Integrating New Technologies into the Treatment of CP and DCD ...

Curr Dev Disord Rep (2016) 3:138–151 DOI 10.1007/s40474-016-0083-9

DISORDERS OF MOTOR (PH WILSON, SECTION EDITOR)

Integrating New Technologies into the Treatment of CP and DCD Peter Wilson 1 & Dido Green 2 & Karen Caeyenberghs 1 & Bert Steenbergen 1,3 & Jonathan Duckworth 4

Published online: 11 April 2016 # Springer International Publishing Switzerland 2016

Abstract This paper examines how current understandings of childhood participation and motor development provide opportunities for using new technologies (such as virtual reality—VR) for children with neurodevelopmental disorders. Specifically, the International Classification of Functioning, Disability and Health is used to conceptualize the role of technology in treatment across body structures and body function, activity performance, and participation (WHO 2007, 2012). First, we review the particular motor control and learning mechanisms that have been implicated in children with atypical motor development, like DCD. This section will highlight avenues for targeted remediation. Next, VR-based rehabilitation systems are reviewed in relation to neurodevelopmental disorders, focusing first on CP and second on more recent applications for children with DCD. We describe the evolution of particular design innovations in virtual rehabilitation including recent advances using tangible interfaces, as well as other methods targeting cognitive function more specifically. Benefits of these various treatments will be viewed through the lens of current theory and evaluated at the level of child and family outcomes. Finally, we consider the broader aspects of the potential for technological innovation in rehabilitation

This article is part of the Topical Collection on Disorders of Motor * Peter Wilson [email protected]

1

Centre for Disability and Development Research (CeDDR), Australian Catholic University, Melbourne, Australia

2

Oxford-Brookes University, Oxford, UK

3

Radboud University, Nijmegen, The Netherlands

4

RMIT University, Melbourne, Australia

and its impact on brain function, activity competence, and longer-term participation. Keywords Developmental coordination disorder . Cerebral palsy . Rehabilitation . Virtual reality . Cognitive training . Gaming . Interactive digital media

Introduction The ICF Framework—an Ecological Approach to Rehabilitation The International Classification of Functioning, Disability and Health for Children and Young People (ICF-CY [1]) takes a shift in focus from a person’s impairments to participation across multiple contexts. Taking an ecological perspective, the ICF incorporates both strengths and deficits across physical, psychosocial, and environmental domains to define the nature of any difficulty and the impact on participation (see Fig. 1). The impact of childhood disability per se on both the child and their family is a central concern. It follows that interventions are designed to optimize the synergies/ interactions that exist between child, task, and environmental factors in order to maximize participation across contexts. The ICF looks at children with neurodevelopmental disorders (like developmental coordination disorders (DCD)) in a holistic and positive manner to identify any personal, social, or environmental constraints on their health. This approach supports the development of tailored intervention programs and the removal of any barriers to greater participation in daily life [3]. New digital technologies afford an exciting means of engaging children in therapy and providing intervention environments and experiences that can easily be adapted to individual needs. The ubiquitous nature of interactive digital

Curr Dev Disord Rep (2016) 3:138–151

Fig. 1 ICF framework [2]

media in everyday life provides important opportunities for the design of new therapies and participatory engagement.

Development of Neuromotor and Cognitive Function in Children: Implications for VR-Based Applications Understanding the neurocognitive basis of motor control, learning, and development is the conceptual foundation for intervention. In this section, we describe some of the more important concepts/mechanisms in motor development and behavior—predictive control (an aspect of internal modeling), interactive specialization, and the coupling of motor and cognitive systems. These same concepts are also important in understanding deviations from typical development (BNeurodevelopmental Disorders of Movement: a Primer on CP and DCD^ section), the intriguing parallels between cerebral palsy (CP) and DCD, and reconceptualization of motor intervention (BImplications for Treatment^ section).

Early Stages of Motor Development The newborn infant enters the world with a range of primitive (but adaptive) movement reflexes and a visual system that is already attuned to movement but lacking in acuity. Impressive is a functional neural system for object perception (e.g., object permanence) and gross localization. Basic movement synergies are also present that enable young infants to respond reflexively to salient objects that enter their visual field using basic arm, head, and torso movements [4]. These early movements are loosely coordinated, but the rough edges of interjoint coupling are smoothed over time and with experience, rapidly over the first 6 months. These (repetitive and fairly automatic) early object-oriented interactions enable the infant to develop higher-order object concepts while also learning the dynamics of their own motor system) [5, 6]. In this way, mechanisms of motor control emerge from the interaction of the infant with their physical world.

