Feasibility of Eye Tracking Assisted Vestibular Rehabilitation Strategy Using Immersive Virtual Reality
Jeong Hye Park, Han Jae Jeon, Eun-Cheon Lim, Ja-Won Koo, Hyo-Jeong Lee, Hyung-Jong Kim, Jung Seop Lee, Chang-Geun Song, Sung Kwang Hong, Jeong Hye Park, Han Jae Jeon, Eun-Cheon Lim, Ja-Won Koo, Hyo-Jeong Lee, Hyung-Jong Kim, Jung Seop Lee, Chang-Geun Song, Sung Kwang Hong
Abstract
Objectives: Even though vestibular rehabilitation therapy (VRT) using head-mounted display (HMD) has been highlighted recently as a popular virtual reality platform, we should consider that HMD itself do not provide interactive environment for VRT. This study aimed to test the feasibility of interactive components using eye tracking assisted strategy through neurophysiologic evidence.
Methods: HMD implemented with an infrared-based eye tracker was used to generate a virtual environment for VRT. Eighteen healthy subjects participated in our experiment, wherein they performed a saccadic eye exercise (SEE) under two conditions of feedback-on (F-on, visualization of eye position) and feedback-off (F-off, non-visualization of eye position). Eye position was continuously monitored in real time on those two conditions, but this information was not provided to the participants. Electroencephalogram recordings were used to estimate neural dynamics and attention during SEE, in which only valid trials (correct responses) were included in electroencephalogram analysis.
Results: SEE accuracy was higher in the F-on than F-off condition (P=0.039). The power spectral density of beta band was higher in the F-on condition on the frontal (P=0.047), central (P=0.042), and occipital areas (P=0.045). Beta-event-related desynchronization was significantly more pronounced in the F-on (-0.19 on frontal and -0.22 on central clusters) than in the F-off condition (0.23 on frontal and 0.05 on central) on preparatory phase (P=0.005 for frontal and P=0.024 for central). In addition, more abundant functional connectivity was revealed under the F-on condition.
Conclusion: Considering substantial gain may come from goal directed attention and activation of brain-network while performing VRT, our preclinical study from SEE suggests that eye tracking algorithms may work efficiently in vestibular rehabilitation using HMD.
Keywords: Electroencephalography; Rehabilitation; Vestibular Diseases; Virtual Reality.
Conflict of interest statement
No potential conflict of interest relevant to this article was reported.
Figures
References
- Cohen HS, Gottshall KR, Graziano M, Malmstrom EM, Sharpe MH. International survey of vestibular rehabilitation therapists by the Barany Society Ad Hoc Committee on Vestibular Rehabilitation Therapy. J Vestib Res. 2009;19(1-2):15–20.
- Hecker HC, Haug CO, Herndon JW. Treatment of the vertiginous patient using Cawthorne’s vestibular exercises. Laryngoscope. 1974 Nov;84(11):2065–72.
- Hillier SL, McDonnell M. Vestibular rehabilitation for unilateral peripheral vestibular dysfunction. Clin Otolaryngol. 2011 Jun;36(3):248–9.
- Bamiou DE, Luxon LM. Vertigo: clinical management and rehabilitation. In: Gleeson M, Luxon L, editors. Scott-Brown’s otorhinolaryngology, head and neck surgery. Bora Raton (FL): CRC Press; 2008. pp. 3791–817.
- Meldrum D, Herdman S, Vance R, Murray D, Malone K, Duffy D, et al. Effectiveness of conventional versus virtual reality-based balance exercises in vestibular rehabilitation for unilateral peripheral vestibular loss: results of a randomized controlled trial. Arch Phys Med Rehabil. 2015 Jul;96(7):1319–28.
- Pavlou M, Kanegaonkar RG, Swapp D, Bamiou DE, Slater M, Luxon LM. The effect of virtual reality on visual vertigo symptoms in patients with peripheral vestibular dysfunction: a pilot study. J Vestib Res. 2012;22(5-6):273–81.
- Alahmari KA, Sparto PJ, Marchetti GF, Redfern MS, Furman JM, Whitney SL. Comparison of virtual reality based therapy with customized vestibular physical therapy for the treatment of vestibular disorders. IEEE Trans Neural Syst Rehabil Eng. 2014 Mar;22(2):389–99.
- Yeh SC, Chen S, Wang PC, Su MC, Chang CH, Tsai PY. Interactive 3-dimensional virtual reality rehabilitation for patients with chronic imbalance and vestibular dysfunction. Technol Health Care. 2014;22(6):915–21.
