Abstract
This paper aims to present previous works in augmented sensory guidance for motor learning and psychophysiological factors and contextualize how these approaches may facilitate greater optimization of motor rehabilitation after neurotraumas with virtual reality. Through library resources at Stevens Institute of Technology, we searched for related works using multiple electronic databases and search engines with a medical focus (detailed in the paper). Searches were for articles published between 1980 and 2023 examining upper extremity rehabilitation, virtual reality, cognition, and modes and features of sensory feedback (specific search terms detailed in the paper). Strategic activation of sensory modalities for augmented guidance using virtual reality may improve motor training to develop further skill retention in persons suffering from impulsive neurological damage. Features with unique motor learning characteristics to consider with augmented feedback signals include representation, timing, complexity, and intermittency. Furthermore, monitoring psychophysiological factors (e.g., sense of agency, cognitive loading, attention) that represent mental and psychological processes may assist in critically evaluating novel designs in computerized rehabilitation. Virtual reality approaches should better incorporate augmented sensory feedback and leverage psychophysiological factors to advance motor rehabilitation after neurotraumas.
Similar content being viewed by others
1 Introduction
1.1 Problem and significance
Neurotraumas (e.g., stroke, spinal cord injury, and traumatic brain injury) affect millions of people annually and are among the leading causes of death and disability [1,2,3]. Affected individuals are frequently limited in mobility and must regain critical skills for independence and performing activities of daily living [4]. It is estimated that 50 percent of spinal cord injury cases involve upper extremity dysfunction [3], and about 65 percent of stroke survivors cannot use their affected hand for up to six months after the injury [5]. Thus, it is crucial to identify and deploy new forms of physical therapy after neurotrauma that will rehabilitate functional abilities effectively and quickly. Several classes of pathologies can benefit from novel therapies to rehabilitate motor function, including systemic diseases (e.g., Parkinson’s Disease [6]) and developmental disabilities (e.g., Autism Spectrum Disorder [7]). However, rehabilitation after neurotrauma is a special case to consider [8] as functional or cognitive deficits generally improve with sufficient time and proper management, yet negative sequelae from mild neurotraumas can persist as lifelong impairments [9]. This paper aims to contextualize how novel therapies with computerized interfaces, such as virtual reality, can specifically be optimized with cognitively-centered approach elements (e.g., augmented sensory feedback for motor learning, adapting training based on monitored psychophysiological measures) for persons rehabilitating upper-extremity motor function after neurotraumas. However, several of the proposed considerations can be reasonably extended to other pathologies benefitting from physical therapies to improve motor function.
1.2 Virtual reality motor rehabilitation – why it works, how to optimize
Computerized interfaces are increasingly prevalent for rehabilitation, given their features of programmability and flexibility to customize approaches for each user to achieve greater efficiency and engagement. Virtual reality is highly viable in motor rehabilitation since it can facilitate task-oriented movements while augmenting sensory activation. Furthermore, virtual reality paradigms can be programmed to accommodate various levels of movement ability and include gamification elements for greater engagement [10]. Previous studies have demonstrated benefits with virtual reality rehabilitation alone and when combined with traditional therapies [4, 11]. The apparent advantages of virtual reality approaches include greater motivation, engagement, and convenient repetition for the high-fidelity practice of functional movements [11]. However, empirical research has yet to demonstrate precisely how virtual reality mechanistically generates positive outcomes. While improved motor function is the primary metric of interest, psychophysiological factors such as motivation and engagement are crucial in facilitating effective motor rehabilitation. Thus, it is critical to consider how cognitive elements may be explicitly incorporated to optimize virtual reality motor rehabilitation. Although virtual reality therapies have already demonstrated promising results, more empirical research must be conducted to understand and leverage their underlying mechanisms.
It is unclear how programmable virtual reality elements (e.g., task type and complexity, environment, delivery of sensory guidance) can generate better motor control. Recent studies examining virtual reality for motor rehabilitation have explored factors of convenience [12], adaptability [13, 14], quality of motion control [15], and level of immersion[16, 17]. However, it is not evident how we can further optimize the design and deployment of virtual reality protocols for greater functional benefit beyond the motivation to undergo more training repetitions. Ultimately, it would be invaluable to understand how specific modifications to virtual reality design and training elements produce cognitive connections that directly support improved motor outcomes. Such findings would elucidate the benefits of virtual reality beyond motivation. Furthermore, these findings would incentivize the development of intelligent virtual reality approaches that may accelerate positive motor outcomes.
Despite the plethora of options to customize computerized interfaces, virtual reality rehabilitation approaches mainly rely on colorful, gamified displays to incentivize more practice repetitions. Advanced principles for motor learning and motor control are still not standardly considered in designing and deploying virtual reality protocols [18]. However, virtual reality environments allow for creating various complex functional tasks, providing sensory guidance cues, and real-time monitoring of user variables to adapt training. Furthermore, virtual reality platforms can provide highly stimulating visual, auditory, and haptic interfaces to guide users to perform complex motor functions more effectively. Thus, virtual reality environments can readily facilitate the greater cognitive engagement necessary to accelerate improvements in motor function further.
Recent literature reviews have specifically suggested how various VR-supported exercise therapies can effectively improve motor rehabilitation outcomes for upper extremity function [19,20,21] after stroke. Recent studies have also suggested how VR therapies produce measurable changes in neural activity, as measured by fMRI [22], and can be coupled with emerging approaches, e.g., action observation therapy [23], whereby patients observe purposeful action to be subsequently imitated while engaging multiple sensory modalities.
1.3 Objective of review paper
The primary objective of this paper is to review the literature relevant to identifying and exploiting cognitive-based approaches to motor rehabilitation with computerized interfaces for persons with neurotraumas. Furthermore, this review paper focuses on rehabilitating upper-extremity functions, given their broad use in daily activities, less stereotypical nature than common lower-extremity functions (e.g., gait), and common focus in rehabilitation after severe neurotraumas. Through relevant literature, this paper will suggest ways to maximize the potential of upper-extremity rehabilitation after neurotraumas through cognitive-level modulation via computerized feedback.
1.4 Literature review search methods
Through library resources available at Stevens Institute of Technology, we searched for articles and book chapters describing relevant studies associated with virtual reality rehabilitation in the following databases and related search engines: PubMed (MEDLINE), Web of Science, Scopus, ScienceDirect, SpringerLink, Wiley Online Library (Cochrane Library), and Google Scholar. Our search was restricted to articles between 1980 and 2023. Our primary search terms, pursued independently and in combinations included: “virtual reality,” “motor rehabilitation,” “stroke,” “spinal cord injury,” “traumatic brain injury,” “neurotraumas,” “augmented sensory feedback,” “multimodal feedback,” “intermittent feedback,” “terminal feedback,” “sense of agency,” “cognition,” “cognitive load,” “motivation,” “attention,” “reaction time,” “memory,” “upper extremity function.” Additionally, we reference our own recently published or submitted works. Given this is an “opinion/perspective” review paper attempting to contextualize new, in some ways non-traditional, approaches to virtual reality rehabilitation, no statistical meta-analyses were applied to the review results. Rather we summarize works emanating from the above literature searches and make recommendations of how elements of these studies may be innovatively applied to motor rehabilitation paradigms using computerized interfaces such as virtual reality.
1.5 Organization of review paper
This paper will first review training approaches for upper-extremity motor rehabilitation in Sect. 2, especially those employing virtual reality, as established by previous studies. Next, and more critically, in Sects. 3 through 5, we will review and relate literature from motor control learning and psychology to suggest cognitive bases to optimize virtual reality motor rehabilitation. The primary areas of discussion include: 1) how activating sensory modalities through computerized interfaces for feedback can be leveraged to accelerate motor rehabilitation outcomes, 2) how features in augmented sensory guidance can optimize motor outcomes, and 3) how certain psychophysiological factors should be further considered in the development of new virtual reality rehabilitation protocols.
2 Upper-extremity motor rehabilitation
2.1 Traditional rehabilitation of upper-extremity function after neurotraumas and the role of motor learning
Conventional rehabilitation strategies use exercises to improve the motor skills needed to perform daily activities. A physical or occupational therapist will supervise and guide rehabilitative practices for people with motor impairments [4, 24]. These professionals implement repetitive task training to reformulate neuromotor connections and to increase strength, range of motion, and coordination [3]. Cervical-level spinal cord injury and stroke can result in upper-extremity paresis that compromises the ability to reach and grasp [7]. Conventional therapies for rehabilitating upper-extremity function after spinal cord injury typically include joint exercises that facilitate greater strength, dexterity, and range of motion [24, 25]. Stroke rehabilitation typically centers on functional task practice [26], adjusting difficulty levels for each person. This training entails rigorous practices that improve motor skills transferrable to functional tasks. Persons can also receive task-specific training [27, 28]. For eligible persons with hemiparesis, therapists may incorporate constraint-induced movement therapy to compel more engagement of the affected side [29]. Unfortunately, less than one-third of stroke or spinal cord injury survivors receive outpatient rehabilitation [30]. Participation in regular rehabilitation is challenged by the effort and time involved in physical therapy. Conventional rehabilitation can frustrate patients due to its tedious and repetitive nature [4]. Ancillary factors that reduce outpatient treatment are lack of access to rehabilitation centers, family/caregiver support, and the financial resources to pursue regular physical therapy. Thus, rehabilitation methods must be designed to be highly efficient, whereby participants can achieve functional gains with fewer repetitions or exposures to therapy.