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Critical to motor learning and development is the capacity of the motor system to learn the systematic relationship that exists between motor output commands and the effects of these commands on the biomechanical system. Knowledge of this relationship emerges as a function of (use-dependent) error-based learning where, for a given motor output, an effector unit (e.g., an arm) is moved in a given trajectory, specified in kinematic terms [7]. Repeated movements thus supply the motor system with a series of output commands that can be calibrated against sensory inputs. Over time, the child learns this calibration and adjusts output signals to better approximate a desired movement goal. This process of perceptualmotor mapping enables feedforward (or predictive) control, an aspect of internal modeling [8]. Mature reaching is controlled by an integrated system of feedback and feedforward control [9]. This mechanism of control has a miraculous ability to effect rapid changes in movement trajectory (in real time) in response to sudden events in the ambient environment; e.g., trajectory can be altered in as little as 70–100 ms in response to visual perturbations [10]. Such changes are only possible to the extent that the nervous system can predict the future location of the moving limb using a forward (internal) model [9]. The speed and flexibility of this control is one of the hallmarks of skilled action, which develops rapidly over childhood [11]—this is shown in a range of contexts including force adaptation [12], isometric force control [13], anticipatory postural adjustments [14], and rapid online control of reaching [11]. Target-directed reaching provides perhaps the clearest demonstration of the development of predictive control over childhood. In earlier studies, we showed that younger children are slower to adjust their reaching to visual perturbation than older children, suggesting a reduced ability to integrate predictive estimates of limb position with online feedback [11]. For static targets, the movement times of older children (8– 12 years) were around 550 ms and increased to around 800 ms on trials when the target jumped at movement onset. For younger children aged 5–7 years, the relative increase was much greater (from around 640 to 1030 ms), and movement trajectory was corrected later on jump trials. These online corrections are served by internal feedback loops which enable seamless integration of predictive error signals with motor commands throughout the movement cycle [15–17]. Interactive Specialization: Coupling Motor and Cognitive Control in the Development of Goal-Directed Actions The theory of interactive specialization provides a parsimonious and biologically plausible explanation for the emergence of new behavior over time and experience. A key assumption is that the functional output of a given cortical region is dependent on its reciprocal couplings to other regions. As such, cognitive functions and behaviors emerge as a consequence of

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changes to multiple neural regions rather than particular sites (or modules) within the CNS; i.e., the weighted activity of several brain regions—whose architecture and rate of maturation may vary—supports functional changes in cognition and behavior [18]. Functional circuits within the central nervous system (CNS) are initially ill-defined and may be activated in response to a broad range of stimuli. Over time and with experience, these circuits or networks become more specialized. For a given band of stimuli, there develops a shift in activation from diffuse to more focal regions [19]. Frontal cortical systems unfold rapidly over the course of child development, and play a particularly important role in the control of goal-directed movement, enabling more flexible behavior in the face of changing or more challenging task and environmental demands [20]. For example, as task complexity increases and with it the number of sub-routines, executive control systems (like working memory, executive attention, and inhibitory control) become increasingly important. Maturation and experience dictate how readily and efficiently these neural networks can be enlisted; in the case of visuospatial working memory and attention, for example, white matter networks spanning dorso-lateral prefrontal and parietal cortex show accelerated growth during later childhood which supports action planning [21]. As well, frontal networks enhance basic learning functions like action observation and imitation to the extent that the observer is better able to discern the intention (or goal) behind the action [22]. And in more recent work, we have shown that the ability to couple online motor control and inhibitory control unfolds gradually over the course of development [23]. In general, the amount of topdown (or front to back) control increases substantially over childhood to enable more complex actions that fit the child to meet the ever increasing challenges of development [24].

Neurodevelopmental Disorders of Movement: a Primer on CP and DCD In cases of neural damage or problems of functional connectivity, reorganization of the developing system has been shown to be influenced by activity. Eyre and colleagues [25] have shown activity-dependent withdrawal of ipsilateral corticospinal neural connections during the first 2 years of life which are retained in some children with hemiplegic cerebral palsy with a functional cost [25]. Accumulating evidence shows the importance of task-specific intense and repetitive training for motor skill acquisition and neural plasticity for improved functional ability [26–28]. However, less evidence is present for the translation of specific gains shown in the clinical setting to longer-term functional benefits. However, engaging children in such repetitive exercise is challenging and the potential benefits of these therapy programs can be compromised by frustration and poor compliance.


In children with DCD, alterations of brain connectivity have been related to motor deficits (for reviews see [29–31]). Microstructural compromise has been demonstrated within a number of motor, sensory, and cerebellar pathways in DCD [32–35], indicating developmental alterations in white matter organization of the sensorimotor pathways. Converging evidence across functional MRI studies also indicates abnormal activation of brain areas in DCD during performance of motor tasks (e.g., [34, 36–38]). Cortical thinning in medial orbitofrontal cortex was also observed in DCD children [33], which correlated with lower scores on tests of motor functioning. Finally, a weaker segregation and integration of the structural connectome (network) was found in DCD children, and these abnormalities of the connectome were related to visuomotor deficits [32]. These changes in brain structure and function in DCD are likely to reflect Bectopic miswiring,^ or atypical brain development. Despite the fact that these MRI studies have advanced our theoretical understanding of the disorder, it would be informative in the future to examine the effects of training programs on motor performance and brain connectivity in children with DCD. Delay in the functional coupling between motor control and executive function has been observed in DCD using goal-directed reaching tasks under varying cognitive load (as when, for example, they must inhibit an action to a specific cue and move to a contralateral location). We see greater reliance on slower feedback systems under these conditions [39]. Indeed, given the strong evidence for executive function deficits in developmental coordination disorders (DCD), we see a double disadvantage in the control of action: poor predictive control coupled with deficits of executive function, resulting in impaired acquisition of movement skill and perhaps self-regulation [40]. Indeed, there is strong evidence of a link between executive control and movement skill, more generally. Levels of inhibitory control, for example, are quite strongly correlated with movement skill in both younger [41] and older [42] children. And more recent work shows persistent difficulties in EF into younger adulthood, impacting aspects of task planning and organization [43].

