Conclusion**

This chapter outlines the physiological changes, combined effects of MI, muscle strengthening, and effects on stroke patients in rPMS. The rPMS parameters used in studies are listed in **Tables 1** and **2**. rPMS has attracted attention as a new neuromodulation technique that can noninvasively deliver repetitive magnetic stimulation


#### **Table 1.**

*rPMS parameters in basic research on healthy subjects.*


*Clinical Application of Repetitive Peripheral Magnetic Stimulation in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105787*

#### **Table 2.**

*rPMS parameters in clinical research.*

to peripheral nerves and muscles using induced current from a pulsed magnetic field. Unlike NMES, rPMS is painless and has excellent potential for application in clinical settings. In particular, many clinical studies for stroke rehabilitation have been reported in recent years. Further development of rPMS research is expected, including its effectiveness when combined with other therapies and its integration with technology.

### **Acknowledgements**

This work was supported by the Yuumi Memorial Foundation for Home Health Care and JSPS KAKENHI Grant Number JP20K11173.

### **Conflict of interest**

The authors declare no conflict of interest.

### **Appendices and nomenclature**


*Clinical Application of Repetitive Peripheral Magnetic Stimulation in Rehabilitation DOI: http://dx.doi.org/10.5772/intechopen.105787*

#### **Author details**

Ryu Ushio1 , Kousuke Tamura1 , Shoya Fujikawa1 , Chihiro Ohsumi1 , Shun Sawai2,3, Ryosuke Yamamoto4 and Hideki Nakano1,2\*

1 Faculty of Health Sciences, Neurorehabilitation Laboratory, Department of Physical Therapy, Kyoto Tachibana University, Kyoto, Japan

2 Neurorehabilitation Laboratory, Graduate School of Health Sciences, Kyoto Tachibana University, Kyoto, Japan

3 Department of Rehabilitation, Kuno Hospital, Kyoto, Japan

4 Department of Rehabilitation, Tesseikai Neurosurgical Hospital, Osaka, Japan

\*Address all correspondence to: nakano-h@tachibana-u.ac.jp

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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#### *Neurorehabilitation and Physical Therapy*

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#### **Chapter 4**

## Possibility of Using a VR System as an Action Observation Therapeutical Technique

*Jaroslav Langer, Monika Šorfová and David Ravnik*

#### **Abstract**

In recent years, 3D virtual reality (VR) systems are increasingly finding their way into biomedical applications. Nevertheless, in most cases a 3D VR is being used as an interactive system (such as Xbox Kinect or Playstation VR). These interactive systems, however effective they may have proven, not only limit use of 3D VR in patients incapable to engage in these systems due to their physical or mental disability, but also put significant requirements on medical institutions for an equipment, medical personal, and therefore institutional budget. In this article, we are proposing a 3D VR as an stand-alone action observation training device, which could limit requirements associated with abovementioned interactive systems due to its capability to stimulate a mirror neuron system of human brain, while adding minimal demands on both patient and medical facility. Research studies that confirm activity in the motor cortex will be described. We focus on the literature that describes theories, models, and experimental studies dealing with the effects of motion observations that are involved in the control and final performance of motor skills.

**Keywords:** virtual reality, mirror neuron, action observation, motor imagery

#### **1. Introduction**

3D virtual reality (VR) is currently being used mainly for gaming purposes. However, there is an increasing number of VR implementations in fields of sports training and rehabilitation. The system being used as a VR training system is usually an interactive gaming system (e.g., Playstation VR, Nintendo Wii...). Nevertheless, a simple action observation (AO) using 3D VR system without its interactive component is also an interesting, if not regularly implemented, option to increase a therapy time without an involvement of therapist in the process, due to AO's capability to activate mirror neuron network. In case the use of VR in such a way is possible, it might open up new ways of therapeutical approaches in many patient cases, where there is a lack of cooperation with patient and the interactive VR system would not be applicable.

#### **2. Mirror neuron**

A theory of the specific premotor brain cells, which are activated not only during actual motor execution of a movement, but also during observing the movement, was first formulated in 1992 by si Pellegrino [1]. An activation in the F5 area of the makak's brain was found, which was the same for particular movement components (such as a grasp) as for an observation of a human grasping an object. This provided a mechanism for explanation of AO's relation to the motor planning. A consequential research [2] described 532 specific neuron cells in abovementioned cortex area, which were named "mirror neurons" (MNs). Most of the newly found structures were reacting to the movement related to a hand grasp and about 30% of them were involved in specific manipulations and movements. Therefore, the theory about MN being an inherent part of the motor planning was developed.

#### **2.1 A road to human trials**

In subsequential studies, other major brain areas containing MN were described. Also different cells were found to have different activation stimulus (e.g., MN activated only during AO, MN activated during AO and motor execution...). However most of the research was still focused on the F5 brain area of monkey's brain, where the highest number of MN was found, mainly due to inaccurate or unsafe observing methods for human trials.