Since the primary goal of upper extremity rehabilitation following a spinal cord injury or stroke is to regain motor control, most rehabilitation paradigms implicitly incorporate motor learning. Motor learning involves the development of intrinsic mechanisms, such as neuromuscular control, to repeat a movement independently [31]. This motor training objective naturally relates to reformulating neural connections following neurotraumas for motor recovery [32, 33]. Practical training for motor tasks is often executed in two phases. The first phase is guided training, where feedback is provided in real-time or immediately after task completion. The second phase is retention, where guidance feedback is removed, and participants must perform the task independently and ecologically [34]. High performance during training ensures the participant's capability to do a given motor task well; however, only with high performance during retention is there demonstrable development of intrinsic mechanisms. Transfer tests can further indicate long-term learning whereby a task is presented during a retention test different from training but still leveraging the motor skills practiced during training [34]. Traditional physical therapy approaches aim for the successful transfer of skills through the development of motor skills during training to facilitate improved performance of activities of daily living. However, guidance during conventional rehabilitative training does not typically consider the presentation of augmented feedback intended to maximize retention outcomes.
There are inherent theoretical trade-offs between training and retention repetitions of movement. For example, the guidance hypothesis suggests that higher reliance on feedback during training can negatively affect motor learning retention [35, 36]. This phenomenon has been evaluated by altering the frequency of feedback trials as motor learning improves. Physical therapy methods could better cognitively engage participants during rehabilitation if programmable and customizable tools are enacted that leverage motor learning processes and make motor rehabilitation more efficient.
Many traditional rehabilitation exercises do not precisely simulate daily activities but focus on developing capabilities (e.g., strength, dexterity) that transfer to functional tasks. On the other hand, virtual reality paradigms can provide environments and tasks that have high fidelity, on physical and cognitive levels, to the user in simulating activities of daily living [11]. Consequently, patients may achieve more direct gains in relevant functions more quickly. Furthermore, virtual reality rehabilitation tasks can be more motivating to perform, easier to adjust on the fly, and convenient to repeat [37]. Through programmability, virtual reality tasks can be readily gamified or uniquely immersive to incentivize participation, and they can be customized on more granular levels in terms of adapting difficulty or modifying the task at hand [38, 39]. Such approaches can reduce the onus on clinicians being another human-in-the-loop to customize the training regime and focus more on supporting, guiding, and directing the patients at a high level. Furthermore, virtual reality can be used effectively in isolation or in combination with traditional therapy to maximize outcomes [11, 40, 41]. Thus, although conventional rehabilitation alone is effective, it is limited in its scope compared to virtual reality to customize training for greater motivation, efficiency, and convenience [42]. Ultimately, participation in motor rehabilitation therapies relies on users feeling cognitively engaged and experiencing more reliable gains in motor outcomes. Computerized interfaces, such as virtual reality, can further customize treatments to accommodate current levels of function and conduct training regimes that accelerate functional gains.
2.2 Virtual reality for motor rehabilitation
Advanced rehabilitative methods increasingly utilize computerized interfaces such as robotics and virtual reality to provide enhanced sensory feedback and gamification [43, 44]. Virtual reality rehabilitation is an attractive alternative to conventional therapy due to customizability and contextual incentives (e.g., in-game rewards) that foster greater motivation and engagement [45]. Programmability features allow finer adjustments of difficulty levels for each user and better simulation of activities of daily living for functional fidelity [11]. Virtual reality rehabilitation is also increasingly prevalent due to its commercially available and affordable technologies for home practice that can supplement the work done with a physical therapist [12]. Various virtual reality approaches have been utilized for persons with either spinal cord injury [4, 33, 41, 46] or stroke [47,48,49,50,51,52,53,54,55,56,57]. These studies demonstrate the effectiveness of virtual reality paradigms in improving motor function through methods that motivate greater participation in therapy. The primary objective of virtual reality therapies is to show improvement in functional capabilities. Brosnan et al. (2009) demonstrated how virtual reality therapy addressed motor deficits after stroke patients by encouraging the use of the hemiplegic side of the body while also increasing satisfaction, motivation, and interest in physical therapy [52].
Although virtual reality therapy has positively affected motor rehabilitation, it is unclear whether it is more effective than conventional therapy when controlling for dosage. A fair comparison can only be made when the therapy dose is similar in duration and intensity. Supplementing traditional rehabilitation methods with virtual reality therapy conclusively improved functional outcomes [4, 53]; however, the mechanism of improvement is likely attributable to increased dosage. Indeed, patients report greater enjoyment of therapy with virtual reality as it encourages greater participation in rehabilitative practices [54]. However, we assert there is still a missed opportunity in that virtual reality therapies could be better designed to incorporate sensory feedback and psychophysiological factors to outperform conventional approaches further. Therefore, it is necessary to consider further and investigate the incorporation of augmented guidance to facilitate motor learning and psychophysiological factors to verify neural engagement in virtual reality rehabilitation (Fig. 1).
3 Activation of sensory modalities for motor rehabilitation
3.1 Visual feedback in virtual reality
Visual feedback is the most valuable and exploitable sensory modality in virtual reality. Visual feedback provides cues about task performance, such as body position or muscle activity, either in real-time or immediately following task completion. Visual feedback guides spatial positioning during movement tasks more effectively than audio or haptic feedback [55, 56]. Supplementary visual cues in virtual reality can improve the performance of isometric and dynamic exercises [57], and explicit visual cues about one’s spatial position can immediately reduce errors in a movement trajectory [58], including with virtual mirrors [59]. However, when virtual reality paradigms enhance visual presentations for immersion and gamification, the user’s capacity to receive additional visual guidance to improve performance should be carefully considered. Task-irrelevant immersive elements, such as extra objects within view or visual rewards for a more gamified context, can detract from the task-relevant intention (e.g., memory) of a visual stimulus used for guidance [60]. How visual feedback is best presented can also depend on participant experience and task complexity [61].
For persons recovering from neurotraumas, learning control schemes for brain-computer interfaces can be highly predicated on visual feedback, contingent on high attention [62]. Although this example is for an assistive device system, the ability to improve control, even if independent and voluntary, over a computerized interface such as virtual reality is highly prevalent for demonstrating functional gains for rehabilitation paradigms. Furthermore, there is growing evidence to suggest that if key neurocircuits are therapeutically reactivated with appropriate sensory feedback, neurological functions (e.g., limb movement, locomotion, etc.) can be better reanimated after neurotrauma [63, 64].
3.2 Multimodal sensory feedback for guiding motor tasks
Multimodal feedback entails the provision of augmented guidance cues through multiple sensory modalities (e.g., visual, auditory, and haptic) concurrently to enhance motor task performance and rehabilitative benefits [57] (Fig. 2). During physical rehabilitation, multimodal feedback, when adding audio or haptic cues to visual feedback, enhances complex motor learning compared to unimodal sensory feedback [65]. Furthermore, visual-audio and visual-haptic forms of multimodal feedback are especially beneficial for increasing perceptional accuracy and spatiotemporal learning [57], leading considerations to optimize motor practices within virtual reality environments. We consider visual-audio and visual-haptic pairings in greater detail in the following sub-sections.
In general, multimodal sensory feedback has only been employed anecdotally for neuromotor rehabilitation [57]. While sensory-driven platforms have been developed to recover function, like post-stroke goal-directed reaching [66], there is a clear opportunity for deeper investigation when employing highly customizable and programmable platforms like virtual reality. The notion of multimodal approaches to neuromotor intervention is identifying multiple pathways in which to elicit more neural activation during training. Multimodal neural activation with augmented sensory feedback [67] through virtual reality [68] is a potentially promising pathway that has not been well tapped for rehabilitation after neurotraumas.
3.2.1 Adding haptic cues to visual feedback
Haptic feedback broadly encompasses any sensation related to touch. Examples include changes in applied forces, pressure, vibration, or temperature to relay signal information (e.g., amplitude and frequency [69].) related to task performance or the surrounding environment. Haptic feedback can be repulsive or attractive in cueing error magnitudes [70]. Haptic feedback is also effective in encoding supplementary information (e.g., force interactions) that facilitates user integration with movement-restoration devices, such as motor-actuated prostheses [71, 72]. In these cases, visual feedback is fundamental to informing the user about functional performance, and haptic feedback concurrently provides accompanying task information (e.g., errors, forces). Receiving augmented cues about task-related performance (e.g., encoding errors in performance) in real-time entails explicit feedback from which users constantly modulate their actions according to this feedback to guide performance [73].
