Background
Motor impairments are a common consequence of stroke and a major cause of disability [
1]. Specifically, upper limb paresis is among the most significant deficits and represents an important obstacle for independence [
2]. Impairment of upper limb motor function is present in more than 80 % of stroke survivors, and moderate dexterity after six months is only expected in 30 to 40 % of the cases [
3].
It is commonly assumed that recovery of motor function after a brain injury involves neural reorganization of spared areas in both hemispheres to take over functions previously driven by the injured areas [
4]. In fact, brain plasticity and behavior are interrelated: on one hand, behavior is a result of reorganized brain activity [
1,
4]; on the other hand, adaptive neural reorganization is driven by skill-dependent experiences and behavior [
4]. Nevertheless, reorganization is not driven by mere repetition. It only occurs when the experience implies learning [
4]. Therefore, it can be deduced that motor rehabilitation should focus on driving plasticity by experiences that mean a challenge for the motor skills of the patients. In addition, motor learning principles, such as intensity, repetition, task-orientation, and feedback have proven to modulate the functional improvement after stroke [
5‐
9].
Virtual Reality (VR) is an especially interesting research field since it allows to create computer-generated environments and provide customized experiences involving different sensory channels, commonly sight, hearing, and/or touch [
10]. An increasing number of studies report promising results of its application to motor rehabilitation after stroke [
10,
11], specifically for upper limb [
11‐
13]. First, movement kinematics when reaching, grasping, transporting, and releasing objects in a virtual environment are comparable to those in the physical world, thus suggesting that the training of arm movements in VR can be a feasible alternative [
14]. Second, VR has been shown effective at improving upper limb movements for reaching and grasping tasks involving proximal segments and global arm movements, in individuals with stroke in both acute and chronic stages [
11,
13]. Third, distal fine motor control has also been effectively improved using VR, generally combined with robotic-like devices [
2,
15,
16]. Fourth, controlled trials suggest that VR may be beneficial to improve upper limb function and performance in activities of daily living, to a greater extent than same dosage of conventional therapy [
3]. Finally, mixed-reality systems involving virtual and tangible objects may be useful in improving both functionality and the kinematics of reaching [
17,
18]. Mixed-reality systems are particularly interesting because they combine interesting features of VR with tangible objects that subjects must manipulate. For instance, proprioceptive feedback has been suggested to exploit multimodal aspects of the observation of goal-oriented movements and the feedback on one’s actions [
12]. However, clinical research so far with these systems has mainly focused on shoulder and elbow training without specific involvement of hand and finger dexterity.
Basing on the existing evidence, we have developed a mixed reality system that satisfies the motor learning and neural plasticity principles to promote the rehabilitation of task-directed movements of the paretic upper limb involving hands and fingers. The system fits the motor condition of each subject allowing the training of a wide spectrum of movements, from gross proximal movements to finger dexterity, while being portable and inexpensive, in contrast to robotic systems. The objective of this paper is twofold: first, to determine the clinical effectiveness of an experimental intervention with the system to improve the motor function of arm, hand, and fingers in individuals with chronic stroke; and second, to determine the acceptance of this intervention as defined by users’ ratings of usability and motivation.
Discussion
This study evaluates the effectiveness and acceptance of a low-cost mixed reality instrument that provides intensive task-oriented exercises for arm, hand, and finger function rehabilitation in a population of chronic stroke survivors with hemiparesis. Positive effects of the experimental intervention were detected in both activity and participation, and also influenced the progression of the participants.
The significant improvement in timed tests related to activity after the experimental intervention must be highlighted, since task performance is considered an indicative of functional improvement in individuals with chronic stroke [
36], and since movement speed and quality of movement are interrelated [
37]. Our results supports previous findings using mixed reality systems in the Wolf Motor Function Test [
17]. Interestingly, changes detected by the Wolf Motor Function Test have been reported to be of clinical importance [
37]. The strong tendency towards statistical significance detected in the Fugl-Meyer Assessment Scale are also in line with previous reports [
17,
18]. The different nature of this scale and the Wolf Motor Function Test and the chronicity of our sample could have prevented greater effects. This scale has been shown to be more sensitive in the acute phase [
38] and for chronicity of less than six months [
39]. However, it may separate motor recovery from functional recovery and, therefore, may not be responsive to functional improvements in chronic populations [
40]. The Fugl-Meyer Assessment Scale focuses on multijoint upper extremity function and examines synergy patterns that may no longer form the basis of our intervention [
41]. Moreover, it is a 3-point scale and do not differentiate changes in the less affected extremity. In contrast, the Wolf Motor Function Test assesses the performance time involving single joint or interjoint movements, which were frequently engaged in our intervention. The significant improvement in the gross manual dexterity, assessed by the Box and Block Test, could have been facilitated by an improvement in control of the elbow and wrist synergies and the grasping mechanism promoted by the interaction with tangible objects, which supports previous findings [
18]. In addition, the specific training of the flexion and extension of the wrist in different positions and the metacarpophalangeal and interphalangeal joint promoted by our system, could also explain the improvement detected in the Nine Hole Peg Test. It is important to highlight that previous research on stroke survivors involving some robotic systems has shown no improvement after intervention in the Box and Block Test [
12,
42] unless the wrist joint [
43] or finger dexterity [
44] are specifically trained. However, these two last robotic systems failed to provide improvement reflected in the Nine Hole Peg Test, even in acute phase [
45]. This should highlight the benefits of our system, since it can promote hand dexterity, as measured by the Box and Block Test and the Nine Hole Peg Test, while being cheaper and more portable than robotic systems.
