Comparison of uni- and multimodal motion stimulation on visual neglect: A proof-of-concept study.

Spatial neglect is characterized by the failure to attend stimuli presented in the contralesional space. Typically, the visual modality is more severely impaired than the auditory one. This dissociation offers the possibility of cross-modal interactions, whereby auditory stimuli may have beneficial effects on the visual modality. A new auditory motion stimulation method with music dynamically moving from the right to the left hemispace has recently been shown to improve visual neglect. The aim of the present study was twofold: a) to compare the effects of unimodal auditory against visual motion stimulation, i.e., smooth pursuit training, which is an established therapeutical approach in neglect therapy and b) to explore whether a combination of auditory + visual motion stimulation, i.e., multimodal motion stimulation, would be more effective than unimodal auditory or visual motion stimulation. 28 patients with left-sided neglect due to a first-ever, right-hemispheric subacute stroke were included. Patients either received auditory, visual, or multimodal motion stimulation. The between-group effect of each motion stimulation condition as well as a control group without motion stimulation was investigated by means of a one-way ANOVA with the patient's visual exploration behaviour as an outcome variable. Our results showed that unimodal auditory motion stimulation is equally effective as unimodal visual motion stimulation: both interventions significantly improved neglect compared to the control group. Multimodal motion stimulation also significantly improved neglect, however, did not show greater improvement than unimodal auditory or visual motion stimulation alone. Besides the established visual motion stimulation, this proof-of-concept study suggests that auditory motion stimulation seems to be an alternative promising therapeutic approach to improve visual attention in neglect patients. Multimodal motion stimulation does not lead to any additional therapeutic gain. In neurorehabilitation, the implementation of either auditory or visual motion stimulation seems therefore reasonable.

Effects of Virtual Reality-Based Multimodal Audio-Tactile Cueing in Patients With Spatial Attention Deficits: Pilot Usability Study.

BACKGROUND: Virtual reality (VR) devices are increasingly being used in medicine and other areas for a broad spectrum of applications. One of the possible applications of VR involves the creation of an environment manipulated in a way that helps patients with disturbances in the spatial allocation of visual attention (so-called hemispatial neglect). One approach to ameliorate neglect is to apply cross-modal cues (ie, cues in sensory modalities other than the visual one, eg, auditory and tactile) to guide visual attention toward the neglected space. So far, no study has investigated the effects of audio-tactile cues in VR on the spatial deployment of visual attention in neglect patients. OBJECTIVE: This pilot study aimed to investigate the feasibility and usability of multimodal (audio-tactile) cueing, as implemented in a 3D VR setting, in patients with neglect, and obtain preliminary results concerning the effects of different types of cues on visual attention allocation compared with noncued conditions. METHODS: Patients were placed in a virtual environment using a head-mounted display (HMD). The inlay of the HMD was equipped to deliver tactile feedback to the forehead. The task was to find and flag appearing birds. The birds could appear at 4 different presentation angles (lateral and paracentral on the left and right sides), and with (auditory, tactile, or audio-tactile cue) or without (no cue) a spatially meaningful cue. The task usability and feasibility, and 2 simple in-task measures (performance and early orientation) were assessed in 12 right-hemispheric stroke patients with neglect (5 with and 7 without additional somatosensory impairment). RESULTS: The new VR setup showed high usability (mean score 10.2, SD 1.85; maximum score 12) and no relevant side effects (mean score 0.833, SD 0.834; maximum score 21). A repeated measures ANOVA on task performance data, with presentation angle, cue type, and group as factors, revealed a significant main effect of cue type (F30,3=9.863; P<.001) and a significant 3-way interaction (F90,9=2.057; P=.04). Post-hoc analyses revealed that among patients without somatosensory impairment, any cue led to better performance compared with no cue, for targets on the left side, and audio-tactile cues did not seem to have additive effects. Among patients with somatosensory impairment, performance was better with both auditory and audio-tactile cueing than with no cue, at every presentation angle; conversely, tactile cueing alone had no significant effect at any presentation angle. Analysis of early orientation data showed that any type of cue triggered better orientation in both groups for lateral presentation angles, possibly reflecting an early alerting effect. CONCLUSIONS: Overall, audio-tactile cueing seems to be a promising method to guide patient attention. For instance, in the future, it could be used as an add-on method that supports attentional orientation during established therapeutic approaches.

Visual Neglect after PICA Stroke-A Case Study.

After cerebellar stroke, cognition can be impaired, as described within the framework of the so-called Cerebellar Cognitive Affective Syndrome (CCAS). However, it remains unclear whether visual neglect can also be part of CCAS. We describe the case of a patient with a subacute cerebellar stroke after thrombosis of the left posterior inferior cerebellar artery (PICA), who showed a left-sided visual neglect, indicating that the cerebellum also has a modulatory function on visual attention. The neglect, however, was mild and only detectable when using the sensitive neuro-psychological Five-Point Test as well as video-oculography assessment, yet remained unnoticed when evaluated with common neglect-specific paper-pencil tests. Three weeks later, follow-up assessments revealed an amelioration of neglect symptoms. Therefore, these findings suggest that visual neglect may be a part of CCAS, but that the choice of neglect assessments and the time delay since stroke onset may be crucial. Although the exact underlying pathophysiological mechanisms remain unclear, we propose cerebellar-cerebral diaschisis as a possible explanation of why neglect can occur on the ipsilateral side. Further research applying sensitive assessment tools at different post-stroke stages is needed to investigate the incidence, lesion correlates, and pathophysiology of neglect after cerebellar lesions.