Implications for Treatment Deficits in motor planning and predictive control suggest at least two possible avenues for intervention in CP/DCD: use of augmented feedback (AF) and attentional training. Importantly, methods of AF have been shown to benefit both populations, with multisensory (extrinsic) feedback and techniques that cue attentional focus being shown to exert good treatment effects [44, 45]. Each is discussed in turn, with implications for the use of VR systems.


Augmented Feedback AF involves the provision of (external) information about the performance of an action, over and above that available as a natural consequence of movement. There are several types of AF: knowledge of results (KR), knowledge of performance (KP), and concurrent AF. KR involves providing information about movement outcome (e.g., target hits for a set of trials), while KP concerns the manner in which the movement was performed and its form. Concurrent AF involves the provision of feedback in real time, commonly the use of correlated visual, haptic, or auditory input. The benefits of AF have been reported widely in the motor learning literature [46, 47]. For instance, high-intensity training using a combination of AF is likely to yield stronger and transferable effects in relation to upper-limb function; however, experimental studies looking at critical ingredients for efficacy and, ultimately, randomized control trials (RCTs) are required to test AF effects.

Attentional Training There is now strong converging evidence to support the benefits of an external focus of attention during skill acquisition, both in adults and children [48–50]. As a training tool, external cues are provided that encourage the performer to focus on the effects of their movement (e.g., trajectory) rather than their internal state or bodily sensations. Importantly, performance on retention and transfer tasks also tends to be better after external focus training compared with internal focus [50]. As well, basic research shows that concurrent AF which biases attention to the effect of the movement yields stronger training and retention effects than feedback about movement form [48, 51]. The ideomotor theory of Hommel, Prinz, and colleagues explains these training effects in terms of action prediction (aka internal modeling [52, 53]). Put simply, actions are controlled by their intended effects. With practice, the performer learns to predict action effects in advance, with these predictive models used as a template for monitoring real-time sensory feedback. Training that helps the performer direct their attention to movement effects may enhance this process of prediction, and with it the ability to adjust movements seamlessly in real time [50]. This may provide a more powerful medium for skill development and rehabilitation than other forms of feedback. In virtual rehabilitation of brain injury, the little work that does exist shows some advantages of training external focus for upperlimb function [54]. A sobering fact is that most verbal instructions by movement therapists to patients concern body movements and sensation, which is likely to induce an internal focus of attention [55].

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Trends in Technology-Mediated Rehabilitation for Childhood Disability Principles for Interaction Design From an ICF perspective, interventions should have a clear focus on enhancement of participation. Importantly, this broad goal can be addressed by having participation outcomes as a downstream effect of training, or by making participation itself the medium of therapeutic change. For example, in the classical medical model, treatments are seen primarily as a means of improving basic body functions (like muscle strength) and specific activity competencies (like movement skill). Improvements in daily functioning and participation are then seen as transfer effects. Alternately, participation experiences per se can be designed as the medium for change, implemented within community settings. Our work utilizing Bmagic camps^ as a medium for intervention in children with hemiplegia is a recent example [56]. Here, the design of therapeutic workspaces is critical to engage children in meaningful and creative activities that are fun and social in orientation, driving sustained recovery. This approach fits well with the ICF framework which stresses the ecology of participatory activities and experiences, including the structure of the environment at a physical and social level. Learning environments that present (natural) affordances for interaction should be a design imperative in virtual rehabilitation. In the case of virtual environments (VE), it is critical to present object and spatial properties of the workspace in a meaningful, compelling, and veridical way. Conventional computer user interfaces tend to neglect the intrinsic importance of body movement and tangible interaction and limit opportunities for relearning movements. Physical input devices or tangible user interfaces (TUIs), however, can exploit multiple human sensory channels otherwise neglected in conventional interfaces and can promote rich and dexterous interaction [57]. From the perspective of embodied interaction, a first-person experience of user interaction is one that capitalizes on our physical skills and our familiarity with real-world objects [58]. The use of TUIs integrates and supports the manipulation of physical objects in ways that are natural to the user’s body and their environment and provides a stronger basis for meaningful action and the development of movement skill. In particular, TUIs can enhance perceptual experiences for children with neurodevelopmental disabilities, affording opportunities for manual actions and exploration they might not otherwise have at home or in school [59]. In the sections that follow, we describe how exposure to novel VEs and AF can stimulate action and skill development in children, assisting the crucial mapping that must occur between selfinitiated action and its sensorimotor effects on the world. Advances in digital technology, digital arts, and interaction design are presenting exciting and viable prospects for clinical