Although clinical scales do not allow the ultimate distinction between true recovery and behavioural compensation [
46,
47], the results suggest effective motor learning and motor skill retention derived from the experimental treatment. We hypothesize that the improvement in the clinical condition of the participants could be explained by the nature of the exercises, which satisfied the motor learning and neural plasticity principles. First, exercises were intensive and repetitive, characteristics that have been reported to influence improvement [
5]. Second, they represented meaningful tasks specially designed to address functional activities, which has been reported of major importance for motor rehabilitation [
5,
6] and is known to positively affect arm-hand function recovery and motor control in stroke patients [
46]. Third, augmented extrinsic feedback, a major aspect of motor learning [
6,
8,
46], was provided during the training in the visual, auditory, and tactile channels. Interestingly, auditory augmentation of visual feedback can be beneficial during the execution of upper limb movements [
48]. Fourth, the training drove subject´s attention to the effect of the action, which has been reported to enhance learning [
49]. Finally, the difficulty of the training was particularized to each participant in each session, which is essential for motor learning and neural reorganization [
6,
46,
49]. Previous research has found that functional improvement, which has been associated with cortical reorganization by different neuroimaging studies [
10,
50], can occur at any time [
12,
51,
52]. However, the chronicity of the sample, which ensured that the functional improvement was externally driven by the intervention [
1,
5], could have limited greater improvement. It is important to highlight though that clinical improvement provided by the experimental intervention was retained after the second A-phase, it is, after returning to physical therapy. The practice under varied conditions promoted by the experimental system could have supported this retention, which has been reported as a better indicator of motor learning than the performance during or just after the practice [
6].
The limited results obtained in the body structure and in the body function domains may be related to task-specific effects of motor learning [
5,
46]. In line with the tendency of the last decade to shift the efforts of hand-arm rehabilitation from the function level towards the activity and participation level [
46], the mixed reality system was designed to train specific tasks that imply the use of the affected arm, hand, and fingers, without explicit focus on strength or joint movement. This orientation, together with the discrete nature of the Manual Function Test (with scores ranging from 1 to 4), and, again, with the chronicity of the sample, could have prevented significant improvement in these components.
The positive reports on perception of improvement and on the use of the paretic arm after the experimental intervention evidenced by the Motor Activity Log, and the high scores about usefulness and enjoyment evidenced by the Intrinsic Motivation Inventory, could depict a relationship between acceptance of the intervention and its repercussion to daily life. This fact could be explained by the ability of the system to motivate patients, which would support previous studies [
12,
15,
51,
52]. Importantly, motivation is believed critical for learning [
7,
49], and is considered one of the basic principles that should be satisfied by any rehabilitation approach [
6,
9]. Finding the rehabilitation enjoyable is thought to increase the level of engagement, participation, and compliance [
15], thus increasing the effectiveness of a rehabilitation program.
These results must be interpreted taking into account the limitations of the study. First, the characteristics of the sample are inherently linked to the specialized neurorehabilitation service where the study took place, which could restrict the generalization of the results. Second, no kinematic analysis was performed. Consequently, although compensatory strategies were restricted during the intervention, they were not controlled during the assessment, which could have influenced the performance in the scales and tests. Third, although the physical therapist who assessed the participants’ condition did not know the protocol, the therapists who administered and controlled the intervention were not blind. Fourth, the requirements of the system could restrict interaction of some individuals. Participants were required to have enough motor control to actively move the hemiparetic arm, hand, and fingers along the table and enough cognitive and communication skills to understand and follow instructions. Finally, the sample of the study (n = 30) actually can be considered as a small sample, which can also limit the extrapolation of the results.
However, the improvement detected in our sample supports the clinical effectiveness of mixed reality interventions that satisfy the motor learning and neural reorganization principles to improve upper extremity motor ability and finger dexterity in chronic stroke survivors. The effectiveness of the system together with its low cost, its portability, and its acceptance could promote its integration in the clinical practice as an alternative to more expensive systems, such as robotic instruments.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
All the authors designed the study and interpreted the results. In addition, CC and EN contributed to the data acquisition, and RL and MA designed the hardware and software components of the system. All the authors have revised the manuscript and have given their final approval for publication.