The effectiveness of adding explicit haptic (e.g., vibration, forces, imposed motions felt proprioceptively, etc.) feedback to visual cues for virtual reality motor rehabilitation tasks will depend on factors ancillary to the training. These factors include task type, task complexity, user functional abilities, and user experiences with exercise activities. The challenge with adding explicit haptic feedback stems from possible cognitive overloading, especially if tasks are sufficiently simple to be mastered with visual feedback alone. For example, Hasson and Manczurowsky (2015) determined that vibration did not improve skill acquisition with a simple upper-extremity task if presented independently or with visual feedback [74]. Their results concluded that vibrotactile feedback was detrimental when participants had difficulty integrating the haptic cues with the viewed virtual avatar. Thus, to maximize potential rehabilitative benefits with explicit haptic feedback, the specific characteristics of the task and user must be carefully considered.
Alternatively, implicit haptic feedback, which is not directly guiding task performance, is intended to impact user engagement and actions in motor rehabilitation. Within virtual reality environments, implicit haptic feedback is typically employed for greater immersion or better simulation of physical interactions. Occasionally, haptic feedback is provided without real-world fidelity but simply for greater user engagement through sensory substitution. In this approach, one sensory modality (e.g., pressure) is translated into stimuli for another sensory modality (e.g., vibration magnitude). While not as ecologically valid, such approaches can foster greater immersion toward improved training outcomes [58].
3.2.2 Adding audio cues to visual feedback
Auditory feedback involves converting data produced by user activity [75] into additional sound cues (sonification) readily provided through virtual reality interfaces or wearable systems. As with haptic feedback, audio feedback can be readily coupled with augmented visual inputs used as an implicit or explicit learning tool [76]. With implicit learning, real-time sonification is provided independently of any reference. Explicit learning would entail the sonification of performance errors between the user’s movement and a target. Ultimately, audio feedback is only helpful for motor learning if the sound cues are consistent and timely [77]. Thus, any technical limitations that delay processing time can significantly limit the effectiveness of audio-based approaches for motor rehabilitation.
Augmented auditory feedback receives less attention than visual and haptic feedback with motor rehabilitation approaches, given its potential as a unique cognitive distractor [78]. However, the influence of auditory feedback on motor learning should not be discounted when designing virtual reality rehabilitation platforms. For example, in clinical stroke populations, it has been shown that audio feedback can make rehabilitation exercises more engaging for the participants, resulting in improved mobility and reduced reports of pain [79]. In addition, melodic sonification is proven to increase retention rates [80]. Positive emotional responses can emanate from sounds, especially music. Still, if the sound is not employed naturally for the motor task or the specific user, it may generate adverse motor responses [81]. These results motivate the inclusion of audio feedback in motor rehabilitation programs; however, careful considerations should be made in how auditory feedback is incorporated.
Virtual reality rehabilitation often includes auditory and visual components, and studies have directly compared the two modalities. Using functional magnetic resonance imaging, auditory and visual learning are shown to activate different brain areas when subjects perform the learned task without the stimulus present [82]. This result suggests that the design of a sensory-based motor learning method should consider the location of neurological damage. Concurrent audio and visual feedback can also improve the subject’s engagement and result in greater margins of improvement than either feedback modality individually [83]. While audio can be a helpful tool to enhance virtual reality rehabilitation methods, the feedback protocol should carefully consider customizing sound cues based on individual-level responses to accelerate motor learning trajectories [84,85,86].
4 Features of augmented sensory feedback used for training guidance
When utilizing programmable computerized interfaces for rehabilitation, there are several options for presenting augmented sensory feedback to those with neurotraumas. Persons with neurotraumas may have limitations in carrying a particular cognitive load [87, 88], which would dictate what levels of augmented sensory guidance would be optimal. On the other hand, additional sensory cues may be helpful to elicit greater arousal and attentiveness during training in the presence of neurotraumas [89]. While virtual reality can generate intricate and highly interactive environments with various sensory cues, it is unclear what additional information should be provided to enhance the learning of motor tasks. Since virtual reality readily allows personification elements with virtual avatars, the natural question is: what additional, sensory-based guidance can and should be provided to accelerate functional motor outcomes?
4.1 Simple versus complex feedback
Another feature to consider in augmented guidance is the presented feedback signals' complexity. Typically, feedback complexity will follow the complexity of the motor task [61]. For example, Wulf and Shea (2002) defined simple tasks as those capably learned in a single session or involving only a single degree of freedom. Conversely, complex tasks have multiple degrees of freedom, requiring numerous training sessions to master, and are more ecologically valid [61]. In prescribing visual feedback complexity, simple feedback provides a single DOF or performance variable. In contrast, complex feedback provides two or more streams of information [58]. Sanford et al. (2020) identified a trend in which concurrent complex feedback can be more valuable than simple feedback when provided in body-representative display modes [58]. Virtual reality may amplify these results, whereby elaborate virtual avatars can enhance embodiment [90] and sense of presence [91]. Complex feedback may be used even for relatively simple tasks if the body segments are constrained, e.g., squat maneuver with feet creating kinematic closed-chain to the ground [58, 92]. In this way, even a multi-segmental motion will effectively follow a single degree-of-freedom (e.g., squat depth). However, tracking multiple segments concurrently with complex feedback would still be highly feasible if not beneficial to performing the movement [58]. Given the complex nature of upper-extremity tasks (e.g., reach-to-grasp), complex feedback is expected to be most effective. Virtual reality training of complex tasks often displays a target image of a total body linkage or hand, with multiple segments and joint DOFs indicated against an entire user-generated body position. In this way, complex and representative feedback modes are again naturally coupled. Importantly, providing inappropriately complex feedback can cause cognitive overload and likely involves information irrelevant to the task or desired skill [93].
4.2 Abstract versus representative feedback
Previous studies with computerized interfaces have shown abstract feedback, displaying movements against targets as line plots or bar graphs [94] with no body-discernable features. Abstract feedback is often associated with simple tasks [61]. Representative—also known as natural— feedback uses virtual avatars or mirrors of the participant's body position and is related to complex feedback [57, 58, 92]. Abstract feedback is typically used with simple tasks since it requires only one performance variable to track, and a single trace readily represents it. Representative feedback is more associated with complex movement tasks [61], as displaying multiple performance variables concurrently as disjointed lines or graphs is neither sustainable nor informative. When developing virtual reality rehabilitation paradigms, displaying performance errors representatively and across multiple degrees of freedom (i.e., for complex function) can immediately improve motor performance [58]. An example of abstract versus representative feedback for visual guidance of two-legged squat kinematics [58, 92] is shown in Fig. 3. With abstract feedback, the participant is shown sinusoidal trajectories to track using dynamic traces that change with the angular motions of the participant’s body segments while performing the squat. With representative feedback, those same angular trajectories are displayed in real-time with a sagittal-plane view of two overlaying dynamic stick-figures, one that moves according to the participant’s squat motions and the other adhering to the target trajectories the participant should match.
Complex-representative visual feedback involves concurrently displaying multiple performance variables projected onto a multi-segment avatar the user can embody, including virtual reality interfaces driven by myoelectric commands [95]. For example, Blana et al. (2016) developed a virtual reality prosthesis training system, integrating motion capture and EMG control to display a transparent guide arm against an opaque avatar actively controlled by participants [96]. This approach facilitated relatively fast training for users to complete 3D-reaching tasks without adverse effects. Complex-representative feedback can exist in the first- or third-person perspective. Perez-Marcos et al. (2017) conducted a pilot study with stroke patients to demonstrate the beneficial effects of virtual reality rehabilitation on upper extremity function and range of movement with multiple tasks projected in either first- or third-person displays [97].
Although abstract feedback is classically associated with simple tasks, abstract motor tasking coupled with cross-training elements can induce positive cognitive outcomes [98]. Aoyagi et al. (2019) showed that adding weights during a figure-8 tracing task with upper-extremity motions increased the perception of agency. Few studies have evaluated abstract feedback within virtual reality immersive environments due to the natural match between complex-representative feedback and body avatars. However, if intelligently designed to feel natural and complementary to the virtual avatars being controlled, with or without a sense of embodiment, simple and abstract feedback to depict target motion paths may still be effective in training better motor performance, even within sophisticated virtual environments.
