The TBI group displayed reaches that were characterized by shorter distances, lower peak velocities, and smaller postural displacements than reaches in the control group. All participants reached ~9% farther in the VE presented at a 50° angle than they did in the PE. Arm displacement in the VE at the more natural 10° angle was reduced by the same 9-10% compared to the PE. Virtual reaches were slower than reaches performed in the PE. Overall, the results provide evidence that the VE modifies arm reaching while standing in patients with TBI and in healthy individuals. The environment must be viewed at a particular oblique angle that deviates from the natural view that is typically used to observe the real physical world. In TBI participants, the performance in PE reaches correlated with the severity of motor deficits, whereas visual perceptual abilities affected the performance in the VE.
As a result of the various pathological mechanisms following a brain injury [
10‐
13], a deficit in functional reach characteristics was present in all our participants with TBI. Reaching-to-point movements mostly involve trunk and proximal segments of the body, whereas the manual dexterity requirements are minimal. Thus, the lack of fine hand/finger coordination, which is common among survivors of brain injury, was unlikely to underlie the functional reach deficit. The observed restricted reaching abilities may be attributed to abnormal postural control and to the reduced distance that a person can intentionally displace his or her COM by leaning in a given direction without losing balance, stepping, or grasping a supporting surface. In rehabilitation literature, this ability is referred to as the “limit of stability” and is used as a quantitative measure of postural control [
30,
31]. The limit of stability is sensitive to even small changes in sensorimotor function [
32,
33], and affects the performance of daily life activities in vulnerable individuals [
34]. The clinical scores on the BBS and FGA, together with reduced COM displacements confirm impairments of postural control in our TBI participants. This can explain their reduction in functional reach abilities compared to healthy individuals. The results are consistent with other studies in patients with stroke [
35], multiple sclerosis [
36], children with TBI [
37], and older individuals [
21,
30,
31].
Virtual versus physical reaches
Despite the absolute difference in arm displacements, participants in both groups showed increased reaching distance in the VE, although with some reservations. In particular, the virtual scene had to be viewed at an oblique angle for positive outcomes to be observed. In addressing the differences between physical and virtual reaches, this study does not aim to uncover the specific neural mechanism(s) that facilitate the reach-to-point movement in a VE. Because the true mechanisms and potential neural substrates controlling the movements of a body representation (avatar) in an artificially generated 3D environment are not well understood, further explanations of this phenomenon may be considered as speculative. Functional reaches performed in the VE differed from movements made in an equivalent PE. Consistent with the results of previous works [
38,
39], virtual reaches were slower, had lower peak velocities, and had longer movement times. These features characterize the reaching performance as an exploratory behavior, rather than as an established movement pattern. When exploring a novel environment, an animal as well as human is not yet aware of the task-specific boundaries. In this situation, the final result is unpredictable and may either exceed expectations or be underachieved. Partially supporting this hypothesis, arm reaching in the VE projected in an oblique plane was extremely beneficial for participants, whereas reaching outcomes in other conditions either declined or remained unchanged.
An exploratory nature of movement behavior in a VE may be induced by several factors. Despite recent progress in 3D projection technology, an artificial computer-generated VE distorts visual perception [
40]. Observing the environment via goggles typically reduces the field of view, limits the visual resolution acuity, and affects the natural accommodation and vergence mechanisms of the human gaze system, thereby degrading depth cue information [
41]. According to previous studies, participants in a VE underestimate distances and perceive objects as being closer than they are [
42,
43]. Consequently, the user is unsure of the object location in the VE and applies a series of corrective motions, which typically slow down the arm in its approach to a final destination. Confirming this statement experimentally, Subramanian and Levin [
44] showed that arm pointing to a virtual target is influenced by viewing media in healthy individuals and patients with stroke. Authors found that viewing the virtual target via head mounted display with reduced field of view changed visual perception accordingly. This resulted in less accurate arm pointing, compared to that performed toward the target projected on a large screen and viewed via polarized glasses. Another factor altering movement performance in VE is a lack proprioceptive feedback. This feedback is necessary for accurate, precise, and predictable reaching-to-point movement [
45], which was distorted in our participants as they reached for virtual objects. Finally, the reach-to-point movement in the VE was completed with a hand avatar and not with the index finger as in the PE. Rather than an anatomical extension of the hand of the participant, the avatar is a tool or instrument that needs to be mastered. Motor behaviors associated with complex manual tool use arise from functionally different brain networks, which are typically used for simple reaching and grasping in humans [
46]. This explanation may help clarify the VE-induced modification of arm movement in our experiment.