Development of a Search Task Using Immersive Virtual Reality: Proof-of-Concept Study.

BACKGROUND: Serious games are gaining increasing importance in neurorehabilitation since they increase motivation and adherence to therapy, thereby potentially improving its outcome. The benefits of serious games, such as the possibility to implement adaptive feedback and the calculation of comparable performance measures, can be even further improved by using immersive virtual reality (iVR), allowing a more intuitive interaction with training devices and higher ecological validity. OBJECTIVE: This study aimed to develop a visual search task embedded in a serious game setting for iVR, including self-adapting difficulty scaling, thus being able to adjust to the needs and ability levels of different groups of individuals. METHODS: In a two-step process, a serious game in iVR (bird search task) was developed and tested in healthy young (n=21) and elderly (n=23) participants and in a group of patients with impaired visual exploration behavior (ie, patients with hemispatial neglect after right-hemispheric stroke; n=11). Usability, side effects, game experience, immersion, and presence of the iVR serious game were assessed by validated questionnaires. Moreover, in the group of stroke patients, the performance in the iVR serious game was also considered with respect to hemispatial neglect severity, as assessed by established objective hemispatial neglect measures. RESULTS: In all 3 groups, reported usability of the iVR serious game was above 4.5 (on a Likert scale with scores ranging from 1 to 5) and reported side effects were infrequent and of low intensity (below 1.5 on a Likert scale with scores ranging from 1 to 4). All 3 groups equally judged the iVR serious game as highly motivating and entertaining. Performance in the game (in terms of mean search time) showed a lateralized increase in search time in patients with hemispatial neglect that varied strongly as a function of objective hemispatial neglect severity. CONCLUSIONS: The developed iVR serious game, "bird search task," was a motivating, entertaining, and immersive task, which can, due to its adaptive difficulty scaling, adjust and be played by different populations with different levels of skills, including individuals with cognitive impairments. As a complementary finding, it seems that performance in the game is able to capture typical patterns of impaired visual exploration behavior in hemispatial neglect, as there is a high correlation between performance and neglect severity as assessed with a cancellation task.

Test-Retest-Reliability of Video-Oculography During Free Visual Exploration in Right-Hemispheric Stroke Patients With Neglect.

The Mean gaze position during free visual exploration (FVE) is a sensitive tool to detect neglect in patients after a right-hemispheric stroke. Here we investigated the test-retest-reliability of mean gaze position during FVE in 23 patients with left-sided neglect after a first-ever sub-acute right-hemispheric stroke. We analyzed the reliability between different test sets administered within 11 days (test sets A and B, each including different images and their mirrored versions), and between repeated measures using the same test set administered three times within 2 days (test set C, including the same images and their mirrored versions). The intra-class correlation coefficient (ICC) showed good reliability between the two different test sets (test sets A and B; ICC = 0.819), and excellent reliability for the repeated measures with the same test set C (ICC = 0.964). FVE can therefore be recommended for the longitudinal assessments of patients' neglect severity during neurorehabilitation as well as in treatment trials.

Visual Exploration Area in Neglect: A New Analysis Method for Video-Oculography Data Based on Foveal Vision.

Video-oculography during free visual exploration (FVE) is a valuable tool to evaluate visual attention spatial allocation in neglect patients after right-hemispheric stroke. In conventional FVE analyses, the position of a visual fixation is conceived as a single point in space. Here, we describe a new complementary method to analyze FVE data based on foveal vision, leading to an accurate estimate of the portion of the picture that was effectively explored. In 15 neglect patients and 20 healthy controls, visual exploration areas (i.e., considering 1° visual angle around every single fixation) were computed. Furthermore, the proportion of single and overlapping fixations was analyzed. Overlapping fixations were further categorized into capture fixations (successive overlapping fixation, putatively reflecting problem of disengagement) and re-capture fixations (temporally distant overlapping fixations, putatively reflecting spatial working memory deficits). The results of this new analysis approach were compared to the ones of conventional approaches. Conventional analyses showed the typical visual attention deficits in neglect patients versus healthy controls: significantly less fixations and time spent within the left and significantly more fixations and time spent within the right screen half. According to the results of our new approach, patients showed a significantly smaller visual exploration area within the left screen half. However, the right visual exploration area did not differ between groups. Furthermore, in neglect patients, the proportion of overlapping fixations within the right screen half was significantly higher than within the left screen half, as well as significantly higher than in healthy controls within either screen halves. Whereas neglect patients showed significantly more capture fixations than healthy controls, the number of re-capture fixations did not differ between groups. These results suggest that, in neglect patients, the efficiency of visual exploration is also reduced within the right screen half and that impaired disengagement might be an important mechanism leading to overlapping fixations. Our new analysis of the visual exploration area, based on foveal vision, may be a promising additional approach in visual attention research. It allows to accurately measure the portion of the picture that was effectively explored, disentangle single from overlapping fixations, and distinguish between capture and re-capture fixations.