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NeuroRehabilitation 25 (2009) 2944 29

DOI 10.3233/NRE-2009-0497
IOS Press

Sensorimotor training in virtual reality: A


review
Sergei V. Adamovich a,b,, Gerard G. Fluetb , Eugene Tunik b and Alma S. Meriansb
a
New Jersey Institute of Technology, Department of Biomedical Engineering, University Heights, Newark, NJ, USA
b
University of Medicine and Dentistry of New Jersey, Department of Rehabilitation and Movement Science,
Newark, NJ, USA

Abstract. Recent experimental evidence suggests that rapid advancement of virtual reality (VR) technologies has great potential
for the development of novel strategies for sensorimotor training in neurorehabilitation. We discuss what the adaptive and engaging
virtual environments can provide for massive and intensive sensorimotor stimulation needed to induce brain reorganization.
Second, discrepancies between the veridical and virtual feedback can be introduced in VR to facilitate activation of targeted
brain networks, which in turn can potentially speed up the recovery process. Here we review the existing experimental evidence
regarding the beneficial effects of training in virtual environments on the recovery of function in the areas of gait, upper extremity
function and balance, in various patient populations. We also discuss possible mechanisms underlying these effects. We feel
that future research in the area of virtual rehabilitation should follow several important paths. Imaging studies to evaluate the
effects of sensory manipulation on brain activation patterns and the effect of various training parameters on long term changes
in brain function are needed to guide future clinical inquiry. Larger clinical studies are also needed to establish the efficacy of
sensorimotor rehabilitation using VR in various clinical populations and most importantly, to identify VR training parameters
that are associated with optimal transfer to real-world functional improvements.

Keywords: Virtual reality, virtual environment, sensorimotor training, rehabilitation

1. Introduction the presence or absence of somatosensory feedback


and the modality used to collect data from the partici-
Virtual reality (VR) can be defined as an approach to pant. Visual stimuli are grouped by the level of immer-
user-computer interface that involves real-time simula- sion. Two-dimensional presentations are considered
tion of an environment, scenario or activity that allows non-immersive. Three dimensional presentations uti-
for user interaction via multiple sensory channels [19]. lizing stereoscopic projections or displays with a fixed
VR technology, and its application, is rapidly expand- visual perspective are considered semi-immersive. Ful-
ing across a variety of disciplines. Virtual environ-
ly immersive systems allow for changing visual per-
ments (VEs) in VR can be used to present richly com-
spective with head movement. There are a myriad of
plex multimodal sensory information to the user and
methods of collecting data from a subject. Some sys-
can elicit a substantial feeling of realness and agency,
despite its artificial nature [105]. tems utilize joysticks, hand controls or steering wheels.
Virtual reality systems are generally classified by Motion tracking systems that utilize video and op-
the visual presentations they provide to a participant, toelectronic cameras, electromagnetic and ultrasound
sensors, accelerometers and gyroscopes provide kine-
matic data. Instrumented gloves can add precision to
Address for correspondence: Sergei Adamovich PhD, Motor
tracking of hand motion. The data collected from these
Control and Rehabilitation Laboratory, Department of Biomedical
devices is used to control a computerized representation
Engineering, New Jersey Institute of Technology, 665 Fenster Hall,
University Heights, Newark, NJ 07102, USA. Fax: +1 973 596 5222; of the user or an avatar that represents their movements
E-mail: sergei.adamovich@njit.edu. and interacts with the VE. Video capture virtual reality

ISSN 1053-8135/09/$17.00 2009 IOS Press and the authors. All rights reserved
30 S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review

(VCVR) is a family of video camera based motion cap- 2. Why might training in VR be beneficial for
ture systems that record and digitize pictures of partic- restoring neural function?
ipants as they move, and transfer those images into a
virtual environment, in real time [123]. These systems Recent studies show evidence of the potential of VR-
differ from other forms of VR in terms of their visual based interventions to benefit patients with disordered
presentation which is a mirror image of the participant. movement due to neurological dysfunction. Known
Flicker glasses that display alternating right/left views neurophysiological and behavioral benefits of move-
ment observation [8,18,25], imagery [20], repetitive
of the picture or head-mounted visual displays (HMD)
massed practice and imitation therapies [42] in facili-
may be used for greater immersion (for both gait and
tating voluntary production of movement can be eas-
upper extremity systems). The most immersive system
ily incorporated into VR to optimize the training ex-
is the CAVE (University of Illinois at Chicago) which perience and allow the clinician to use sensory stimu-
is a room-size, 3D video and auditory system. Finally, lation through VR as a tool to facilitate targeted brain
newer systems that utilize robots to provide interaction networks, such as the motor areas, critical for neural
forces between the user and VE are classified as haptic and functional recovery. The potential for function-
systems. Several systems like GENTLE-S [27], MIT- al recovery can be optimized by tapping into a num-
Manus [1] and PneuWREX [127] can be used to pro- ber of neurophysiological processes that occur after a
vide haptic effects during upper extremity activities in brain lesion, such as enhanced potential for neuroplas-
VEs. LOKOMAT (Hocoma) is a robotic exoskeleton, tic changes early in the recovery phase and stimulation
while CAREN System (Motek) utilizes self-paced mo- of sensorimotor areas that may otherwise undergo dete-
torized treadmills mounted on a 6 degree-offreedom rioration due to disuse. VR may be useful in a number
motion. These systems are designed to facilitate gait of ways to deal with these processes and potentially
training, and both systems can be integrated with VE by trigger compensatory neuroplastic changes.
presenting virtual locomotion scenarios displayed on a
2.1. Mass practice
screen in front of the subject. The CAREN system can
be combined with a harness for safety or body weight
Animal and human studies have shown that impor-
support. tant variables in learning and relearning motor skills
Many disciplines of healthcare now rely on VR, such and in changing neural architecture are the quantity, du-
as for training surgeons [80], delivery of cognitive ther- ration and intensity of training sessions. There is evi-
apy [102], and delivery of post-traumatic stress disor- dence to demonstrate that plasticity is use-dependent
der therapy [108]. The use of VR for sensorimotor and intensive massed and repeated practice may be
training is a promising addition to its already broad necessary to modify neural organization [57,87,88,118,
utility in healthcare. Initial investigations into this fam- 120,128]. The importance of intensity and repeti-
ily of approaches to rehabilitation emerged in the mid tion has also been confirmed for stroke patients in the
1990s. Several reviews summarize the first generation chronic phase [119] in the treatment paradigm referred
of this research [52,63,107,117,123], with more recent to as constraint-induced-movement-therapy (CIMT).
systematic reviews examining the clinical efficacy of Use-dependent cortical expansion has been shown up to
sensorimotor training in VE for rehabilitating upper ex- 6 months after 12-days of CIMT therapy in people post
tremity function [49] and gait [29] after stroke. This stroke [78]. Dependence on existing therapies alone
to promote neuroplastic changes might not always be
review adds to the existing literature by integrating the
practical. For example, changes at the synaptic level
above studies with more recent reports, some emanat-
are evident in the rodent brain after the animal is ex-
ing from our laboratories, that discuss how spatial and
posed to thousands of repetitions of a given task over a
temporal manipulations in VR may be used intelligent- short interval of time, i.e. 12,000 repetitions over 23
ly to enhance sensorimotor training, and how they can days [88,101]. In stark contrast, the affected extrem-
be interfaced with robotics for rehabilitation purposes. ity is moved at best 12 hours/day in the weeks after
We conclude with a discussion of the development and stroke [10,11] and as few as 1020 repetitions per train-
efficacy of telerehabilitation applications, which can be ing session in the chronic phase [74]. More than 50%
interfaced with VR to improve the accessibility of VR of this time is spent on rehabilitating the lower extrem-
to the broader patient population. ities and balance rather than the hand [5860]. Use of
S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review 31