Nowadays (03/2022) PubMed returns over 200 results to search of "mirror neurons AND human". Usually, an activity of MN system is measured by functional MRI. A problem is in contrast agents, which are normally used in the monkey trials (most often monocrystalic iron oxide nanoparticles), but are toxic for the human bodies [3].

For differentiation of specific neuron cells via fMRI is theoretically possible solution in natural neuron adaptation on stimulus-neural response decreases with stimulation. For MN, the decrease should be present both via observing and via executing movement. There are studies available [4] that confirm this theory, whereas others did not find any MN adaptation signs in humans [5] or in monkeys [6].

However, there is an evidence for neuron activity in same regions of premotor cortex during action observation for humans and monkeys [7].

In 2012, Molenberghse et al. described on fMRI (n = 125) 14 areas with the corresponding activity to the stimulus as with the monkey brains. These areas mainly contain prefrontal gyrus, ventral and dorsal motor cortex an parietal lobe during action observation; however, MN characteristic activity was also found in the amygdala, insula, and other regions of cortex during emotional and acoustic stimulation. In total there was described activity corresponding to MNs in 34 Brodmann areas of the human brain. Although the authors conclude the paper with the observation that, taking into account the findings from monkey brains, it is unlikely that all the 34 regions directly contain MN cells, there is found the recurrent response of the human brain to sensory (optical, auditory, and emotional) stimuli, as well as downstream activity in cortical areas, corresponding to the presence of MN [8].

#### **2.2 Stimulation of MN as a way to train motor skills**

The abovementioned findings open up, among other things, the possibility of using the MN stimulation as a training or therapeutic tool. Due to the activation of some MN during the execution and monitoring of the movement, and provided that these MN are involved in movement imagery and planning, their targeted involvement can be as a tool for training motor functions. In practice, the targeted MN can be set into two types: the aforementioned action observation and a motor imagery (MI).

#### **3. Action observation and a clinical use**

The use of AO in the treatment of motor deficits is a relatively well-documented phenomenon. Some authors refer to AO directly as to a mechanism activating MN that mediates sensory and emotional learning, as well as learning from an observation of movement, and thus represents the potential for the use of AO and its action through MN as a passive rehabilitation and learning technique for both cognitivebehavioral and motor function [9].

The effect of independent AO on postural stability and movement coordination has been described. For example, Son & Kang [10] observed another person performing the same test between two measurements and found a significant increase in stability during Y-balance test compared with the control group. Given that observation of another person performing the test was the only difference in the test protocol between the test and control groups, the authors conclude that AO, even without the use of an additional training technique, has the potential to affect stability.

Similarly, Gatti et al. [11], in their comparison of the AO and balance effect training, focus on the effect of AO on the stability. The authors measured the changes in center of pressure (COP) in stance modifications. The sample of probands (n = 79) was divided into three groups with different training protocols (AO, AO with a movement imitation, balance training) and one control group. The balance training consisted of a series of coordination and stability demanding movements (walking on the balance beam, standing on a trampoline on one leg, standing on a roller, etc.). The video used showed the same movements performed by a professional athlete. According to the results of this work, the AO together with the imitation of the movements even appears to be an equivalent training tool to increase postural control as a stand-alone balance training (effect size ES [0,7]) compared with the control group. AO alone then has a lower effect size (ES [0.3]), but still it is significant.

There has also been described an increase in muscle strength in the hand movement after AO therapy. For example, Porro et al. [12] found that of the 82 participants in the experiments, for the physical training, group muscle strength was 50% higher than baseline values were, but even in the AO-only intervention group, this change was significant (+33%) compared with the baseline values. There was no significant change in the control group.

The findings open the question of using AO for motor stability learning with temporarily immobile patients or in specific motor deficits.

A positive effect of AO intervention for post-stroke patients has also been described. Nevertheless, AO appears to be the most effective as an addition to execution of an observed activity (overall balance index 2.3 ± 2.0 before and 1.2 ± 0.8 post-test; mEFAP 102.2 ± 45.5 pre and 54.2 ± 41.4 post-test) [13].

For children and adolescents with Down syndrome, the use of "therapeutic virtual reality" represents an opportunity to significantly improve coordination and stability of movement and, last but not least, the fun in exercise (46.86 + 7.98 before, 53.57 + 1.99 after therapy in the KTK motor test) [14]. Lohse et al. [15] in a systematic review and meta-analysis of 26 papers describing the effect of VR in the rehabilitation of stroke patients found that using VR therapy results in significant effect

compared with conventional therapeutic methods in standard motor tests results (ES [0.48]), as well as in functional tests ("ADL" tests; ES [0.58]). VR games (XBox 360 Kinect) were also used to successfully influence the coordination skills of children with central coordination disorder as measured by the DCDQ test (p = 0.003 for α = 0,05) [16]. And in addition to the aforementioned collection of work dedicated to MN activity on fMRI, there are also five studies measuring EEG from which the result is that both AO and mirror therapies increase the possibility of motor unit inhibition in spasticity [17].