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rehabilitation [60]. When designed with the end user in mind, virtual rehabilitation has potential to stimulate a high level of interest, improve engagement and enjoyment in patient groups, enhance learning, provide safe task conditions, and complement standard therapy. Recent work integrating digital media art and rehabilitation science has shown that intuitive design and playful forms of user interaction are inherently motivating and critical to treatment efficacy [61, 62]. Importantly, VR provides a palette of design solutions that can be scaled to the individual needs of children with disabilities, encouraging repeated practice of both exploratory and functional actions [63]. Virtual Rehabilitation of Motor Function in CP and DCD Rehabilitation systems using interactive digital technologies can be classified in a number of ways, reflecting both the evolution of the technology itself and the particular issues of the target population or neurodisability. First, a distinction can be drawn between game-like systems that use the logic of many off-the-shelf products (like Wii Fit) and those systems designed more specifically for learning and rehabilitation (i.e., virtual tutor and tele-rehab). Second, systems can be grouped according to the particular behavioral or psychological focus of therapy, e.g., upper- or lower-limb rehabilitation, physical fitness/balance, functional rehabilitation, participation and play, social interaction, and self-regulation (for review, see [64, 65]). Comparisons of the opportunities afforded by system type and design in order to facilitate specific behavioral or participatory outcomes will be considered specifically in relation to motor function of children with movement impairments. Video Capture Early forays in virtual rehabilitation of motor and cognitive function in children were mainly directed at children with CP and acquired brain injury (ABI), with video capture technology the primary medium using systems such as the IREX or GX (see the review [65]). There have been few RCTs of VR systems targeting CP, and those that do exist have demonstrated equivocal changes in skill and participation across settings and over time. An early study of 31 children with CP [66] failed to show any significant treatment effect with the Gesture Xtreme, IREX system, while a smaller RCT [67] involving mixed types of CP (n = 10) showed the EyeToy system to yield treatment effects at the body function level while functional gains in activity were not reported. Smaller case series/case studies have suggested some positive benefits to reaching function in children with CP. Using the EyeToy system, Chen et al. [68] showed improved reaching (kinematics) translating to functional performance in three children with HCP using a series of reaching games. You et al. [69], utilizing


the IREX VR, showed improved functional arm movements in a child with HCP, with associated enhancement of cortical activation on functional magnetic resonance imaging. More recently, a well-powered RCT of a web-based interactive computer gaming system, the BMove it to improve it^ (MitiiTM), demonstrated potential for home-based interventions to augment therapy dose in order to enhance some outcomes [70]. An advantage of this particular system is the flexibility provided to the therapist to remotely monitor progress and adjust the challenges and tasks within the system. While the benefits of the MitiiTM system for children with unilateral CP extended beyond visual perceptual functions to enhanced daily activity performance, there were few differences in the trained tasks of speed and dexterity of the affected upper limb and lack of capacity to target fine motor manipulation. A dose-dependent response was identified [70]. Of note is that some children achieved less than 10 h of the 60-h protocol (6/47) whereas 10/47 completed 50 of the 60 h. Thus, it is unclear what the salient ingredients of the MitiiTM program were especially when considering the variability of engagement in the program over the 20-week trial. Limitations of VR and interactive computer systems in engaging children in therapeutic programs over extended periods have also been highlighted [71]. An assumption that video capture systems engage children is somewhat challenged by these recent studies. Additionally, these systems often, and importantly, do not encourage functional movement patterns that also reinforce the natural spatiotemporal relationship between sensory inputs and motor outputs—the body representation displayed digitally is removed from the performer’s egocentric frame of reference. Of particular concern is the delay in sensory feedback which may confound learning in immersed systems. If considering haptic feedback potentiated at 70–80 ms, and central motor conduction times (CMCT) of corticospinal tract connectivity (of typical contralateral tracts (CLT) of 3 to 5 ms), there may well be a confound between motor initiation, sensory feedback, and subsequent motor adaptation [72]. Systems that use gloves (and thus reduce haptic feedback) and that are dependent on visual feedback suffer further confounds. By comparison, use of tangible user interfaces (TUIs) affords more intuitive and direct forms of user interaction, efficient kinematics, and higher levels of presence, which support stronger treatment effects and greater generalization (e.g., [62, 73]). Off-the-Shelf Interactive Games The home entertainment industry has generated a number of affordable products with rehabilitation potential; at face value, leisure opportunities for children with disabilities as well as rehabilitation at the impairment level might be promoted. Figure 2 illustrates the areas in which evidence or potential


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Fig. 2 VR applications across dimensions of ICF [2]