VR as a training environment may provide a rehabili- aspect of VR is its versatility in presenting complex
tation tool that can be used to exploit the nervous sys- sensory stimulation, through a combination of visual,
tems capacity for sensorimotor adaptation by provid- somatosensory (haptic), and auditory feedback. Intel-
ing a technological method for individualized intensive ligent manipulation of these parameters may offer the
and repetitive training. clinician a yet unattained level of control over the ther-
apeutic efficacy of a given intervention. The current
2.2. Dynamic and operant conditioning of skill state of the art in using these approaches is reviewed
below.
In addition to the training intensity and volume nec-
essary to induce neural plasticity, sensorimotor stimu-
lation must involve the learning of new motor skills. 3. Effects of visual augmentation on neural circuits
Empirical data strongly emphasize that learning new
motor skills is essential for inducing functional plastic- In order to understand the potential of VR to bene-
ity [68,89,101], therefore, it appears that critical vari- fit recovery at the functional outcomes level in patient
ables necessary to promote functional changes and neu- populations, one needs to understand the neural pro-
ral plasticity are the dynamic and adaptive development cesses that VR may be affecting and, in the case of
and formation of new motor skills. It is believed that patient populations, how VR may affect recovery at the
adaptive training paradigms that continually and inter- neural level. A related and equally important question
actively move the subjects performance toward the tar- is whether interacting in VR engages similar neural
geted skill are important to optimize re-learning of mo- circuits to those recruited for actions performed in the
tor skills [79]. Once again, VR-based applications can real-world.
provide adaptive learning algorithms and graded reha- The wiring of the brain lends nicely to using visual
bilitation activities that can be methodically manipulat- feedback in VR to augment distributed, but intercon-
ed to meet this need. nected, cortical regions. For example, retrograde trac-
er studies show rich intra-hemispheric cortico-cortical
2.3. VR delivered during critical periods to augment connections that link occipital, parietal, and frontal cor-
neuroplastic changes tices [76,77,113]. Moreover, single unit recordings
demonstrate that a substantial number of motor, premo-
One of the central problems facing patients and clini- tor, and parietal neurons are modulated by visual infor-
cians is that most interventions are impractical to deliv- mation [4547,62], suggesting that visual information
er to patients at perhaps the most opportune time, that can provide a potent signal for reorganization of sen-
is during the acute phase of stroke when the potential sorimotor circuits. At the behavioral level, movement
to harness neuroplastic changes is greatest but during errors in the visual domain can influence motor corti-
which phase the patient is too paretic to perform hand cal areas during motor learning [15,48,84,85,104] and
training. If the same principle that is apparent in the de- active / rewarded practice, can be used to reduce move-
veloping nervous system of cats applies to the lesioned ment errors through feedback, and can shape neural
adult cortex of humans, that lack of stimulation to mo- activity in motor and premotor areas [15,126]. Finally,
tor cortex during a critical period leads to lost corti- even observation of actions (images and video clips), if
cospinal synaptic connections [36] and that stimulation performed repetitiously and intentionally, can facilitate
of motor cortical networks during the same critical pe- the magnitude of motor evoked potentials (MEPs) and
riod can reinstate some of these otherwise lost connec- influence corticocortical interactions (both, intracorti-
tions [109], then the acute paretic phase in stroke may cal facilitation and inhibition) in the motor and premo-
perpetuate functional and neural deterioration simply tor areas [75,93,112,115]. This work provides a strong
due to absence of cortical stimulation. foundation for testing hypotheses on the possible ef-
The above sections provide an overview of the mul- fects that can be produced through visual feedback in
tifaceted components in skill re-acquisition, such as VR and opens possibilities for clinical application.
mass practice, rich environments, and timing of VR An important consideration in the use of VR as a
delivery that may mediate neuroplasticity following a sensorimotor training tool is the quality of VE render-
lesion. The versatility of VR in these respects offers ing compared to what we are used to perceiving in the
the clinician various ways to modulate brain reorga- natural world. In other words, the fidelity of the VR
nization. However, perhaps an even more appealing environment may be an important factor in its effec-
32 S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review