All of the above explanations suggest that our participants might employ different central motor programs during the PE and VE reaches. In the PE, the reaching pattern was formed long before an actual movement started and was based on a subjective estimation by the participant of how far he or she could reach without loss of balance. In other words, the final arm destination was determined before an actual movement began, and few adjustments were applied by the CNS in the process of performance. In the VE, the movement took longer and allowed time for the participant to change his or her final arm position, as well as to modify the performance pattern. The result of adjustment could be either increase or decrease of the reaching distance. These observations suggest that the VE can be a powerful instrument for manipulating human motor behavior, once we learn how to use it efficiently.
Participants with TBI improved their reaches by 7 cm in the VE, and by 4 cm in the PE after performing a series of virtual trials. The reaching increase in our participants fell in the range (3.7–11 cm) of minimal detectable changes established for functional reach tests in vulnerable individuals [
47,
48]. This fact does not confirm the clinical significance of practicing in a VE, nor does it suggest that practice in VE is more efficient than in the PE. Repetition of the same number of reaches in the PE only could potentially result in an equivalent change. The results of the study do suggest, however that the VE practice can be used as an efficient therapeutic instrument in the rehabilitation of individuals with acquired brain injuries. Successful learning transfer requires that the skills have similar elements, have similar mechanisms of sensory corrections, and be practiced in similar contexts [
49]. In this regard, VR-based technologies are the most advantageous in simulating any type of environment, with feedback and sensory conditions closely matching real ones. As another experimental confirmation, after practicing the virtual tasks, participants with TBI showed a significant improvement in their performance of real-world movements, such as pouring a cup of water [
50].
Improvements of PE reaches in control individuals were much more modest than those in TBI participants. Most likely, their initial performance was very close to a maximum ceiling that could not be exceeded. Once the ceiling was reached, the control individuals had very little room for improvement, which was not the case in participants with TBI.
Effect of viewing angle
The second goal of the study was to test the effect of manipulating the viewing angle on reaching distance in patients with TBI. Patients reached farther when the scene was presented at a mid-view angle, whereas reaching distance in the more natural view was shorter. These results support our previous study [
20], which utilized the same experimental paradigm and showed that healthy young individuals demonstrate the largest reaches toward a more oblique target (flower). In intact brains, viewing a target under oblique angles changes the activities of the cortical and subcortical areas, which are involved in visuomotor integration [
51,
52]. Numerous studies have also reported that viewing a target under a more oblique plane alters the estimated object properties and distances [
53,
54], increases the isometric muscle force [
55], and facilitates the performance of cognitive tasks, such as reading a book and watching a display [
56,
57].
These changes may be mediated by several mechanisms, such as through proprioceptive feedback from extraocular muscles. Finding a target located more obliquely activates muscles that are normally relaxed when looking straight ahead. Through a chain of brainstem reflexes, this proprioceptive feedback modifies the activity of the neck muscles that, in turn, affects postural and motor control [
58‐
60]. Another mechanism altering motor and postural responses may be a different depth perception of the virtual hedge. A hedge presented in a mid-view angle may provide a participant with greater depth perception than the more natural view (10° angle). The consequent changes in eye vergence [
61] do not need to be large to influence motion and posture [
59]. Finally, the mid-view angles may be more convenient for reaching even in a PE, by providing a better presentation of the properties of the object. This aspect, however, was not investigated in detail.
Overall, the participants with TBI altered their reaching movements in response to the viewing angle in a similar manner as healthy individuals. In the TBI group, the performance of virtual reaches moderately correlated with visual perceptual deficits. These visual perceptual deficits included impaired visual discrimination, visual memory, visual spatial relations, and visual motor integration. The results suggest that the visual perception likely needs to be intact to allow for the maximum efficient use of the VE for motor skills retraining after brain injury. Furthermore, this may be true for a simple goal-directed movement, such as reaching-to-point while standing, but may not include highly coordinated manipulative actions. The lack correlation between motor abnormalities and reaches in the VE, but not in the PE was unexpected. Perhaps the clinical scales were not chosen correctly to reflect the complexity of symptom manifestations in our TBI participants. Another possibility is that virtual and physical reaches require different abilities, and as a result they are affected differently by brain injury-related sensorimotor abnormalities. All these explanations are rather speculative and require further investigation.