Current applications of VR technologies across dimensions of ICF

Impairment Level

Activity Performance & Skill

Participation

Range of movement

Eating and drinking

Family activities

Posture and balance

Self-care

Social activities

Gait & mobility

Meal preparation

School activities

Reaching: kinematics

Play

Pre-vocational

Grasp & release: kinematics

Upper-limb function

Leisure

Cognitive control (incl. memory)

Community (e.g., shopping)

Social cognition & problem solving

Environment

Personal Factors

Physical and emotional support

Scaled for age

Equipment access & affordance via

Motivation/Interests

interfacing

exists for the use of VR technologies across ICF levels. Commercially available gaming consoles using motion sensors (such as the Nintendo Wii) offer low-cost VR therapy options (www.nintendo.co.uk) with compelling use of visual and auditory feedback. Data for commercial gaming systems, however, is also mixed for both CP and DCD. Interactive Games for CP In a study of spastic hemiplegic CP, Jelsma and colleagues [74] showed benefits from training on the Nintendo Wii Fit on clinical measures of balance control, but no transfer effects on functional measures. A case study using the Wii system also showed improved motor skill in a child with diplegic cerebral palsy; a minimum of 7 h of effective use of the system saw improved postural and functional mobility (e.g., distance walked with forearm crutches) [75]. See also recent data on the MitiiTM system described in the previous section. However, robust empirical data remain limited in childhood disability [70, 76]. Recent evaluations of off-the-shelf systems for children with hemiplegia are encouraging but are based on small samples. Applications vary across ICF domains targeting specific areas of impairment (upper-limb control), activity performance (meal preparation, street crossing, etc.), and participation (notably in leisure activities). Golomb et al. [77] showed improved manual ability (lifting objects) in three adolescents

with hemiplegic CP (HCP) using a combination of 5DT Ultra Glove and PlayStation3 game console. Such are relatively inexpensive and are easy to use for children with HCP. However, evaluation work has not yet separated the specific benefits of the VR system from the intensity and duration of training per se (13 to 25 h over 36–67 days, 8 h over 4 weeks, and 20 h over 4 weeks, respectively). The question of dosage is critical in determining the specific effects of VR and computer-based systems. James et al. [70] suggested that the first 20 h, consolidated into a short period, were the critical determinants of outcomes. Other intensive therapies such as constraint-induced movement therapy (CIMT) or hand-arm bimanual intensive therapy (HABIT) use protocols varying from 60 to 90 h over 2–8 weeks and show evidence of positive transfer to ADLs [56]. Interactive Games for DCD The Wii Fit has recently been used in a school lunchtime program to promote motor and psychosocial skills in children with DCD [78]. Importantly, children were engaged in a daily activity considered desirable by their non-DCD peers. Positive effects on balance and motor coordination were evidenced despite constraints to power and methodology. Ferguson et al. [79] also considered the use of Nintendo Wii Fit within a school setting in contrast to group-based task-focused intervention. Unfortunately, lack

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of comparable dosage restricts interpretation of outcomes. Similar to the studies in children with CP, there is potential for off-the-shelf systems to augment but not supplement standard therapies. In another recent study of DCD, Ashkenazi and colleagues [80] evaluated a short course of therapy (10 × 60-min sessions) using the Sony’s Playstation©-2 EyeToy. The system uses a web camera as a video capture interface to track limb gestures in two dimensions. A visual representation of the user is projected on a digital display and tracking enables the child to interact with virtual objects. Audiovisual feedback is provided to reinforce the success or otherwise of the movements, which are often target-directed within the context of a simple virtual game like volleyball or ten-pin bowling. Using a simple within-groups design and small sample of nine children, benefits of therapy were shown at post-test on the Movement Assessment Battery for Children (MABC) total score and balance sub-scale, and DCD-Q, the latter indicating some immediate but minor transfer to everyday performance. However, the research design was quite limited: natural recovery could not be ruled out, and follow-up assessments were not conducted. In a related study, the EyeToy was shown to be equally as effective as conventional perceptual-motor therapy for children with DCD on balance and functional mobility tasks [80]. Similar design issues were evident, however. The Nintendo Wii Fit system has also been compared with Neuromotor Task Training (NTT) in a recent South African study [79]. The study was notable for recruiting children aged 6–10 years from a low-income community in Cape Town; as such, around 90 % of children had never seen or used the Wii Fit before. Training consisted on 18 × 30-min sessions, spread over 6 weeks. The motor performance of both groups improved, as assessed on the MABC; however, effects were more limited to balance items and anaerobic capacity in the Wii intervention group, compared with more generalized benefits of NTT across motor skill and fitness items. Unfortunately, follow-up data were not collected. The authors did note that the level of engagement and enjoyment of children in both groups was high, which may have a number of positive flow on effects for self-esteem and movement confidence. Taken together, while the Wii Fit did not yield strong results on motor proficiency, the psychosocial outcomes of enhanced participation may be an equally important consideration in the longer term. VR-specific effects were also hard to disentangle from training intensity per se. In a related study, Jelsma and colleagues [81] studied a Wii Fit intervention in a group of children with probable DCD (aged 6–12 years) who experienced particular problems in balance control [81]. The period of intervention was 18 × 30min sessions, as per Ferguson et al., above. Using a half crossover design, results showed strong evidence for improved motor functioning in the intervention group, over and above natural recovery over a similar time period. Balance items