Integration of abstract and representative cues is readily done in virtual reality. A previous study merged non-motor abstract cues (e.g., words, color changes) with representative guidance of motor actions in the form of various hand gestures (e.g., wrist deviations, hand pronation/supination, different grip configurations, etc.) [99]. As another example, color changes as abstract cues can highlight target areas of interest during full-body movements primarily guided by complex-representative feedback [100]. While participants utilized complex-representative feedback to match target body positions, the color changes successfully reinforced performance errors. Hybrid feedback approaches that cognitively engage users without distraction during rehabilitative training should be further investigated for their potential to improve motor outcomes.
4.3 Concurrent versus terminal feedback
Another essential feature to consider with augmented guidance in virtual reality motor rehabilitation is the timing of the feedback. Concurrent feedback is provided in real-time to guide the user toward target positions while performing the movement simultaneously [57]. Terminal feedback is provided immediately after completing the movement to summarily indicate performance errors about the previous movement in preparation for the next training repetition [57]. Both concurrent and terminal feedback can present identically and be similarly identified along particular feedback features (i.e., degree of complexity, rate of intermittency, level of body representation). The key difference is receiving real-time feedback while moving (concurrent) versus observing a replay of the feedback that would have been observed in real-time but after movement completion (terminal). Motor rehabilitation may incorporate concurrent and terminal feedback simultaneously [101] or transition from concurrent to terminal over a long period as the participant's motor learning improves [102]. Concurrent feedback is most beneficial in the early stages of motor learning when the person is relatively naïve to the task, making more significant adjustments and more considerable gains in performance [102]. Terminal feedback becomes beneficial in the latter stages of motor learning when only finer adjustments are made while improving long-term learning [102]. Thus, the optimal timing in providing feedback will be dictated by where one is in the motor rehabilitation learning cycle.
4.4 Continuous versus reduced frequency (intermittent) feedback
This section will discuss feedback frequency, or intermittency, as a fourth feature in designing optimal virtual reality rehabilitation protocols with augmented guidance. As referenced previously (Sect. 2.1), participants of motor learning protocols can accelerate the development of independent capabilities by reducing feedback frequency over an extended course of training [35, 36]. This approach aims to reduce the reliance on sensory feedback to support the higher performance of movements. The three primary methods to employ reduced frequency training are bandwidth [103,104,105], faded [106], and self-paced [107,108,109]. All three methods have been evaluated positively with terminal feedback, but only bandwidth feedback has been proven effective when coupled with concurrent feedback [92, 110]. For intermittent feedback training based on bandwidth performance, feedback is only provided when the participant’s performance errors (e.g., in tracking a target trajectory) exceed a pre-set error magnitude (i.e., error band) [92, 111]. Figure 4 presents example time-stamped trajectory tracking with continuous versus intermittent (bandwidth) feedback. Thus, there is an implicit reward to perform well, i.e., maintaining low error levels, by observing a removal (disappearance) of feedback, which also promotes greater reliance on intrinsic mechanisms. In a study not employing virtual reality, bandwidth feedback demonstrated greater potential for learning than continuous feedback for the two-legged squat exercise [92]. Further research is necessary to determine the boundaries of feasibility and optimality in employing concurrent bandwidth feedback with virtual reality applications, especially for ensuring better long-term outcomes.
5 Psychophysiological factors in motor rehabilitation
Although any form of motor training inherently accesses cognitive resources, most conventional methods for physical therapy do not strategically consider psychophysiological factors in motor rehabilitation processes. Advanced rehabilitative methodologies employ computerized interfaces, including robotics [112] and virtual reality [113], for improved motivation and motor performance. However, as previously mentioned, if the dosage is similar, the added benefits of computerized rehabilitation approaches compared to traditional therapies become more negligible [114]. Thus, it remains uncertain whether current methods with virtual reality induce the neural engagement necessary to improve motor outcomes efficiently. As discussed, computerized rehabilitation offers several design options to engage users, including gamification [115], customization [116], and augmented feedback [117]. However, how we can best assess whether specific virtual reality rehabilitation designs will result in desirable neural engagement is unclear. This section discusses potential psychophysiological factors that should be monitored to gauge engagement in improving motor performance (Fig. 5).
Psychophysiological measures must be monitored for those with neurotraumas to assess bodily functions that directly impact health and quality of life. For example, spinal cord injury can result in various autonomic dysfunctions that increase mortality from cardiovascular and respiratory disease [118]. Thus, persons with neurotraumas may have unique responses to variations in training guidance that are readily measurable from skin-surface recordings, especially at the brain (electroencephalography) in reflecting a host of cognitive processes (e.g., load [119], attention [120]) affecting motor performance. In addition to physiological signals, survey measures can indicate critical cognitive states for persons with neurotraumas. Surveys have been extensively used to assess perceptions of utility and motivation to participate in rehabilitative therapies, especially novel approaches such as virtual reality [121]. Ultimately, generating positive perceptions from user perspectives can determine clinical acceptance of rehabilitation approaches [122]. Explicitly and formally considering such measures with rehabilitation paradigms may be crucial to ensure greater therapeutic effectiveness.
5.1 Motivation
As mentioned, motivation is a (if not the) critical user-perception measure to assess the potential success of virtual reality rehabilitation programs [11]. More specifically, motivational factors can influence the speed of movement initiation and execution [123]. Customization within virtual reality to capability levels can also increase motivation with motor learning [18]. Motivation can increase when the exercises seem applicable to daily activities [124]. Mouatt et al. (2020) demonstrated that immersive environments that manipulate ‘real’ competition enhanced participant motivation [42]. Therefore, motivation should be systematically considered in the development of virtual reality methods, leading to the inclusion of more goal or task-oriented, competitive, and transferable elements.
5.2 Sense of agency
The sense of agency is the neural perception of the true authorship of voluntary action and its related consequences [125]. In general, the higher agency one has, the better movement control one perceives; it is therefore intuitive to consider greater agency as a basis for improved functional performance [126]. Previous virtual reality studies have investigated the effect of modified visual feedback on agency and indicate that enhanced feedback in virtual reality can improve agency [127]. Other studies have shown that variations in control, as perceived visually, can co-modulate agency with motor performance at motion [128] and force [129] levels. In gamified environments with instrumented wearables, informing users about the successful accomplishment of motor tasks can also facilitate positive correlations in agency and performance [130, 131].
An implicit measure of agency that can be directly coupled to motor actions is based on the phenomenon of intentional binding [132]. Intentional binding refers to the perception of a compressed time interval between a voluntary action and related sensory consequence [132]. Sensory cues, including visual and audio feedback, are often provided to subjects while performing functional movement tasks such as reaching and grasping [133]. As such, these cues can be readily integrated within virtual reality applications (as color changes or sound) for action-outcome events to assess intentional binding.
5.3 Attention and reaction time
Attention is a well-established measure of cognitive engagement during activity [134]. Attention is often measured in virtual reality headsets with eye-tracking capabilities that analyze the focus of attention [135] or saccadic times in response to visual stimuli [136]. Attention demonstrates the ability to screen out irrelevant stimuli and focus on information directly related to the given task [137]. Attentional focus directly impacts movement performance and efficiency [34]. Rehabilitation methods can be designed to improve attention in persons with neuromuscular pathologies [138]. Virtual reality can provide specific stimuli to add or remove distractions intended to test attention [139]. Highly customized virtual reality systems can significantly improve attention compared to conventional methods [47]. However, virtual reality designs centered on improving attention may not similarly achieve gains in executive function for persons with brain injury [140]. Thus, optimal protocols with virtual reality may need to balance the evaluation of psychophysiological factors like attention while pursuing gains in motor function. Reaction time is a crucial indicator of cognitive processing during motor performance [141] and can be a surrogate measure for attention levels [142]. Previously, studies have assessed reaction time as an indicator of sensorimotor coordination and performance [143]. Virtual reality approaches may be effectively pursued to measure and improve motor reaction times.
5.4 Cognitive load and working memory
Cognitive load fundamentally infers the amount of information that working memory can hold at a given instance of activity [144]. Working memory is the cognitive system that stores information in advance for utilization in complex tasks. Since working memory relates to information processing, learning, and problem-solving, it is a variable well-posed to leverage motor control principles in virtual reality rehabilitation [145]. Virtual reality interactions are proven to improve real-world performance through memory-level therapies [146]. Furthermore, virtual reality motor rehabilitation with proven neuroplasticity improvements will enhance working memory [147]. Thus, cognitive loading can be highly sensitive to variations in virtual reality protocols for motor rehabilitation, including the level of immersion [148]. Ultimately, a desirable range of cognitive loading should be experienced by users undergoing motor rehabilitation with virtual reality. Cognitive overload occurs when there is too much information or too many tasks to execute or learn simultaneously, resulting in an inability to process this information [144] productively. Cognitive loading is crucial for optimizing the effects of augmented feedback methods since cognitive overload can inhibit motor learning [115]. Thus, participants can risk cognitive overload with even simple tasks if augmented feedback is overwhelming. However, cognitive underload must also be avoided, typically with adjustments in task challenge, to mitigate possible user disengagement during motor task practice [149].