Hebert [18] showed that AO has a positive effect on coordination, the ability to plan and to learn, even for complex activities and movements such as a "speed stacking" (building pyramids from the cups). In three training rounds of VR, the probands in the first round were slower than in the second round (Cohen's d = 0.64) and in the second round they were slower than in the third round (Cohen's d = 0.56).

LoJacono et al. then showed that training in a virtual environment can change the movement strategy in a real environment. Between two "cross obstacle" tests in the real environment, probands (n = 40) underwent training of the same movement on a treadmill with an obstacle projected using VR. It was confirmed that the training effect is already observable in the virtual environment (F[3,36] = 5.10, p = .01, η2 = 0.30), and even that there is a change in movement strategy in the real environment and that the movement after the training is performed more safely (F[4,34] = 4.42, p = .01, η2 = .34) [19].

#### **4. Motor imagery and its clinical use**

From the available evidence, MN system activity is present not only at the abovementioned observation, but also when imagining movement [20–23]. At first glance, thus the MI appears to be a substitutable mechanism for AO and VR systems.

However, specific studies dedicated to this possibility seem to suggest otherwise. According to data from Gonzalez-Rosa et al. from EEG imaging during the implementation of complex movements of all four limbs during the training, there is an increase in activity for the both training mechanisms (F(4, 52) = 4.18, p = 0.02), but with a significantly higher MN activation during AO in both the parietal lobe (p = 0.03) and frontal lobe (p = 0.79) compared with MI training. Then, during the execution of the trained movement, the observable effect during kinematic analysis in movement speed (F(5,130) = 6.58, p < 0.01), as well as a group effect [F(2, 26) =3.73, p = 0.03] with a significant difference between the AO and MI groups (p = 0.03) occurred. The results, among others, were interpreted by the authors as showing lower MN activation and thus lower clinical effect of MI, probably due to the imagery of unspecified movement difficult for probands to imagine specifically. The authors open a discussion on the imaginative abilities of the probands [24].

Similarly, Neuper et al. describe MN activation in MI, but lower than in AO [25]. And Bakker et al. [26], measuring brain excitability, found an effect of imagining a simple dorsiflexion leg movement, but for a complex movement (walking), this effect was only evident for probands with above-average excitability for the simple movement.

Thus, although MI appears to be a suitable alternative to therapies using AO, the resulting activation can be highly variable. In its use, reliance must be placed on the interindividual psychomotor abilities of the patients and during the course of therapy there is no option beyond the relatively complicated EEG measurement *Possibility of Using a VR System as an Action Observation Therapeutical Technique DOI: http://dx.doi.org/10.5772/intechopen.105579*

or fMRI to check for correct implementation of the therapy. In contrast, in AO, the therapy can act on relatively complex and specific motor functions (grip, dorsiflexion of the leg, etc.) in a specific way, which is easily repeatable in the case of videoassisted AO.

Based on the different brain activity and the different effects of each type of training in the above works, we hypothesize that using AO visual feedback contributes positively to the activation of the MN system and thus potentially leading to a higher training effects. The aforementioned findings pointing to a lower effectiveness of MI training compared with AO, as well as to interindividual differences in the effect of MI on brain activity (especially in more complex movements), represent potential limitations to the use of MI in clinical practice.

#### **5. Mechanisms in AO and MI**

Differences between AO and MI are not only in clinical effects but also in mechanisms of their effects on brain activity—AO has a higher proportion of visual feedback, thus providing a concrete representation of the trained movement. Following a different principle of MN activation, different activity of individual brain regions was found.

During AO, activity was observed mainly in the brain regions ventral and dorsal premotor cortex (VPC, DPC), in the upper and inferior parietal lobe, in the sulcus temporalis superior, and in the dorsolateral prefrontal cortex. Combination of these areas is called an "action observation network" (AON). In some of these areas, particularly in the VPC, in the inferior temporal lobe and in the sulcus temporalis superior, the presence of MN has been described [27]. AON activity is also associated with an increase in motor-evoked potentials, i.e., with an increase in corticospinal excitability.