showed most improvement across MABC and BOTMP subscales. At the level of underlying mechanisms, these findings were suggested to reflect the ability of the intervention to provide AF and large numbers of learning trials in intense periods of training, enhancing implicit learning and predictive motor control (Wilson et al. 2013). In another study by Jelsma and colleagues [82], the shortterm learning profiles of children (5–11 years) on the Wii Fit ski slalom game were compared between South African and Dutch cultures. Intriguingly, the learning rates did not differ between cultural groups; however, the rates were somewhat less than that seen in a group of typically developing (TD) children [82]. Moreover, the two DCD groups did not trade speed for accuracy in the manner shown by the TD group, suggesting different task strategies. Importantly, the performance benefits of repeated practice on the slalom game were maintained after 6 weeks in all groups. Transfer of learning effects to motor skill in general were not a focus of this study. It is unclear whether this study involved some of the same children as the original 2013 paper above. Not all recent studies using commercial active video games (AVG) show encouraging results, however. Using a rigorous cross-over design, Straker and colleagues [83] reported no significant gain in motor function in DCD after a 16-week course of therapy involving AVG. The intervention included a range of non-violent games, played on PlayStation3 and MS Xbox360 with Kinect motion input. As such, the interface is quite different to the Wii Fit which involves more complex (whole body) postural adjustments. The Limits of Off-the-Shelf Interactive Games Off-theshelf systems are made with the typical child/user in mind, and require a requisite level of skill or neuromotor capacity to interact effectively with the virtual or other task environments [84]. Indeed, such systems are not designed to allow the user to vary task conditions—difficulty level, for example— below a typical entry point that would then invite or enable the participation of a child with a motor disability. Even when this provision is available within the system (e.g., MitiiTM), there are questions as to whether the therapist can remotely vary the challenges sufficiently to (a) target individual need, (b) promote specific motor skills that underpin functional deficits for each child, (c) increase challenges incrementally to maintain engagement of the child, and (d) provide appropriate feedback on performance that motivates the child to continue with the therapy. This presents an ethical and practical challenge to therapists. While mainstream commercial applications are often simply not usable or scalable for younger children with movement difficulties, the motor system of these children is likely to show high plasticity and be more responsive to adapted, virtual interventions [85]. Recent accounts of CP have highlighted the highly individualized way in which motor deficits and the accompanying sensory, perceptual,


cognitive, psychological, and communication deficits interact to express the functional impairment and disability [86–88]. With collaborative goal setting clearly in mind [89], virtual rehab systems must provide intuitive interfaces for interaction—the interface must enable identification of the goal of the activity and afford responses that are appropriate to the broader goals of therapy [68, 90, 91]. Avatar-Based Systems Targeting Everyday Activities As with off-the-shelf interactive computer games and VR systems, applications designed to target everyday functional activities in pediatric rehabilitation have shown short-term gains but lack evidence for far transfer over time [92]. Similar issues arise with trying to tease out the influence of engagement (and thus dosage) with particular salient ingredients of intervention such as the nature and timing of feedback. Virtual Tutor Systems Virtual tutor systems using desktop hardware were designed originally for patients with brain injury but have also been utilized in CP. Such systems present video simulations of goal-directed tasks (like reach and object placement) and then invite participants to reproduce these movements while providing various forms of AF in real time and post-performance [54]. Akhutina et al. [90] successfully used an avatar-based VE with additional desktop tasks for children with CP, including those with severe learning deficits. Children with lower levels of cognitive ability showed no training benefits (see also [68]). Despite this, there is some evidence that virtual tutors can assist children with intellectual disabilities to learn basic behavioral routines [93]. Customized Mixed-Reality Systems CP Building on earlier work with adult ABI [62, 94, 95], the Elements system has shown promise for children with mixed forms of hemiplegia (including CP). A multiple case study by Green and Wilson [84] showed significant benefits of the system for reaching and object placement in children with CP. Importantly, there was some evidence of positive transfer to daily functional activities such as ability to open doors and manual feeding. Enhanced engagement in therapy and the facilitating effects of AF were cited as important factors in learning and transfer. Interaction with multimodal VR interfaces may support the ability to acquire novel movements, particularly when adapted to the altered neuromotor constraints of the specific condition and/or the learning experiences required for performance of useful (pragmatic) actions [96]. However, well-controlled clinical trials are required to test whether these early results can be replicated in larger