tiveness to recruit neural circuits and deliver desirable the virtual hand avatar seen in 1st person perspective
outcomes at the functional level. Although VE can and animated by pre-recorded kinematic data. These
be used to provide sophisticated visual information to blocks were interleaved with rest periods during which
users and elicit a feeling of real presence [105,106], subjects viewed static virtual hand avatars, control tri-
some work suggests that observation of actions per- als in which the avatars were replaced with moving
formed by virtual effectors (i.e. the hand) may be less non-anthropomorphic objects, or with blocks in which
effective in recruiting neural circuits than observation subjects imitated the finger sequence under the above
of real hand actions [95]. In a study by Perani, the feedback condition. Our data showed a time-variant in-
authors used fMRI to measure the blood oxygen level- crease in activation in the left insular cortex for the ob-
dependent (BOLD) signal as subjects observed high- serve with the intent to imitate condition but not in the
fidelity and low-fidelity renderings of a virtual hand other conditions. Moreover, imitation with veridical
perform a reaching task and compared these conditions feedback from the virtual avatar (relative to the control
with a control in which subjects observed real hand ac- condition) recruited the angular gyrus, precuneus, and
tions. The authors found that both virtual conditions extrastriate body area, regions which are (along with
produced significantly smaller activation in the fron- insular cortex) associated with the sense of agency [4].
toparietal circuit that was recruited in the real condi- Thus, the virtual hand avatars may be useful for senso-
tion. rimotor training by serving as disembodied tools when
However, other evidence suggests that sensorimo- observing actions and as embodied extensions of the
tor training in VR may actually have similar effects to subjects own body (pseudo-tools) when practicing the
those noted after real-world training. This evidence actions.
comes from several domains. First, studies that have The above data inform of potentially useful appli-
compared the kinematics of movements performed dur- cations of visual manipulation in VR. For example,
ing interaction in a virtual visual environment to those intentional observation of movement can be used to
when acting in the real world have found remarkable stimulate the sensorimotor system without necessitat-
similarities. For example, healthy subjects responding ing overt movement itself. Adding more sophisticated
to targets moving at different velocities exhibit simi- manipulations in VR, such as to the color/brightness
lar movement time, path curvature time, time to peak of objects, their location, form, perspective (1st versus
velocity, and reactions times whether the task is per- 3rd person), temporal/spatial distortions of the move-
formed in a VE or in the real world [33]. Interestingly, ment trajectory, and feedback replays, can perhaps po-
stroke patients kinematics for reachto-grasp move- tentiate these effects in ways that cannot be achieved
ments also show similarities in peak wrist velocity, an- in the natural world. For example, simulating forward
gular shoulder/elbow relationship and maximum grip motion by using an optic flow field, and manipulating
aperture when acting in the virtual versus a real envi- the speed of the illusory motion during gait training in
ronment [122]. stroke patients, one can facilitate either faster or slower
In two studies performed on persons with stroke, walking speeds [73].
functional improvements following VR training were Another example of a sophisticated VR-based ma-
paralleled by a shift from a predominantly contrale- nipulation emerges from an intervention called mirror
sional sensorimotor activation pre-therapy to a predom- visual feedback therapy, introduced by Ramachandran
inantly ipsilesional activation post-therapy [54,129]. and coworkers [7] for amputee and stroke patients. We
Similar shifts in hemispheric lateralization are observed developed a virtual mirror feedback interface and have
after therapy performed in the real world [24,111], sug- used it in conjunction with fMRI to study the effects of
gesting that training an affected limb in VR may tap in- this form of visual feedback on neural circuits. In our
to similar neural reorganization processes as observed study [82], a stroke patient performed movements with
after training in the real world. the unaffected hand that, with the aid of manipulations
Our own work extends this by demonstrating that in the VE, animated either the corresponding or con-
interacting with virtual representations of ones own tralateral virtual hand model (in real time). Our find-
hands in VR recruits brain regions involved in attri- ings revealed that activations in the sensorimotor cortex
bution of agency [6]. To study such brain-behavior of the affected hemisphere (the inactive cortex) were
interactions, we integrated our VR system with fMRI significantly increased simply by providing feedback
and asked thirteen healthy subjects to observe, with of the contralateral hand. This effect was also evident
the intent to imitate, finger sequences performed by in healthy subjects. In a follow up experiment, we mea-
S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review 33

sured the MEPs in motor cortex [2], as healthy subjects for other patient populations, we review those as well.
were exposed to the same feedback conditions as in the Although the evidence generally supports VRs effi-
fMRI study. Our data indicated that MEPs were sub- cacy in retraining upper extremity (UE) function after
stantially increased in both feedback conditions (cor- stroke, the majority of these studies include case stud-
responding and contralateral virtual hand models) but ies, small feasibility studies, or studies without strong
that the MEP amplitude increased by about 8% more in control groups. Stroke rehabilitation training programs
the contralateral relative to the corresponding feedback are most effective when requiring practice regimens
condition. This is in direct line with similar studies that that both engage and increasingly challenge the pa-
have used a real, rather than a virtual, mirror feedback tient [13]. VR can aid in this sense by systematically
setup [37,39,43] and adds to the body of evidence that adapting task difficulty to the patients ability as he/she
suggests that sensorimotor training in VR may have progresses through training and by providing a moti-
similar effects on neural circuits to real-world training. vational factor to encourage longer engagement in the
The advantage of VR, however, is its versatility to allow exercises than would otherwise be seen in a real-world
more control over the type of feedback. environment [30].
Studies on the use of non-VR presentations of visual Multiple authors describing the training of upper ex-
stimulation support the possibility of this type of train- tremity reaching and functional activities in virtual en-
ing. A study of horizontally flowing visual information vironments have shown that motor skills can be learned
on healthy persons that were stationary produced acti- through repetitive practice within both immersive and
vation of the visual cortex and a corresponding decrease non-immersive and visually simple and complex virtual
in the vestibular areas in a PET scan study by [28]. The environments (see [49] for an extensive review). More
authors postulated that this was a strategy to resolve the recent studies have also shown similar results. Stewart
sensory conflict produced by these conditions. Brandt et al. [114] describe a VR system that allows subjects to
et al. showed activation of adjacent areas of the visual perform complex 3-dimensional tasks involving object
cortex and deactivation of multisensory vestibular cen- manipulation and/or reaching. Following a twelve ses-
ters in a PET scan study of healthy persons in response sion intervention with this system, one of the two pilot
to large field optokinetic stimuli [32]. Similar findings subjects demonstrated improvements at the impairment
were described by Konen et al. in an fMRI study of and functional level. Piron and colleagues compared
normal responses to optokinetic stimulation and pur- a group of subjects less than 3 months after a middle
suit/scanning type movements [70]. In an fMRI study cerebral artery stroke [97]. Twenty-eight subjects per-
of persons with chronic bilateral vestibular failure, sub- formed upper extremity rehabilitation activities in a vi-
jects visual cortex activation was stronger in response sual and auditory based, 2-dimensional virtual environ-
to simulated visual motion than in healthy controls. ment and a second group of 13 subjects performed a
The investigators describe this as an up-regulation of comparable volume of conventional upper extremity re-
sensitivity to visual stimuli as a compensation for a lack habilitation. The VR rehabilitation group made statisti-
of vestibular information [31]. Each of these studies cally significant gains on impairment (UE Fugl-Meyer)
support the use of visually simulated movement to elicit and functional independence measures (FIM) while the
this functional activation/deactivation pattern when the conventional rehabilitation group made smaller, non
brain is presented with conflicting information (simu- significant improvements in these measures.
lated visual motion in a stationary subject). These studies have focused on upper extremity train-
ing. Because of fiscal constraints, current service deliv-
ery models favor gait-training and proximal arm func-
4. Visual feedback only in VR tion [18]. However, the impact of even mild to mod-
erate deficits in hand control effect many activities of
The preponderance of evidence for the therapeutic daily living with detrimental consequences to social
use of VR has come from intervention studies in the and work-related participation. In our own laborato-
stroke patient population. The reason for this is in part ry, a group of eight subjects with mild to moderate
attributed to the high prevalence of stroke and the partic- hemiparesis secondary to stroke performed 13 sessions
ular challenges that upper extremity movement deficits of sensorimotor training in virtual environments that
pose to rehabilitation. Given the above, the following provided rich visual feedback as the subjects played 5
sections are weighted in reviewing VR applications for game-like activities targeting independent finger flex-
stroke populations, however, where data is available ion, finger strength, and finger extension speed. Sub-
34 S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review