During MI, activity is observable in the supplementary motor area, in the primary motor area, the premotor area, the basal ganglia area, and the cerebellum, areas similar to those involved in real movement; however, the activity in these areas is in comparison to the actual execution of the movement different—in MI, the activity of the premotor cortex in particular is significantly lower [28]. At the same time, the activated regions differ according to the type of motor imagery. For example, the parietal lobe is activated similarly in both kinesthetic and visual imagery, but there are observable variations in motor and visual centers [29–30]. It is therefore necessary to differentiate and correctly instruct the different modalities of MI depending on the intended activation.

#### **6. VR parameters to optimize results**

With the assumption that VR can be an effective tool to influence MN and thus motor function, the question arises on what parameters the VR used should meet.

Perez-Marcos [31] talks in his overview of VR technology about four qualities of VR environments: immersion, interaction, sensorimotor capabilities, and illusion. Immersion is fundamental potential advantage of 3D VR systems. However, it is not just about the type of projection, but about the overall way in which the virtual environment is mediated. Immersivity can also be supported by other sensory perceptions (e.g., audio, tactile...).

Above all, the possibility of interaction increases the fidelity of the experience. Nevertheless it seems that the immersiveness induced by the use of appropriate inputs can, over time, "burn out" if there is no opportunity to interact with the virtual environment. The simplest form of the interaction is said to be the response of the image to the movement of the head—by looking around in the virtual environment. Notwithstanding it can be extended to include for example image response to an observer activity or, in the case of robotic systems, mechanisms using biofeedback.

Sensorimotor interactions allow for another "layer" of interaction with the virtual environment. One of the top forms is the mentioned biofeedback (e.g., EMG-driven exoskeleton), or the mediation of specific tactile sensations related to our activity in the projected image. In practical applications, it is usually a vibrating game system controller. More advanced sensorimotor response can be provided by some robotic systems.

In the context of VR, illusion is the last "stage" in the quality of the environment, including all the previous ones. An ideal VR system would be able to provide such a high immersiveness, such a high level of interaction and such faithful sensorimotor information, that it would be possible to fully feel and fully "trust" in one's presence in a virtual environment.

Wenk et al. elaborated, in their comparison of the different VR principles, the difference between immersive (3D) virtual reality (IVR) and 2D VR (screen) as to an impact on the movement quality as assessed by the motor and cognitive tests. The study participants placed objects on the marks in the virtual environment while counting them. During the test, task duration, straightness of trajectory of movement, speed of movement, and cognitive load were measured. In the IVR environment, compared with the 2D VR, the tests were performed faster (ES [0.7519]) and with a more direct trajectory (ES [0.7194]) [32]. And Panek et al. described lower brain activity during 2D VR observation compared with observing therapist performing the movement. These findings seem to suggest that the higher the immersion, the higher the activity [33].

#### **7. Suggestion of VR for motor training via AO**

As a consequence of the abovementioned findings, we argue it is possible to suggest principles for VR implementation to the clinical practice. First of all, the chosen system should provide the highest possible level of immersion possible. The use of 3D VR systems over 2D VR is therefore preferable. The video chosen for the intervention should be made in such a way that the 3D environment presented provides the most "real life experience" possible - "first person" video format is preferable over thirdperson game animations. The movements chosen for the AO should be presented specifically and simply enough so that observers can relate to their execution—e.g., grabbing a ball in the video is preferable over the video of painting a picture on canvas.

With abovementioned principles, it is theoretically possible to start using VR as stand-alone system for AO, without the use of interactive system. Although the implementation of interactive component is arguably beneficial (at least to the brain activity), the use of VR for AO poses possibility to intervene in patient cases, where an active cooperation is (for whatever reason) not possible.

*Possibility of Using a VR System as an Action Observation Therapeutical Technique DOI: http://dx.doi.org/10.5772/intechopen.105579*

#### **8. Conclusion**

In this article, we aimed to summarize the principles involved in action observation via VR system used as a stand-alone action observation training device. Although the published studies indicate that in many cases (e.g., balance tests, coordination skills, etc.) the implementation of interactive component is arguably beneficial (at least to the brain activity), the use of VR for AO poses possibility to intervene in patient cases, where an active cooperation is (for whatever reason) not possible. With the information gained from our literature research, we are suggesting the parameters for VR video suitable for AO training. Although more research and thorough clinical trials for this principle are definitely needed, the use of 3D VR without interactive component involved seems to pose an interesting opportunity for implementing relatively new and attractive technology to increase efficiency of standard therapeutical approaches.

#### **Acknowledgements**

Written as part of project: SVV 260599 2020 -2022, PROGRES, Cooperation 2022 - 2026.

#### **Conflict of interest**

The authors declare no conflict of interest.

#### **Author details**

Jaroslav Langer1 \*, Monika Šorfová1 and David Ravnik<sup>2</sup>

1 UK FTVS, Prague, Czechia

2 Faculty of Health Sciences, University of Primorska, Slovenia

\*Address all correspondence to: jarosl.langer@gmail.com

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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