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groups and/or extended to other pediatric populations including DCD. DCD The effects of customized haptic feedback in a virtual learning task have also been evaluated in probable DCD [97]. Here, learning profiles were examined in a task that required the child to follow a virtual path on a display by using a haptic VR stylus device (Phantom Omni; Sensable TechnologiesTM). The virtual path magnetically attracted the hand-held stylus, with the degree of support varied parametrically for each individual child; as performance improved, the degree of support was reduced. Results were notable in showing that children with DCD tended to catch up to TD peers over repeated learning trials. Unfortunately, a standardized motor screening test was not used here to validate group membership, so these results demand replication using a clinical group. Indeed, other learning studies are needed in the area of VR, with learning curves analyzed as a function of parametric changes in key task parameters. Cognitive Training in CP/DCD Cognitive deficits are often less obvious in children with CP or DCD than in patients with acquired brain injury like traumatic brain injury or stroke (for reviews, see [98, 99]) and are sometimes considered a less pervasive problem than motor deficits. However, children with CP or DCD have an increased prevalence of symptoms of reduced attention and working memory capacity, which has an impact on their reading, writing, and arithmetic performance [100–102]. Moreover, there is a lack of evidence of training interventions to improve cognitive deficits in CP or DCD. According to our knowledge, no studies so far have currently investigated the effect of cognitive intervention methods in these clinical groups. In a recent published study protocol by Løhaugen et al. [103], the authors propose a multicenter training study that will include 115 schoolchildren with CP (70 children with unilateral CP, 45 children with unilateral CP, 7–15 years) [103]. Children will train extensively for 5 to 6 weeks, about 30–45 min in each session (25 sessions in total). Training will be self-administered at home via the software Cogmed RobomemoTM. For full details and in depth description of this training program, the interested reader is referred to previous studies [104, 105] or www.Cogmed.com/rm. In brief, working memory capacity will be trained with computerized exercises of verbal (e.g., digits) and spatial (e.g., flashing lights) span tasks under various conditions such as repeating sequences in forwards or backwards order, repeating auditory verbal information with or without visual cues, and repeating sequences of flashing lights in stationary or rotating displays. Before the start of the training, immediately after training and 6 months post-training, all children will be assessed on neuropsychological measures, including the

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Developmental Neuropsychological Assessment (NEPSY). The findings of the proposed study will provide evidencebased knowledge towards the mechanisms underpinning cognitive training that may drive working memory improvement in CP and DCD. Participation—Outcome or Medium for Change (or Both)? The extent to which such systems promote not only specific motor or social competencies but also act as a mechanism for participation in meaningful social and leisure activities has yet to be explored. Children without disabilities are reporting an increased amount of time using computers and associated technologies [106, 107]. And there is growing evidence that many children, with and without disabilities, are engaging with computers and digital game technologies in both play and educational activities [65, 108–110]. While VR-based rehabilitation tends to focus on the impairment level, the outcomes of rehabilitation programs should target the development of motor competencies for enhanced participation across contexts. Scientific evaluation of VR systems in rehabilitation of CP has been fairly rudimentary, but is evolving. An early study by Akhutina et al. [90] showed motor performance gains as a result of VR training for children with complex impairments. Interestingly, training effects were relatively independent of the initial severity of both motor and cognitive impairments in the CP group [90]. In contrast, the results of Jelsma et al. [74] suggest a potential interaction effect between severity and the extent and nature of the therapeutic response. Consistent with the summary of Laufer and Weiss [65], greater detail on individual variation and patterns of responses is required in reports of intervention effects, particularly in order to better understand how applications are working and to optimize programs for individual children. Taken together, evidence in support of VR for children with CP is inconclusive. Current clinical guidelines emphasize the need for intensive motor-based and task-specific therapies such as constraint-induced movement therapy [111–113]. It is likely that VR-based approaches will ultimately fill a niche in therapy that enables practitioners, parents, and teachers to augment standard approaches; this will be felt across clinical, home, and school settings. The attributes of current and emerging systems that will best fill this niche are becoming clearer and are a focus of the next section.

Future Directions: Conceptual Design Considerations for Pediatric Virtual Rehabilitation The availability of consumer-driven interactive devices such as mobile technology, wearable displays, virtual reality, and behavioral sensing devices (e.g., MS Kinect, Fitbit) has led to


a broader acceptance of these technologies in clinical applications for CP and DCD. However, the challenge remains to design tasks and interfaces that are tailored to the particular therapeutic needs of these children and that are sufficiently engaging and motivating to use. We argue here and elsewhere (e.g., [84]) that future innovation in VR-based rehabilitation should address several issues that can best take advantage of the available and emerging technologies. Multi-modal AF The capacity of VR and related technologies to support motor learning through AF is an important design consideration for virtual rehabilitation. As discussed earlier, there is good theoretical reason to believe that provision of AF in its various forms can assist the child in developing predictive control and body schema [114, 115]. Current tracking and display technologies that can enable the provision real-time AF (with minimal lag) have been shown to be effective in motor therapy for children with severe motor and cognitive disabilities [116]. Both DCD and CP have been linked to underlying dysfunction in body schema and predictive control (aka internal modeling deficit [117]). Provision of multisensory AF may provide a treatment modality that can help children develop a more integrated body schema and prospective motor control. Is Tangible (and Curious) Better? A recent review of object use in therapy suggests that the affordance characteristic of real objects is more important than either their functionality or number [118]. TUIs that afford grasp and manipulation as well as provoking a sense of curiosity and Bconflict/impossibility^ around their use may in fact elicit more spontaneous actions; however, this has not been explored systematically using VR [119]. This effect of object affordance appears to be a function of the anticipatory nature of motor representations and motor planning [5, 120–122]. Objects that afford grasp, for example, but that convey little about the functional aspects of their use, can be used as a lever for participation in a therapy context. Mixed-Reality Environments Mixed-reality environments may help bridge the real-virtual divide and improve transfer of rehabilitation activities into everyday life (see [123]). Mixed-reality systems use realtime tracking of an individual’s movements relative to events presented in virtual environments, as well as direct perceptual feedback (e.g., AF) that arises from this interaction. As well, TUIs enable a direct and meaningful mode of interaction within VEs and avoid the potentially disorienting effects of