jects improved in measures of independent finger flex- per and pencil tests [16]. Training in VR has shown
ion, finger speed, strength and range of motion mea- improvement in learning to cross a busy street, with left
sured during training tasks as well as in kinematic mea- to right ratio scores (the ratio of objects seen on left to
sures of reaching and grasping and clinical tests of up- those seen on right) decreasing [23] and in reaching and
per extremity function. The Jebsen Test of Hand Func- grasping activities, where after training patients were
tion (JTHF) [56], a timed test of hand function and able to code objects in the neglected space identically
dexterity, was used to determine whether the kinematic to those presented in their preserved space [9]. How-
improvements gained through practice in the VE mea- ever, it was found that only patients without lesions in
sures transferred to real world functional activities. Af- the inferior parietal/superior temporal regions benefited
ter training, the average time the subjects needed to from this last training paradigm.
complete the six subtests of the JTHF with their hemi- VR neglect intervention is not limited to ambulatory
plegic hand decreased significantly. In contrast, no patients. Virtual environments have been used to assess
changes were observed for the unaffected hand. The spatial attention and neglect in wheelchair navigation.
subjects affected hand improved from pre-therapy to Here the subjects were asked to navigate a virtual path,
post-therapy on average by 12% [5]. encountering objects of varying complexity while in a
We have recently developed a second generation of wheelchair [21]. The VR navigation task was shown
this system. The piano trainer is a refinement and elab- to have a strong correlation with the live wheelchair
oration of one of our previous simulations [81]. The navigation task, and was able to detect deficits in mild
new version consists of a complete virtual piano that patients. This implies VR shows promise as an effi-
plays the appropriate notes as they are pressed by the cient, sensitive measure of assessment and training for
virtual fingers. The position and orientation of both spatial neglect.
hands as well as the flexion and abduction of the fingers A patients gait, or walking pattern, can be signif-
are recorded in real time and translated into 3D move- icantly altered after a stroke. Virtual realty (VR) of-
ment of the virtual hands, shown on the screen in a first fers a variety of methods to assess and improve several
person perspective. The simulation can be utilized for aspects of patient gait post-stroke. VR offers signif-
training the hand alone to improve individuated finger icant advantages over the traditional, qualitative, low
movement (fractionation), or the hand and the arm to- intensity methods of physical therapy. VR enables the
gether to improve the arm trajectory along with finger therapist to control duration, intensity, and feedback
motion. This is achieved by manipulating the octaves during specified treatment. The best VE is one that
on which the songs are played. These tasks can be done immerses and engages the subject in a realistic manner.
unilaterally or bilaterally. Other simulations provide To this end several modalities of human-computer in-
practice in the integration of reach, hand-shaping and terface have been employed [29]. Environments simu-
grasp using a pincer grip to catch and release a bird lating both city and rural landscapes have been used for
while it is perched on different objects located on dif- gait rehabilitation after stroke. These environments are
ferent levels and sections of a 3D workspace [24], see used to retrain gait by providing visual cues to augment
also below, pp. 3738. gait parameters such as stride length and walking ve-
In addition to upper extremity movement deficits locity, as well as objects in the environment to augment
after stroke, spatial neglect is another common syn- obstacle avoidance. Walking speed is often severely
drome following stroke, most frequently due to damage reduced after stroke. Perception of the speed of ones
of the right hemisphere. Up to two-thirds of patients environment has been shown to have an influence on
with acute right-hemisphere stroke demonstrate signs the modulation of walking. Several VR studies have
of contralesional neglect, failing to be aware of visual, been conducted to quantify this effect. One study used
auditory and or tactile stimuli coming from left of their VR to make continuous adjustments to the perception
midline in extrapersonal space. Hemispatial neglect of optic flow speed [40]. Tests showed an inverse re-
has profound effects on the patients ability to inter- lationship between the VR optical flow speed and the
act with and respond to their environments [64]. VR walking speed, of patients after a stroke, though the
simulations have been employed with some success in correlation was weaker than that found in healthy sub-
several studies for both the assessment and treatment of jects. In more recent studies, VE complexity of the
visuo-spatial and visuo-motor neglect [55]. With man- city and rural landscapes has grown to include more
ual exploration tasks, VR applications can detect small life-like scenarios of street walking, collision avoid-
variations in performance undetectable by standard pa- ance and park strolling. In a small study, using scenar-
S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review 35