Achieving target levels of cognitive load could be the key to improving motor rehabilitation efficiency. For example, one study demonstrated that virtual reality training with specific cognitive load levels could significantly improve walking function for chronic stroke participants [150]. Virtual reality methods can vary task or feedback guidance complexity to modulate cognitive loading levels for optimal neural engagement. Ideally, virtual reality methods should also improve working memory to expand cognitive load capacity for movement tasks further. After boundaries of cognitive capabilities are established, virtual reality methods should maintain users within cognitive loading ranges that maximize post-training motor outcomes.
6 Conclusions
We assert that leveraging augmented sensory feedback and psychophysiological factors during virtual reality rehabilitation may be the key to unlocking the full potential of virtual reality motor rehabilitation after neurotraumas. Augmented sensory guidance accelerates motor learning with visual, auditory, and haptic cues presented individually or in combination. Feedback features such as timing, complexity, intermittency, and level of body representation may be specified to optimize virtual reality rehabilitation at subject- and task-specific levels. Additionally, incorporating psychophysiological factors into virtual reality motor paradigms ensures consistent and desirable levels of neural engagement of patients within their rehabilitation regimen. An array of psychophysiological factors (e.g., motivation, agency, attention, cognitive loading) may be monitored and assessed using advanced technologies. Furthermore, these factors can be subsequently manipulated to optimal levels within virtual reality protocols that intelligently adjust guidance levels, task type and difficulty, and immersion for each user.
References
Johnson WD, Griswold DP (2017) Traumatic brain injury: a global challenge. Lancet Neurol 16(12):949–950. https://doi.org/10.1016/S1474-4422(17)30362-9
“Stroke Facts | cdc.gov,” May 25, 2021. https://www.cdc.gov/stroke/facts.htm (accessed Jun. 07, 2021).
Wyndaele M, Wyndaele J-J (2006) Incidence, prevalence and epidemiology of spinal cord injury: what learns a worldwide literature survey? Spinal Cord 44(9):523–529. https://doi.org/10.1038/sj.sc.3101893
Lim DY, Hwang DM, Cho KH, Moon CW, Ahn SY (2020) a fully immersive virtual reality method for upper limb rehabilitation in spinal cord injury. Ann Rehabil Med 44(4):311–319. https://doi.org/10.5535/arm.19181
Dobkin BH (2008) Rehabilitation after stroke. N Engl J Med 9
Kwakkel G, De Goede C, Van Wegen E (2007) Impact of physical therapy for Parkinson’s disease: a critical review of the literature. Parkinsonism Relat Disord 13:S478–S487
Downey R, Rapport MJK (2012) Motor activity in children with autism: a review of current literature. Pediatr Phys Ther 24(1):2–20
Findlay MC, Bauer SZ, Gautam D, Lucke-Wold B (2022) Rehabilitation after neurotrauma: a commentary. J Surg Care 1(1):19
Mouzon BC et al (2018) Lifelong behavioral and neuropathological consequences of repetitive mild traumatic brain injury. Ann Clin Trans Neurol 5(1):64–80
Blandford A, De Pietro G, Gallo L, Gimblett A, Oladimeji P, and Thimbleby H (2011) Engineering interactive computer systems for medicine and healthcare (EICS4Med). In Proceedings of the 3rd ACM SIGCHI symposium on Engineering interactive computing systems - EICS ’11, Pisa, Italy: ACM Press, p. 341. doi: https://doi.org/10.1145/1996461.1996556.
Howard MC (2017) A meta-analysis and systematic literature review of virtual reality rehabilitation programs. Comput Hum Behav 70:317–327. https://doi.org/10.1016/j.chb.2017.01.013
Sheehy L et al (2019) Home-based virtual reality training after discharge from hospital-based stroke rehabilitation: a parallel randomized feasibility trial. Trials 20(1):333. https://doi.org/10.1186/s13063-019-3438-9
B. Steiner, L. Elgert, B. Saalfeld, and K.-H. Wolf, “Gamification in Rehabilitation of Patients With Musculoskeletal Diseases of the Shoulder: Scoping Review,” JMIR Serious Games, vol. 8, no. 3, p. e19914, Aug. 2020, doi: https://doi.org/10.2196/19914.
Dey A, Chatburn A, and Billinghurst M (2019) Exploration of an EEG-based cognitively adaptive training system in virtual reality. In 2019 IEEE Conference on Virtual Reality and 3D User Interfaces (VR), pp. 220–226. doi: https://doi.org/10.1109/VR.2019.8797840.
Wang Z-R, Wang P, Xing L, Mei L-P, Zhao J, Zhang T (2017) Leap Motion-based virtual reality training for improving motor functional recovery of upper limbs and neural reorganization in subacute stroke patients. Neural Regen Res 12(11):1823–1831. https://doi.org/10.4103/1673-5374.219043
Rose T, Nam CS, Chen KB (2018) Immersion of virtual reality for rehabilitation: review. Appl Ergon 69:153–161. https://doi.org/10.1016/j.apergo.2018.01.009
Tieri G, Morone G, Paolucci S, Iosa M (2018) Virtual reality in cognitive and motor rehabilitation: facts, fiction and fallacies. Expert Rev Med Devices 15(2):107–117. https://doi.org/10.1080/17434440.2018.1425613
Levin MF, Weiss PL, Keshner EA (2015) Emergence of virtual reality as a tool for upper limb rehabilitation: incorporation of motor control and motor learning principles. Phys Ther 95(3):415–425. https://doi.org/10.2522/ptj.20130579
Chen J, Or CK, Chen T (2022) Effectiveness of using virtual reality–supported exercise therapy for upper extremity motor rehabilitation in patients with stroke: systematic review and meta-analysis of randomized controlled trials. J Med Internet Res 24(6):e24111
Chung C-R, Su M-C, Lee S-H, Wu EH-K, Tang L-H, Yeh S-C (2022) An Intelligent motor assessment method utilizing a Bi-lateral virtual-reality task for stroke rehabilitation on upper extremity. IEEE J Trans Eng Health Med 10:1–11
Juan M, Elexpuru J, Dias P, Santos BS, Amorim P (2023) Immersive virtual reality for upper limb rehabilitation: comparing hand and controller interaction. Virtual Reality 27(2):1157–1171
Feitosa JA, Fernandes CA, Casseb RF, Castellano G (2022) Effects of virtual reality-based motor rehabilitation: a systematic review of fMRI studies. J Neural Eng 19(1):011002
Errante A et al (2022) Effectiveness of action observation therapy based on virtual reality technology in the motor rehabilitation of paretic stroke patients: a randomized clinical trial. BMC Neurol 22(1):1–11
Winstein CJ et al (2016) Guidelines for adult stroke rehabilitation and recovery: a guideline for healthcare professionals from the American heart Association/American stroke association. Stroke. https://doi.org/10.1161/STR.0000000000000098
(2005) Preservation of upper limb function following spinal cord injury. J Spinal Cord Med 28(5): 434–470
Driessen M-J, Dekker J, Lankhorst G, van der Zee J (1997) Occupational therapy for patients with chronic diseases: CVA, rheumatoid arthritis and progressive diseases of the central nervous system. Disabil Rehabil 19(5):198–204. https://doi.org/10.3109/09638289709166527
Langhorne P, Coupar F, Pollock A (2009) Motor recovery after stroke: a systematic review. Lancet Neurol 8(8):741–754. https://doi.org/10.1016/S1474-4422(09)70150-4
Langhorne P, Bernhardt J, Kwakkel G (2011) Stroke rehabilitation. Lancet 377(9778):1693–1702. https://doi.org/10.1016/S0140-6736(11)60325-5
Kwakkel G, Veerbeek JM, van Wegen EE, Wolf SL (2015) Constraint-induced movement therapy after stroke. Lancet Neurol 14(2):224–234
“Outpatient Rehabilitation Among Stroke Survivors --- 21 States and the District of Columbia, 2005.” https://www.cdc.gov/mmwr/preview/mmwrhtml/mm5620a4.htm (accessed Jun. 07, 2021).