feedback delays that are a feature of many immersive VR systems (like those using head-mounted displays).

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illustrates the number of areas within the ICFDH framework [2] in which VR technologies have shown promise in promoting function and skills in young people.

Simulation, Action Observation, Imagery The tight functional relationship between action observation, motor imagery, and motor planning [124, 125] provides important pointers for task design in virtual rehabilitation. Action simulation using avatars may provide a way of priming the mirror system for movement. VR can provide a means of representing the child’s imitative action visually in a virtual space. Presentation of avatars from various perspectives (third person and egocentric) may scaffold the ability to imagine a modeled action and then imitation. Avatars that embody features of the individual child (vs. other) may also encourage egocentric mapping into the virtual workspace. It would be possible to scale up the complexity of these actions over time, starting with simple visually guided movements and progressing to more complex planning tasks involving several sequential movements. With advancements in technology, programs designed to teach motor imagery skills may be developed, enhancing predictive planning and priming of the motor system before execution. Co-located Rehabilitation Another use of mixed environments involves embedded groups of children in shared game-based VEs, designed to promote social understanding and prosocial behavior in children, particularly those with autism [126–128]. This approach shows potential in harnessing children’s interest in a mutual goal and promoting social learning for participation in play activities. Work by Kandalaft et al. [127] in young adults with high functioning autism shows that social skills developed in training do transfer to everyday social and occupational functioning. Further research is required to determine whether these skills transfer to other social contexts. While research to date has continued to focus on outcomes related to body function levels, participation in computer/VR games is an activity that is meaningful to children of varying abilities across educational, leisure, and social contexts. Weiss and colleagues [128] have begun to address this question in studies exploring use of the Diamond Touch system. This system is designed to develop social cognition to enhance interactive play. VR-based activities can be adapted and scaled flexibly to provide greater access for children with motor, social, and cognitive deficits, enabling participation not only with disabled peers but also able-bodied children. Children with physical disabilities rarely have the opportunity to Bcompete^ in physical activities on an equal playing field with their Bnon-disabled^ peers. VR has the potential to bridge this gap. Figure 2

Conclusion Use of VR and related technologies in rehabilitation is an emerging field in the area of neurodevelopmental disorders. System development and evaluation work in CP has gained momentum over the past 10–15 years, with more recent examples in DCD, albeit confined largely to off-theshelf systems. Of the latter, recent evaluations have been promising, showing evidence of skill development and near transfer. There is currently little evidence for the translation of specific gains shown in field evaluations to longer-term functional gains. This reflects not only some of the limitations of recent study design but also the relatively early stage of research in this field, which has not yet evolved beyond the proof of concept stage. In relation to study design, it has not been possible to dissect how person-related (e.g., motivation and capacity), task, and environmental factors have been modified to effect change. Treatment targeting specific skills such as reaching and grasping should not be considered in isolation from the motivational elements of goal setting, game play, performance, and knowledge of results (KR). Children need to be engaged in the therapeutic process for therapy to be effective [89], supporting generalization across specific skills to activity participation. VR technologies have the potential to expand the opportunities available for engaging children in therapeutic activities across physical, social, and cognitive domains. Indeed, past limitations that restricted access and extension into community and other settings are being superseded by recent advances in portable, low-cost devices. However, Battendance^ and Binvolvement^ are now construed as critical aspects of participation in rehabilitation, implying a paradigm shift towards a collaborative process of treatment [129]. There is a need to identify levels of engagement from the patient/child perspective and use this information to revamp system design and service delivery. Indeed, feedback from individuals with neurodisability, their family, and clinicians can contribute to an iterative design process, informing our understanding of accessibility, usability, modes of user interaction, preferred hardware platforms, and general workspace design [3, 130]. The challenge for (ecological) intervention design is the breadth of areas that may need to be addressed when taking into consideration individual experiences and perspectives, as well as the practical and financial barriers in health care delivery. Meeting this challenge will determine the future of VR-based rehabilitation.

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Compliance with Ethical Standards Conflict of Interest Peter Wilson, Dido Green, Karen Caeyenberghs, Bert Steenbergen, and Jonathan Duckworth declare that they have no conflict of interest.

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17. Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects performed by any of the authors. 18. 19.

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