ios of walking in a corridor, a park and across a street, 4.2. Use of visual feedback in VR for posture and
and a motorized treadmill and a 6 dof motion platform, balance rehabilitation
patients benefited from this practice by increasing their
walking speed and adapting their gait to the changes in The appropriate control of posture and balance un-
the terrain [41]. derlies most functional skills and is achieved through
timely integration of sensory information. For fall pre-
4.1. Use of visual feedback in VR to treat Cerebral vention, this integration requires rapid recalibration of
Palsy visual, vestibular and somatosensory information. Dis-
Children with Cerebral Palsy (CP) have difficulty orders of the nervous system and aging lead to impair-
controlling and coordinating voluntary muscle activi- ments in this mechanism. VR can be used in several
ty. In neuro-rehabilitation, these difficulties combined ways to re-train postural control and balance. First, VR
with the typical mentality of a child, can make this pop- can be used to manipulate visual feedback to produce
ulation challenging. Traditional therapies for muscle conflicts between visual, somatosensory and vestibular
movement are repetitive and offer very little to keep a information as a way to train different sensory systems.
young mind occupied. Interactive VEs can provide a Second, VR feedback can be systematically graded (in
much wider array of activities and scenarios for muscle terms of speed and complexity) in order to challenge
movement. In a selective motor control study of CP a persons static and dynamic postural control over the
patients [17], children were asked to complete several course of sensorimotor training.
ankle exercises using both video capture based training Small sample investigations on the ability to manip-
and conventional programs. While conventional ther- ulate visual stimuli in order to evoke conflict between
apy yielded more repetitions of the required exercises, visual, vestibular and somatosensory systems and cor-
the range of motion and hold time of stretch positions responding changes in vestibular symptoms or postural
were greater in the VR group, thus the benefit of any responses have produced promising results. Scanning
movements was much greater during the VR exercises. in complex visual environments can produce sensory
Approximately 50% of all children with CP sus- conflict. Whitney et al. found that training in immer-
tain upper-extremity dysfunction to some degree [26]. sive VR may be useful for habituation activities for
VRs application extends well into this large area of persons with visual/vestibular impairments. Using an
neuromuscular rehabilitation. We have written above immersive grocery store simulation, a subject with sub
about the motivating advantages to VR. This obviously acute labyrinthine dysfunction experienced compara-
extends to UE exercises. A recently completed study ble symptoms to those she experienced in a real world
was able to incorporate commercially available video grocery store. There was a correlation between the vi-
games into their treatment regimen [26]. The study sual complexity of the simulation and her symptoms
also revealed that to detect the full benefits of VR in as well. Interestingly, a second subject with a more
a patient can require more sensitive diagnostic meth-
chronic lesion had adapted to this conflict and did not
ods than are normally employed in physical and occu-
experience symptoms in this environment [125].
pational therapy (e.g. Peabody Developmental Motor
Immersive VR systems producing flow past a users
Scale, QUEST exam).
peripheral visual fields also produce a sense of motion
In addition to measurable changes in physical ac-
tivity, VR has also shown promise in effecting neuro- similar to the optokinetic stimuli described by Brandt
plasticity in CP patients. fMRI analysis, prior to VR and Dieterich [31,32]. The perception of self motion
training of the upper extremity of a child with hemi- this information creates can be manipulated in VE to
plegic CP, showed predominately bilateral activation elicit specific postural adjustments for training and re-
of the sensorimotor cortices and ipsilateral activation habilitation purposes. In a study on healthy subjects
of the supplementary cortex. After training in a video visual stimuli that produced a conflict with simulta-
capture-based VR system, this bilateral activation dis- neous somatosensory and vestibular signals generat-
appeared and the contralateral sensorimotor cortex was ed by horizontal motion elicited much stronger postu-
activated [130]. These recorded changes were closely ral corrections measured by EMG than those produced
associated with enhanced ability of the subject to per- by either horizontal motion or simulated visual motion
form reaching, dressing, and self-feeding tasks. VRs alone [66]. In another study on twelve healthy sub-
ability to create widely varying scenarios with a spec- jects, center of pressure and perception of vertical mea-
trum of difficulty also lends itself to gait training in CP sured with a wand in the subjects hand was collect-
patients [69]. ed as subjects were presented with optic flow in three
36 S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review