Wulf G (2013) Attentional focus and motor learning: a review of 15 years. Int Rev Sport Exerc Psychol 6(1):1. https://doi.org/10.1080/1750984X.2012.723728
Langhorne P, Coupar F, Pollock A (2009) Motor recovery after stroke: a systematic review. Lancet Neurol 8(8):741. https://doi.org/10.1016/S1474-4422(09)70150-4
De Miguel-Rubio A, Rubio MD, Alba-Rueda A, Salazar A, Moral-Munoz JA, Lucena-Anton D (2020) Virtual reality systems for upper limb motor function recovery in patients with spinal cord injury: systematic review and meta-analysis. JMIR mHealth Uhealth. https://doi.org/10.2196/22537
Wulf G (2013) Attentional focus and motor learning: a review of 15 years. Int Rev Sport Exerc Psychol 6(1):77–104. https://doi.org/10.1080/1750984X.2012.723728
Salmoni AW, Schmidt RA, Walter CB (1984) Knowledge of results and motor learning: a review and critical reappraisal. Psychol Bull 95(3):355–386
Schmidt RA, Young DE, Swinnen S, Shapiro DC (1989) Summary knowledge of results for skill acquisition: support for the guidance hypothesis. J Exp Psychol Learn Mem Cogn 15(2):352–359
Lange B et al (2012) Designing informed game-based rehabilitation tasks leveraging advances in virtual reality. Disabil Rehabil 34(22):1863–1870
Elor A, Powell M, Mahmoodi E, Hawthorne N, Teodorescu M, Kurniawan S (2020) On shooting stars: comparing cave and hmd immersive virtual reality exergaming for adults with mixed ability. ACM Trans Comput Healthc 1(4):1–22
Škola F, Tinková S, Liarokapis F (2019) Progressive training for motor imagery brain-computer interfaces using gamification and virtual reality embodiment. Front Hum Neurosci 13:329
Sveistrup H (2004) Motor rehabilitation using virtual reality. J Neuroeng Rehabil 1(1):1–8
de Araújo AVL, de Neiva JFO, de Monteiro CBM, Magalhães FH (2019) Efficacy of virtual reality rehabilitation after spinal cord injury: a systematic review. BioMed Res Int. https://doi.org/10.1155/2019/7106951
Mouatt B, Smith AE, Mellow ML, Parfitt G, Smith RT, Stanton TR (2020) The use of virtual reality to influence motivation, affect, enjoyment, and engagement during exercise: a scoping review. Front Virtual Reality 1:39. https://doi.org/10.3389/frvir.2020.564664
Webster A, Poyade M, Rooney S, Paul L (2021) Upper limb rehabilitation interventions using virtual reality for people with multiple sclerosis: a systematic review. Mult Scler Relat Disord 47:102610. https://doi.org/10.1016/j.msard.2020.102610
Amorim P, Sousa Santos B, Dias P, Silva S, Martins H (2020) Serious games for stroke telerehabilitation of upper limb: a review for future research. Int J Telerehab 12(2):65–76. https://doi.org/10.5195/ijt.2020.6326
Lohse K, Shirzad N, Verster A, Hodges N, Van der Loos HFM (2013) Video Games and rehabilitation: using design principles to enhance engagement in physical therapy. J Neurol Phys Ther 37(4):166. https://doi.org/10.1097/NPT.0000000000000017
Dimbwadyo-Terrer I, Trincado-Alonso F, De los Reyes-Guzmán A, López-Monteagudo P, Polonio-López B, and Gil-Agudo A (2016) Activities of daily living assessment in spinal cord injury using the virtual reality system Toyra®: functional and kinematic correlations. Virtual Realityhttps://doi.org/10.1007/s10055-015-0276-2
Faria AL, Andrade A, Soares L, Badia SBI (2016) Benefits of virtual reality based cognitive rehabilitation through simulated activities of daily living: a randomized controlled trial with stroke patients. J Neuroeng Rehabil. https://doi.org/10.1186/s12984-016-0204-z
Saposnik G et al (2016) Efficacy and safety of non-immersive virtual reality exercising in stroke rehabilitation (EVREST): a randomised, multicentre, single-blind, controlled trial. Lancet Neurol. https://doi.org/10.1016/S1474-4422(16)30121-1
Perez-Marcos D et al (2017) Increasing upper limb training intensity in chronic stroke using embodied virtual reality: a pilot study. J NeuroEngineering Rehabil. https://doi.org/10.1186/s12984-017-0328-9
Laver KE, Lange B, George S, Deutsch JE, Saposnik G, Crotty M (2017) Virtual reality for stroke rehabilitation. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD008349.pub4
Jack D et al (2001) Virtual reality-enhanced stroke rehabilitation. IEEE Trans Neural Syst Rehabil Eng 9(3):308. https://doi.org/10.1109/7333.948460
Brosnan S (2009) The potential of Wii-rehabilitation for persons recovering from acute stroke. Phys Dis 32:1–4
Kim J-H (2018) Effects of a virtual reality video game exercise program on upper extremity function and daily living activities in stroke patients. J Phys Ther Sci 30(12):1408–1411. https://doi.org/10.1589/jpts.30.1408
Brunner I et al (2016) Is upper limb virtual reality training more intensive than conventional training for patients in the subacute phase after stroke? An analysis of treatment intensity and content. BMC Neurol 16(1):219. https://doi.org/10.1186/s12883-016-0740-y
Sigrist R, Rauter G, Riener R, Wolf P (2013) terminal feedback outperforms concurrent visual, auditory, and haptic feedback in learning a complex rowing-type task. J Mot Behav 45(6):455–472. https://doi.org/10.1080/00222895.2013.826169
Nesbitt K (2017) Designing multi-sensory displays for abstract data, Jan. 2003, Accessed: Aug. 25. [Online]. Available: https://ses.library.usyd.edu.au/handle/2123/4135
Sigrist R, Rauter G, Riener R, Wolf P (2013) Augmented visual, auditory, haptic, and multimodal feedback in motor learning: a review. Psychon Bull Rev 20(1):21–53. https://doi.org/10.3758/s13423-012-0333-8
Sanford S, Liu M, Selvaggi T, Nataraj R (2020) Effects of visual feedback complexity on the performance of a movement task for rehabilitation. J Motor Behav. https://doi.org/10.1080/00222895.2020.1770670
PhiloTan Cet al. (2003) Training for physical tasks in virtual environments: Tai Chi. In: IEEE Virtual Reality, 2003. Proceedings., Los Angeles, CA, USA: IEEE Comput. Soc. Doi:https://doi.org/10.1109/VR.2003.1191125
Smith SA (2019) Virtual reality in episodic memory research: a review. Psychon Bull Rev 26(4):1213–1237. https://doi.org/10.3758/s13423-019-01605-w
Wulf G, Shea CH (2002) Principles derived from the study of simple skills do not generalize to complex skill learning. Psychon Bull Rev 9(2):185–211
Soekadar SR, Birbaumer N, Cohen LG (2011) Brain–computer interfaces in the rehabilitation of stroke and neurotrauma. In: Systems neuroscience and rehabilitation, Springer pp. 3–18.
Côté M-P, Murray M, Lemay MA (2017) Rehabilitation strategies after spinal cord injury: inquiry into the mechanisms of success and failure. J Neurotrauma 34(10):1841–1857
Teng YD, Zafonte RD (2021) Prelude to the special issue on novel neurocircuit, cellular and molecular targets for developing functional rehabilitation therapies of neurotrauma. Exp Neurol 341:113689
Sigrist R, Rauter G, Marchal-Crespo L, Riener R, Wolf P (2015) Sonification and haptic feedback in addition to visual feedback enhances complex motor task learning. Exp Brain Res 233(3):909–925. https://doi.org/10.1007/s00221-014-4167-7
Huang H, Wolf SL, He J (2006) Recent developments in biofeedback for neuromotor rehabilitation. J Neuroeng Rehabil 3(1):1–12
Ono T et al (2015) Multimodal sensory feedback associated with motor attempts alters BOLD responses to paralyzed hand movement in chronic stroke patients. Brain Topogr 28:340–351
Wake N, Sano Y, Oya R, Sumitani M, Kumagaya S, and Kuniyoshi M (2015) Multimodal virtual reality platform for the rehabilitation of phantom limb pain. In: 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER), IEEE, 2015, pp. 787–790.
Haghighi N, Vladis N, Liu Y, and Satyanarayan A (2021) The Effectiveness of Haptic Properties Under Cognitive Load: An Exploratory Study,” arXiv:2006.00372 [cs], Jun. 2020, Accessed: Mar. 18, 2021. [Online]. Available: http://arxiv.org/abs/2006.00372
Beom-Chan L and Sienko KH (2011) Effects of attractive versus repulsive vibrotactile instructional cues during motion replication tasks. In: 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Boston, MA: IEEE, pp. 3533–3536. doi: https://doi.org/10.1109/IEMBS.2011.6090587.
Nunzio AMD et al (2017) Tactile feedback is an effective instrument for the training of grasping with a prosthesis at low- and medium-force levels. Exp Brain Res 235(8):2547–2559. https://doi.org/10.1007/s00221-017-4991-7
Raveh E, Portnoy S, Friedman J (2018) Adding vibrotactile feedback to a myoelectric-controlled hand improves performance when online visual feedback is disturbed. Hum Mov Sci 58:32–40. https://doi.org/10.1016/j.humov.2018.01.008
Ballardini G, Florio V, Canessa A, Carlini G, Morasso P, Casadio M (2020) Vibrotactile feedback for improving standing balance. Front Bioeng Biotechnol 8:94. https://doi.org/10.3389/fbioe.2020.00094
Hasson CJ, Manczurowsky J (2015) Effects of kinematic vibrotactile feedback on learning to control a virtual prosthetic arm. J NeuroEngineering Rehabil 12(1):31. https://doi.org/10.1186/s12984-015-0025-5
Hermann T (2008) Taxonomy and definitions for sonification and auditory display. In Proceedings of the14th International Conference on Auditory Display, Paris, France, p. 8.