planes (yaw, pitch and roll). The effect of complexi- Several studies describe simple virtual rehabilita-
ty of the visual flow patterns on postural response and tion interventions for persons with other neurologic
perceived vertical was greatest in the roll plane and pathologies. Fulk reported a case utilizing a VR-based
much less robust in pitch. Responses to varying levels balance intervention for a woman with MS. The subject
and complexities of visual flow in the pitch plane var- performed a 12 week course of bodyweight support-
ied significantly between subjects [65]. A third study ed ambulation training combined with non-immersive
by Keshner and colleagues described an increased ef- balance activities [38]. The subject improved her
fect of visually simulated motion on postural respons- gait speed, endurance and standing balance measures.
es when subject base of support was decreased, mak- Thornton compared VR-based balance interventions
ing them more dependent on the erroneous, simulated and clinical balance activities in a group of patients
visual information [116]. with traumatic brain injuries. Two groups performed
Mulavara et al. examined the responses of 30 healthy either activity based balance training or balance exer-
subjects to linear or rotating patterns of optic flow while cises in a 2 dimensional VR system. VR participants
walking straight on a treadmill. Subjects demonstrated expressed higher degrees of enjoyment, made larger
adaptation to the condition of flow they were presented. improvements on quantitative measures of balance and
Subjects displayed a consistent right bias on an eyes scored higher on balance confidence measures [121].
closed stepping task immediately following walking Pavlou et al. performed a comparison of conventional
with a right rotating pattern of optic flow, and subjects vestibular rehabilitation activities and exposure to vi-
presented with linear flow in the same plane and direc- sual vestibular conflict produced by an immersive VR
tion of their walking displayed no consistent bias [86]. system as part of a simulator based treatment that also
These studies, illustrate the ability of immersive vir- included rotary chair and other whole body movement
tual environments to impact the integration of visual, simulations. The VR / simulator treatment group made
vestibular and somatosensory inputs and subsequent larger changes on posturography tests and larger im-
postural responses. The incorporation of this element provements in symptoms intensity questionnaires than
into rehabilitation programs with the goal of hasten- the conventional rehabilitation group [94].
ing the adaptation process in persons with vestibular The safety of VE-based balance training also makes
pathology and to train postural responses in persons it an effective tool for fall prevention interventions in
with balance impairments are the logical next steps elderly populations. VE can provide distracting envi-
for this line of inquiry. ronments or additional cognitive tasks, two conditions
Several authors discuss the use of balance training in- associated with increased frequency of falls in the el-
terventions using VR in a variety of populations. Odds- derly. Bisson and colleagues studied two groups of el-
son et al. studied balance training in a tilted room envi- derly subjects, one that trained on balance activities us-
ronment simulated by lying on a surface that eliminat- ing visual biofeedback displaying force-plate data and
ed friction while being presented with virtually simu- a second performing juggling activities that required
lated immersive visual environments. Healthy subjects lateral reaches in a VCVR environment. Both groups
trained in the virtual environment made improvements achieved statistically significant improvements in reac-
in mediolateral critical time with eyes closed [90]. tion time, and the Community Balance and Mobility
Training in VR allows for the safe and systematic train- Scale [12].
ing of sitting balance in persons with SCI. Kizony et
al. studied the feasibility of applying VCVR technolo-
gy for balance training in persons with paraplegia in a 5. Integration of vision and haptics in VR
study with 13 subjects. Subjects utilized three 3D sim-
ulations, two that involved reaching for moving targets A major development in the use of virtual environ-
and a third that utilized trunk movement to control a ments has been the incorporation of tactile information
snowboard. Users expressed that they enjoyed utilizing and interaction forces into what was previously an es-
the equipment and reported high levels of presence dur- sentially visual experience. Robots of varying com-
ing the activities. The subjects scores on the simula- plexity are being interfaced with more traditional VE
tions correlated well with their performance on a seat- presentations to provide haptic feedback that 1) enrich-
ed functional reaching task, suggesting that their real es the sensory experience, 2) adds physical task param-
world balance and ability to perform the simulations eters, and 3) provides forces that produce biomechani-
measured a similar construct [67]. cal and neuromuscular interactions with the virtual en-
S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review 37

vironment that approximate real world movement more be applied to manipulate objects that vary in size and
accurately than visual only VEs. shape allowing for customization based on therapeutic
Simple haptic feedback can be utilized to add the goals [72]. Haptic forces can also be synchronized with
perception of contact to skills like kicking a soccer ball visual feedback to improve a users sense of agency
or striking a piano key. Lam et al. describe a system in the virtual world. In two small studies involving
that utilized vibratory discs to simulate the feeling of healthy subjects, this feedback combination was found
impact during this type of game. The authors cited to be more effective for skill learning than visual only
advanced skill learning in a group of healthy subjects feedback in healthy subjects [53,110]. The distortion
training with added tactile feedback [71]. Adamovich of forces in a virtual environment is another line of
et al. used a force reflecting exoskeleton that simulates inquiry afforded by haptics. Patton et al. found that
contact with piano keys [2]. Collisions with virtual haptic forces that augmented the errors of subjects with
world obstacles can also be used to teach normal move- strokes were more effective in teaching desired trajec-
ment trajectories such as the action required to place an tories than haptic forces that guided subjects toward
object on a shelf [4] or step over a curb [124]. these trajectories. These effects were found in sim-
Some previous approaches utilized virtual tutors to ple two dimensional VE [92] and an immersive three
model ideal trajectories [51,99]. Using haptic obsta- dimensional VE [91].
cles to indirectly shape trajectories may avoid the ef- Our laboratory has developed a VR system that uti-
fects of the explicit, cognitive process associated with lizes visual and haptic feedback for the sensorimotor
presenting a model, into what is usually an implicit training of the hemiparetic upper extremity, specifically
process [14]. Further investigations into this potential to train arm reaching and hand manipulation in three-
advantage are necessary because of the significant in- dimensional space. For the upper arm training, each
creases in cost associated with adding haptic effects subject trained using 2 different, 3-dimensional virtual-
to virtual rehabilitation applications. Haptic environ- ly simulated reaching activities over the course of eight
ments can also exert global forces on the user such or nine sessions. Task one had subjects pick up cups
as antigravity support and viscous stabilization forces. off of a haptically rendered table and place them on
This allows more disabled subjects to exercise reaching haptic shelves. Collisions with the table shelves and
and object manipulation in 3D space, which invokes other cups were solid, forcing subjects to alter their
muscular force synergies that are typically used and, trajectory to complete the task. Task two required sub-
advertently, more appropriate neuromuscular feedback jects to move through a standardized set of targets with
as well. Several authors employ these concepts in VR no obstacles. In a group of four chronic stroke sub-
simulations designed to train reaching, grasping, and jects [4], subjects demonstrated a 36% improvement in
lifting. Wolbrecht et al. describe a haptic robotic inter- task duration, and a 45% improvement in hand trajec-
face that provides anti-gravity assistance as needed to tory smoothness on the task with no obstacles. The
lower functioning persons as they interact with virtual same subjects demonstrated a 42% reduction in task
environments. They tested this approach on nine per- duration, and a 70% improvement in hand trajectory
sons with chronic hemiparesis secondary to stroke. As smoothness during the task that utilized haptic obsta-
a group these subjects improved on kinematic measures cles. These subjects seemed to respond to the inde-
during robotic training and clinical measures of upper pendent condition of haptically rendered obstacles with
extremity function [127]. Our laboratory has investi- more efficient learning. Future studies of this concept
gated the feasibility of this assist as needed approach should include a larger sample, generalization testing
for the arm [4] as well as the hand [2]. Subjects in both and measurements of motor control.
studies performed extended training periods in a short For practice in hand manipulation, for patients with
period of time without adverse effects and made similar greater impairments, the piano trainer (see p. 34) can be
kinematic and real world functional improvements. combined with a force reflecting exoskeleton that can
Other tasks involve contact and interaction with tools inhibit mass grasp patterns and/or provide for haptical-
to achieve movement goals. In the real world, object ly rendered finger tip collisions. In a proof of concept
manipulation produces an interaction between user and study, three of our subjects utilized the CyberGrasp ex-
object that is unique (e.g. the angular momentum of oskeleton to facilitate extension of their inactive fin-
the head of hammer). Haptics can simulate the in- gers while utilizing the virtual piano trainer for eight
teraction forces produced by tools in virtual environ- to nine, sixty to ninety-minute sessions. Each of these
ments. Lambercy et al. describe a haptic knob that can three subjects were in the chronic stage of their stroke
38 S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review

recovery and were classified as level 5 hemiparesis for only. Eight chronic subjects with a similar level of
their arms and level three hemiparesis for their hands mild hemiparesis (JTHF pre-test of 140) performed a
using the Chedoke McMaster Stroke Impairment In- comparable volume of training resulting in a 10% im-
ventory [44]. Two of the three subjects made improve- provement in JTHF time, approximately half of the im-
ments in their scores on the Jebsen Test of Hand Func- provements experienced by the subjects using our total
tion (by 13% and 11%). It appears that further in- training approach.
vestigation of this approach for persons with moderate
upper extremity hemiparesis is warranted. 5.1. Use of visual and haptic feedback in VR for gait
It is controversial whether training the upper extrem- rehabilitation
ity as an integrated unit leads to better outcomes than
training the proximal and distal components separate- Several interesting studies have been generated eval-
ly. Current rehabilitation practice describes the need uating the integration of the LOKOMAT, a robotic gait
to develop proximal control and mobility prior to ini- orthosis and virtual environments. Wellner et al. de-
tiating training of the hand. During recovery from a scribe a series of experiments manipulating point of
lesion the hand and arm are thought to compete with view, haptic collisions and augmented auditory feed-
each other for neural territory. Therefore, emphasizing back with a group of healthy subjects as they step over
virtual obstacles with a goal of developing an optimal
initial proximal training may actually have deleterious
training program for gait rehabilitation. Subjects in
effects on the neuroplasticity and functional recovery
these experiments were more successful when provid-
of the hand. However, neural control mechanisms of
ed with haptic feedback from collisions with the virtu-
arm transport and hand-object interaction are interde-
al obstacle, and with a lateral view of themselves and
pendent. Therefore, complex multisegmental motor
their obstacle during training. Furthermore, subjects
training is thought to be more beneficial for skill reten-
expressed that auditory feedback that cued them regard-
tion. We used this system to examine the effectiveness
ing increased gait speed and the distance to approach-
of training the hand and arm as a functional unit. The
ing obstacles was helpful [124]. Tierney et al. describe
virtual simulations used in this protocol include; 1) a
the design of a system for the gait rehabilitation of per-
three dimensional pinching task, (the arm transports sons with strokes utilizing a partial body weight support
the hand to the appropriate place to catch a flying bird system. The authors propose that the normalization of
and the fingers perform a pinching movement to place gait speed afforded by BWS gait training, paired with
it on a tree), 2) a pong based game (the arm moves semi-immersive virtual environments simulating real-
to control the paddle and finger extension engages the world ambulation situations may provide more ecolog-
paddle allowing participants to compete with a live or ically valid stimuli for gait rehabilitation (unpublished
computerized opponent, 3) a realistic full sized virtual observations).
piano keyboard and 4) a three-dimensional hammering It is not clear which component of this system pro-
game, in which the arm controls the position of the vides the positive effects the robotic assistance or the
hammer in 3D space and finger flexion and extension VR. Mirelman et al. described an additive effect of VR
controls the rotation of the hammer as it interacts with simulations to robotic training for gait when compared
the target. to a similar volume of robot-only training [83]. This
In an ongoing study, a group of 8 subjects with chron- study compared two groups of subjects with strokes
ic strokes resulting in mild hemiparesis (mean Jebsen who performed ankle exercises utilizing the Rutgers
Test of Hand Function (JTHF) score = 152), trained Ankle, a six degrees of freedom robot. Nine subjects
for three hours in each of 8 sessions over two weeks performed these activities in a VE. Nine more per-
using these 4 simulations. Each subject demonstrated formed the same program receiving knowledge of re-
improvements in robotically collected kinematics but sults and performance feedback from a therapist. VE
more importantly, the group demonstrated a mean im- group subjects made larger improvements in gait speed,
provement in JTHF of 21% (SD = 15%) and a cor- six minute walk test and community ambulation dis-
responding improvement in Wolf Motor Function Test tance as measured by a pedometer. All of these com-
Aggregate Time of 24% (SD = 11%) (unpublished parisons reached statistical significance and were main-
observations). This data compares quite favorably to tained at three month follow-up. Six of the nine subjects
a study we published previously [5,81], in which we in the VE group made improvements in their gait ve-
trained subjects using an earlier iteration of our sys- locity that were large enough to change their functional
tem practicing tasks that emphasized finger movement ambulation category as defined by Perry et al. [96].
S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review 39