Bevilacqua F et al (2016) Sensori-motor learning with movement sonification: perspectives from recent interdisciplinary studies. Front Neurosci. https://doi.org/10.3389/fnins.2016.00385
van Vugt FT, Tillmann B (2015) Auditory feedback in error-based learning of motor regularity. Brain Res 1606:54–67. https://doi.org/10.1016/j.brainres.2015.02.026
Castro F, Bryjka PA, Di Pino G, Vuckovic A, Nowicky A, Bishop D (2021) Sonification of combined action observation and motor imagery: effects on corticospinal excitability. Brain Cogn 152:105768
Scholz DS et al (2016) Sonification of arm movements in stroke rehabilitation: a novel approach in neurologic music therapy. Front Neurol. https://doi.org/10.3389/fneur.2016.00106
Dyer JF, Stapleton P, Rodger MWM (2017) Advantages of melodic over rhythmic movement sonification in bimanual motor skill learning. Exp Brain Res 235(10):3129–3140. https://doi.org/10.1007/s00221-017-5047-8
Brownley KA, McMurray RG, Hackney AC (1995) Effects of music on physiological and affective responses to graded treadmill exercise in trained and untrained runners. Int J Psychophysiol 19(3):193–201. https://doi.org/10.1016/0167-8760(95)00007-F
Ronsse R, Vitiello N, Lenzi T, van den Kieboom J, Carrozza MC, Ijspeert AJ (2011) Human-robot synchrony: flexible assistance using adaptive oscillators. IEEE Trans Biomed Eng 58(4):1001. https://doi.org/10.1109/TBME.2010.2089629
Soltani P, Salesi M (2013) Effects of exergame and music on acute exercise responses to graded treadmill running. Games Health J 2(2):75–80. https://doi.org/10.1089/g4h.2012.0077
Leocani L et al (2007) Impaired short-term motor learning in multiple sclerosis: evidence from virtual reality. Neurorehabil Neural Repair 21(3):273–278
Dias Pereira dos Santos A, Yacef K, Martinez-Maldonado R (2017), Let’s dance: how to build a user model for dance students using wearable technology. In: Proceedings of the 25th Conference on User Modeling, Adaptation and Personalization, pp. 183–191.
Avanzini F, De Götzen A, Spagnol S, and Rodá A (2009) Integrating auditory feedback in motor rehabilitation systems. In: Proceedings of international conference on multimodal interfaces for skills transfer (SKILLS09), Citeseer, pp. 53–58.
Mayer AR, Bellgowan PS, Hanlon FM (2015) Functional magnetic resonance imaging of mild traumatic brain injury. Neurosci Biobehav Rev 49:8–18
Ettenhofer ML, Hershaw JN, Engle JR, Hungerford LD (2018) Saccadic impairment in chronic traumatic brain injury: examining the influence of cognitive load and injury severity. Brain Inj 32(13–14):1740–1748
Padilla R, Domina A (2016) Effectiveness of sensory stimulation to improve arousal and alertness of people in a coma or persistent vegetative state after traumatic brain injury: a systematic review. Am J Occup Ther 70(3):7003180030p1-7003180030p8
Kilteni K, Groten R, Slater M (2012) The sense of embodiment in virtual reality”, presence teleoperators and virtual. Environments 21(4):373–387. https://doi.org/10.1162/PRES_a_00124
Yao S and Kim G (2019) The Effects of Immersion in a Virtual Reality Game: Presence and Physical Activity. In: HCI in Games, X. Fang, Ed., in Lecture Notes in Computer Science, vol. 11595. Cham: Springer International Publishing, pp. 234–242. doi: https://doi.org/10.1007/978-3-030-22602-2_18.
Sanford S, Liu M, Nataraj R (2021) Concurrent continuous versus bandwidth visual feedback with varying body representation for the 2-legged squat exercise. J Sport Rehabil. https://doi.org/10.1123/jsr.2020-0234
Proteau L (1992) Chapter 4 On The Specificity of Learning and the Role of Visual Information for Movement Control. In: L. Proteau and D. Elliott, (Eds) Advances in Psychology, , Vision and Motor Control, vol. 85. North-Holland, pp. 67–103. doi: https://doi.org/10.1016/S0166-4115(08)62011-7.
Timmers R and Sadakata M (2014), Training expressive performance by means of visual feedback: existing and potential applications of performance measurement techniques. In: Expressiveness in music performance: Empirical approaches across styles and cultures, pp. 304–334, 2014.
Walsh KA, Sanford SP, Collins BD, Harel NY, Nataraj R (2021) Performance potential of classical machine learning and deep learning classifiers for isometric upper-body myoelectric control of direction in virtual reality with reduced muscle inputs. Biomed Signal Process Control 66:102487
Blana D, Kyriacou T, Lambrecht JM, Chadwick EK (2016) Feasibility of using combined EMG and kinematic signals for prosthesis control: a simulation study using a virtual reality environment. J Electromyogr Kinesiol 29:21–27. https://doi.org/10.1016/j.jelekin.2015.06.010
Perez-Marcos D et al (2017) Increasing upper limb training intensity in chronic stroke using embodied virtual reality: a pilot study. J NeuroEngineering Rehabil 14(1):119. https://doi.org/10.1186/s12984-017-0328-9
Aoyagi K et al. (2019) Improvement of Sense of Agency During Upper-Limb Movement for Motor Rehabilitation Using Virtual Reality. In: 2019 41st Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC), Berlin, Germany: IEEE, pp. 118–121. doi: https://doi.org/10.1109/EMBC.2019.8856796.
Cote-Allard U et al (2021) A transferable adaptive domain adversarial neural network for virtual reality augmented emg-based gesture recognition. IEEE Trans Neural Syst Rehabil Eng 29:546–555. https://doi.org/10.1109/TNSRE.2021.3059741
Hülsmann F, Göpfert JP, Hammer B, Kopp S, Botsch M (2018) Classification of motor errors to provide real-time feedback for sports coaching in virtual reality: a case study in squats and Tai Chi pushes. Comput Graph 76:47–59. https://doi.org/10.1016/j.cag.2018.08.003
Park JH, Shea CH, Wright DL (2000) Reduced-frequency concurrent and terminal feedback: a test of the guidance hypothesis. J Mot Behav 32(3):287–296. https://doi.org/10.1080/00222890009601379
P. M. Fitts and M. I. Posner, Human performance. In Human performance. Oxford, England: Brooks/Cole, 1967.
Goodwin JE, Meeuwsen HJ (1995) Using bandwidth knowledge of results to alter relative frequencies during motor skill acquisition. Res Q Exerc Sport 66(2):99–104. https://doi.org/10.1080/02701367.1995.10762217
Sherwood DE (1988) Effect of bandwidth knowledge of results on movement consistency. Percept Mot Skills 66(2):535–542. https://doi.org/10.2466/pms.1988.66.2.535
Sadowski J, Mastalerz A, Niznikowski T (2013) Benefits of bandwidth feedback in learning a complex gymnastic skill. J Hum Kinet 37(1):183–193. https://doi.org/10.2478/hukin-2013-0039
Young DE, Schmidt RA (1992) Augmented kinematic feedback for motor learning. J Mot Behav 24(3):261–273. https://doi.org/10.1080/00222895.1992.9941621
Huet M, Camachon C, Fernandez L, Jacobs DM, Montagne G (2009) Self-controlled concurrent feedback and the education of attention towards perceptual invariants. Hum Mov Sci 28(4):450–467. https://doi.org/10.1016/j.humov.2008.12.004
Aiken CA, Fairbrother JT, Post PG (2012) The effects of self-controlled video feedback on the learning of the basketball set shot. Front Psychol. https://doi.org/10.3389/fpsyg.2012.00338
Post PG, Fairbrother JT, Barros JAC (2011) Self-controlled amount of practice benefits learning of a motor skill. Res Q Exerc Sport 82(3):474–481. https://doi.org/10.1080/02701367.2011.10599780
Bark K et al (2015) Effects of vibrotactile feedback on human learning of arm motions. IEEE Trans Neural Syst Rehabil Eng 23(1):51–63. https://doi.org/10.1109/TNSRE.2014.2327229
Schiffman JM, Luchies CW, Piscitelle L, Hasselquist L, Gregorczyk KN (2006) Discrete bandwidth visual feedback increases structure of output as compared to continuous visual feedback in isometric force control tasks. Clin Biomech 21(10):1042–1050. https://doi.org/10.1016/j.clinbiomech.2006.05.009
Chen Chen F, Appendino S, Battezzato A, Favetto A, Mousavi M, and Pescarmona F (2013) Constraint Study for a Hand Exoskeleton: Human Hand Kinematics and Dynamics, J Robot https://www.hindawi.com/journals/jr/2013/910961/ (accessed Jun. 28, 2018).