5.2. Use of visual and haptic feedback in VR to treat lations utilizing this array included an obstacle course,
Cerebral Palsy wading in a stream, crossing a street and performing a
virtual soccer activity. To date, proof concept studies
A critical limitation of the vision-only VR technol- performed on healthy subjects utilizing questionnaires
ogy for the CP population is the high degree of motor have confirmed the realism of these simulations [69].
function required to access many formats of this tech-
nology. One approach to overcome this issue is the
interfacing of virtual environments with robotic assis- 6. Telerehabilitation
tance to allow participation of more involved patients.
To date, only a handful of small studies have utilized Access to rehabilitation services in rural and other
interactive haptic environments to train children with underserved areas is a critical healthcare issue. Telere-
CP. Our laboratory has investigated the feasibility of habilitation systems (TRS) are one of the approaches
the combination of robotically facilitated movements being developed to address this issue. Many TRS incor-
with rich VE and complex gaming applications. Qiu porate some form of VE in their presentation. Several
et al. describe the experience of two children with the authors have investigated upper extremity interventions
NJIT-RVR system. One of the children made a 45 utilizing TRS in pilot studies. Two studies examined
improvement in active supination and the other sub- the efficacy of TRS based interventions for the hemi-
ject demonstrated clinically significant improvements paretic UE. In one study, impairment level and func-
on the Melbourne Assessment of Upper Extremity Per- tional assessments approached statistically significant
formance after training in VR for one hour per day, 3 levels of improvement after TRS training of gross UE
days a week for three weeks [103]. movements and finer grasping movements [51]. Carey
One of the important assets of VE systems for the et al. examined two groups performing finger exercise
rehabilitation of children is their flexibility. Simple without direct supervision. The experimental group
alterations to graphics and sound effects significantly performed a tracking task presented via a TRS. Con-
improved time on task and attention levels in the chil- trols performed a home exercise program consisting
dren described above. For example, we have success- of a similar volume of non-goal oriented finger move-
fully developed and tested a reaching simulation where ments. While clinical testing results were similar for
adults with strokes received adaptable robot assistance the two groups, fMRI activation during a finger track-
during reaching in three-dimensional space presented ing task was higher in the TRS group after training.
in stereo [4]. The same activity seemed to be not that The results of this study indicate that even the sim-
interesting for CP children under 10. Adding simple plest form of interactive visual feedback during sen-
sound and visual effects to the activity (simulating ex- sorimotor training might be beneficial for facilitation
plosions of the target objects) was sufficient to substan- of brain activation [22]. Heuser et al. utilized the
tially improve attention levels and compliance in this Rutgers Master II, a haptic glove system, in a thirteen
group of 8 children with hemiparetic CP [35]. This session telerehabilitation intervention that utilized VR
flexibility will allow therapists to tailor the presenta- simulations for 5 persons post surgery for carpal tunnel
tion of complex interventions to the developmental and syndrome. Three of the five subjects made substantial
cognitive constraints presented by the diverse group of strength gains measured clinically and all of the sub-
CP patients. jects expressed satisfaction with their telerehabilitation
In a recent study, Fasoli et al. [34] describe a group experience [50].
of 5 to 12 year old children with UE hemiplegia sec- The studies above begin to establish effectiveness of
ondary to CP performing16, sixty minute practice ses- TRS interventions but do not test for the independent
sions in a simple virtual environment with assist as condition of remote supervision. Deutsch et al. exam-
needed robotic facilitation over an eight week period. ined the effects of utilizing a TRS by having subjects
Each session, consisted of 640 repetitive, goal-directed with strokes perform ankle rehabilitation activities in
planar reaching movements. Subjects demonstrated a VE while supervised in person by a therapist. After
improvements in Quality of Upper Extremity Test and three weeks of intervention the subjects performed the
Upper Extremity Fugl-Meyer Assessment scores [34]. same protocol with remote supervision by a therapist.
Finally, one study was able to use the LOKOMAT gait The subjects performance and the volume of activity
orthosis in conjunction with VEs to create a realistic performed during week four, the remote supervision
haptic world designed to treat children with CP. Simu- week, was comparable to week three, suggesting that
40 S.V. Adamovich et al. / Sensorimotor training in virtual reality: A review

remote monitoring would not detract from the produc- back, and can provide adaptive learning algorithms and
tivity of the session [29]. graded rehabilitation activities that can be objective-
A study by Piron et al. compared 12 patients with ly and systematically manipulated to create individual-
stroke performing a remotely monitored telerehabili- ized motor learning paradigms. Thus, it provides a re-
tation program for their hemiparetic UE, and another habilitation tool that can be used to harness the nervous
group of 12 subjects with stroke, performing a similar systems capacity for sensorimotor adaptation.
program of real-world UE activity in their homes su- Virtual rehabilitation for movement disorders has
pervised by a therapist. Both groups made comparable been developing more slowly than virtual technologies
improvements in UE function and untrained reaching in other areas of healthcare. In our opinion there are
kinematics [98]. A second study by Piron et al. [100] several factors underlying this trend. System develop-
compared two groups of 5 subjects with strokes, one ment involves sophisticated interlacing between hard-
that trained UE movements in a VE while supervised ware and software which at the present time is expen-
in person by a therapist and a second performing the sive and requires considerable development expertise.
same VE simulated training program and supervised by The interdisciplinary nature of rehabilitation research
a therapist remotely, using video-conferencing equip- also presents challenges. The design of interfaces to ac-
ment. The TRS group in this study made statistically commodate persons with impaired movement requires
significant improvements in motor performance while skills that span orthopedics, neuroscience, biomedical
the in-person supervision group changes were not sta- engineering, computer science and multiple rehabili-
tistically significant [100]. While each of these studies tation disciplines. More studies are emerging to test
cites comparable or superior benefits for TRS, these VRs efficacy in rehabilitation, however, the effective-
studies were small indicating a need for further study ness of these studies has not yet reached he higher levels
with larger numbers of patients. of evidence found in large scale randomly controlled
The use of telerehabilitation is in the nascent stage
studies. The extent to which repetitive training offers
of development and implementation. While the results
neural and functional benefits beyond the novelty fac-
of these small VR-based studies examining the clinical
tor as well as the ability to integrate this form of ther-
effectiveness of TRS are promising it is important to
apy into a clinical setting remains unknown. Finally,
note that large studies that have evaluated the cost ef-
and perhaps most important, the full potential of VR
fectiveness, and practicality of implementation of tel-
will only emerge after we gain a thorough understand-
erehabilitation services in comparison to hospital based
ing of how various sensory and haptic manipulations in
services have shown mixed results [61].
VR affect neural processes. These issues should be a
central focus of future investigations.
7. Conclusions, limitations, and future directions

Virtual reality technology may be an optimal tool Acknowledgements


for designing therapies that target neuroplastic mech-
anisms in the nervous system, allow for mass practice This work was supported in part by the Nation-
and provide training in complex environments that are al Institute on Disability and Rehabilitation Research,
sometimes impractical or impossible to create in the Rehabilitation Engineering Research Center Grant #
natural world. They also allow for access to rehabilita- H133E050011.
tion services through telerehabilitation. Computerized
systems are well suited to this and afford great precision
in automatically adapting task difficulty based on indi-
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