Adamovich SV et al (2005) A virtual reality: based exercise system for hand rehabilitation post-stroke. Presence Teleoperator Virtual Environ 14(2):161–174. https://doi.org/10.1162/1054746053966996
Qian J, McDonough DJ, Gao Z (2020) The effectiveness of virtual reality exercise on individual’s physiological, psychological and rehabilitative outcomes: a systematic review”. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph17114133
Lohse K, Shirzad N, Verster A, Hodges N, Van der Loos HFM (2013) Video games and rehabilitation: using design principles to enhance engagement in physical therapy. J Neurol Phys Ther 37(4):166–175. https://doi.org/10.1097/NPT.0000000000000017
Im T, An D, Kwon OY, and Kim SY, (2017) A Virtual Reality based Engine Training System - A Prototype Development & Evaluation, SCITEPRESS, pp. 262–267. doi: https://doi.org/10.5220/0006263702620267.
Jack D et al (2001) Virtual reality-enhanced stroke rehabilitation. IEEE Trans Neural Syst Rehabil Eng 9(3):308–318. https://doi.org/10.1109/7333.948460
Krassioukov A (2009) Autonomic function following cervical spinal cord injury. Respir Physiol Neurobiol 169(2):157–164
Antonenko P, Paas F, Grabner R, Van Gog T (2010) Using electroencephalography to measure cognitive load. Educ Psychol Rev 22:425–438
Liu N-H, Chiang C-Y, Chu H-C (2013) Recognizing the degree of human attention using EEG signals from mobile sensors. Sensors 13(8):10273–10286
Glegg SM, Holsti L, Velikonja D, Ansley B, Brum C, Sartor D (2013) Factors influencing therapists’ adoption of virtual reality for brain injury rehabilitation. Cyberpsychol Behav Soc Netw 16(5):385–401
Liu L, Miguel Cruz A, Rios Rincon A, Buttar V, Ranson Q, Goertzen D (2015) What factors determine therapists’ acceptance of new technologies for rehabilitation–a study using the unified theory of acceptance and use of technology (UTAUT). Dis rehabil 37(5):447–455
Mir P, Trender-Gerhard I, Edwards MJ, Schneider SA, Bhatia KP, Jahanshahi M (2011) Motivation and movement: the effect of monetary incentive on performance speed. Exp Brain Res 209(4):551–559
Meyns P, Roman de Mettelinge T, van der Spank J, Coussens M, Van Waelvelde H (2018) Motivation in pediatric motor rehabilitation: a systematic search of the literature using the self-determination theory as a conceptual framework. Dev Neurorehabil 21(6):371–390. https://doi.org/10.1080/17518423.2017.1295286
Moore JW (2016) What Is the sense of agency and why does it matter? Front Psychol. https://doi.org/10.3389/fpsyg.2016.01272
Ein-Gar D, Steinhart Y (2017) Self-control and task timing shift self-efficacy and influence willingness to engage in effortful tasks. Front Psychol. https://doi.org/10.3389/fpsyg.2017.01788
Aoyagi K et al (2021) Modified sensory feedback enhances the sense of agency during continuous body movements in virtual reality. Sci Rep. https://doi.org/10.1038/s41598-021-82154-y
Nataraj R, Sanford S, Shah A, Liu M (2020) Agency and performance of reach-to-grasp with modified control of a virtual hand: implications for rehabilitation. Front Hum Neurosci 14:126. https://doi.org/10.3389/fnhum.2020.00126
Nataraj R, Sanford S (2021) Control modification of grasp force covaries agency and performance on rigid and compliant surfaces. Front Bioeng Biotechnol 8:1544
Nataraj R, Hollinger D, Liu M, Shah A (2020) Disproportionate positive feedback facilitates sense of agency and performance for a reaching movement task with a virtual hand. PLoS ONE 15(5):e0233175
Liu M, Wilder S, Sanford S, Saleh S, Harel NY, Nataraj R (2021) Training with agency-inspired feedback from an instrumented glove to improve functional grasp performance. Sensors 21(4):1173
Moore JW, Obhi SS (2012) Intentional binding and the sense of agency: a review. Conscious Cogn 21(1):546–561. https://doi.org/10.1016/j.concog.2011.12.002
Evans N, Gale S, Schurger A, Blanke O (2015) Visual feedback dominates the sense of agency for brain-machine actions. PLOS ONE 10(6):e0130019. https://doi.org/10.1371/journal.pone.0130019
Goldberg P et al (2021) Attentive or not? toward a machine learning approach to assessing students’ visible engagement in classroom instruction. Educ Psychol Rev 33(1):27–49. https://doi.org/10.1007/s10648-019-09514-z
Schiessl M, Duda S, Thölke A, Fischer R (2003) Eye tracking and its application in usability and media research. MMI-interaktiv J 6(2003):41–50
Valuch C, Pflüger LS, Wallner B, Laeng B, Ansorge U (2015) Using eye tracking to test for individual differences in attention to attractive faces. Front Psychol. https://doi.org/10.3389/fpsyg.2015.00042
Mertes C, Wascher E, Schneider D (2016) From capture to inhibition: how does irrelevant information influence visual search? Evidence from a spatial cuing paradigm. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2016.00232
Chevallier C, Kohls G, Troiani V, Brodkin ES, Schultz RT (2012) The social motivation theory of autism. Trends Cogn Sci 16(4):231–239. https://doi.org/10.1016/j.tics.2012.02.007
Cho BH et al. (2002), Attention Enhancement System using virtual reality and EEG biofeedback. In Proceedings IEEE Virtual Reality 2002, pp. 156–163. doi: https://doi.org/10.1109/VR.2002.996518.
Shin H, Kim K (2015) Virtual reality for cognitive rehabilitation after brain injury: a systematic review. J Phys Ther Sci 27(9):2999–3002. https://doi.org/10.1589/jpts.27.2999
Balakrishnan G, Uppinakudru G, Girwar Singh G, Bangera S, Dutt Raghavendra A, Thangavel D (2014) A comparative study on visual choice reaction time for different colors in females. Neurol Res Int 2014:e301473. https://doi.org/10.1155/2014/301473
Reigal RE, Barrero S, Martín I, Morales-Sánchez V, Juárez-Ruiz de Mier R, Hernández-Mendo A (2019) Relationships between reaction time, selective attention, physical activity, and physical fitness in children. Front Psychol. https://doi.org/10.3389/fpsyg.2019.02278
Batra A, Vyas S, Gupta J, Gupta K, and Hada R, A Comparative Study Between Young and Elderly Indian Males on Audio-Visual Reaction Time.
de Jong T (2010) Cognitive load theory, educational research, and instructional design: some food for thought. Instr Sci 38(2):105–134. https://doi.org/10.1007/s11251-009-9110-0
Levin MF, Weiss PL, Keshner EA (2015) Emergence of virtual reality as a tool for upper limb rehabilitation: incorporation of motor control and motor learning principles. Phys Ther 95(3):425. https://doi.org/10.2522/ptj.20130579
Brooks BM, Rose FD (2003) The use of virtual reality in memory rehabilitation: current findings and future directions. NeuroRehabilitation 18(2):147–157
Grealy MA, Johnson DA, Rushton SK (1999) Improving cognitive function after brain injury: the use of exercise and virtual reality. Arch Phys Med Rehabil 80(6):661–667. https://doi.org/10.1016/s0003-9993(99)90169-7
Frederiksen JG et al (2020) Cognitive load and performance in immersive virtual reality versus conventional virtual reality simulation training of laparoscopic surgery: a randomized trial. Surg Endosc 34(3):1244–1252. https://doi.org/10.1007/s00464-019-06887-8
Carmona NE (2019), The Roles Of Cognitive Load And Appraisal Of Task Difficulty In Predicting Subjective Fatigue And Subsequent Task Disengagement
Cho KH, Kim MK, Lee H-J, Lee WH (2015) Virtual reality training with cognitive load improves walking function in chronic stroke patients. Tohoku J Exp Med 236(4):273–280. https://doi.org/10.1620/tjem.236.273
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors reported no potential conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Dewil, S., Kuptchik, S., Liu, M. et al. The cognitive basis for virtual reality rehabilitation of upper-extremity motor function after neurotraumas. J Multimodal User Interfaces 17, 105–120 (2023). https://doi.org/10.1007/s12193-023-00406-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12193-023-00406-9