- Black FO, Pesznecker SC. Vestibular adaptation and rehabilitation. Curr Opin Otolaryngol Head Neck Surg. 2003 Oct;11(5):355–60.
- Cohen HS. Disability and rehabilitation in the dizzy patient. Curr Opin Neurol. 2006 Feb;19(1):49–54.
- Bergeron M, Lortie CL, Guitton MJ. Use of virtual reality tools for vestibular disorders rehabilitation: a comprehensive analysis. Adv Med. 2015;2015:916735.
- Cooksey FS. Rehabilitation in vestibular injuries. Proc R Soc Lond B Biol Sci. 1946 Mar;39:273–8.
- Cawthorne T. The physiological basis for head exercises. J Char Soc Physiother. 1944;3:106–7.
- Badarny S, Aharon-Peretz J, Susel Z, Habib G, Baram Y. Virtual reality feedback cues for improvement of gait in patients with Parkinson’s disease. Tremor Other Hyperkinet Mov (N Y) 2014 Apr;4:225.
- Hong SK, Park S, Ahn MH, Min BK. Top-down and bottom-up neurodynamic evidence in patients with tinnitus. Hear Res. 2016 Dec;342:86–100.
- Makeig S, Jung TP, Bell AJ, Ghahremani D, Sejnowski TJ. Blind separation of auditory event-related brain responses into independent components. Proc Natl Acad Sci U S A. 1997 Sep;94(20):10979–84.
- Bayliss JD, Ballard DH. Rochester (NY): The University of Rochester, Computer Science Department; The effects of eye tracking in a VR helmet on EEG recordings. 1998.
- Pelz JB, Hayhoe MM, Ballard DH, Shrivastava A, Bayliss JD, von der Heyde M. Development of a virtual laboratory for the study of complex human behavior. In: Merritt JO, Bolas MT, Fisher SS, editors. Stereoscopic displays and virtual reality systems VI. Bellingham: SPIE; 1999.
- Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004 Mar;134(1):9–21.
- Makeig S. Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalogr Clin Neurophysiol. 1993 Apr;86(4):283–93.
- Yuval-Greenberg S, Tomer O, Keren AS, Nelken I, Deouell LY. Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron. 2008 May;58(3):429–41.
- He B, Dai Y, Astolfi L, Babiloni F, Yuan H, Yang L. eConnectome: a MATLAB toolbox for mapping and imaging of brain functional connectivity. J Neurosci Methods. 2011 Feb;195(2):261–9.
- Sohrabpour A, Ye S, Worrell GA, Zhang W, He B. Noninvasive electromagnetic source imaging and granger causality analysis: an electrophysiological connectome (eConnectome) approach. IEEE Trans Biomed Eng. 2016 Dec;63(12):2474–87.
- Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr. 1994 Mar-Apr;18(2):192–205.
- Whitney SL, Sparto PJ, Brown KE, Furman JM, Jacobson JL, Redfern MS. The potential use of virtual reality in vestibular rehabilitation: preliminary findings with the BNAVE. J Neurol Phys Ther. 2002;26(2):72–8.
- Gola M, Magnuski M, Szumska I, Wrobel A. EEG beta band activity is related to attention and attentional deficits in the visual performance of elderly subjects. Int J Psychophysiol. 2013 Sep;89(3):334–41.
- Kilavik BE, Zaepffel M, Brovelli A, MacKay WA, Riehle A. The ups and downs of β oscillations in sensorimotor cortex. Exp Neurol. 2013 Jul;245:15–26.
- Kopell N, Ermentrout GB, Whittington MA, Traub RD. Gamma rhythms and beta rhythms have different synchronization properties. Proc Natl Acad Sci U S A. 2000 Feb;97(4):1867–72.
- Brinkman L, Stolk A, Dijkerman HC, de Lange FP, Toni I. Distinct roles for alpha- and beta-band oscillations during mental simulation of goal-directed actions. J Neurosci. 2014 Oct;34(44):14783–92.
- de Lange FP, Jensen O, Bauer M, Toni I. Interactions between posterior gamma and frontal alpha/beta oscillations during imagined actions. Front Hum Neurosci. 2008 Aug;2:7.
- McFarland DJ, Miner LA, Vaughan TM, Wolpaw JR. Mu and beta rhythm topographies during motor imagery and actual movements. Brain Topogr. 2000;12(3):177–86.
- Ng TH, Sowman PF, Brock J, Johnson BW. Premovement brain activity in a bimanual load-lifting task. Exp Brain Res. 2011 Jan;208(2):189–201.
- Tzagarakis C, Ince NF, Leuthold AC, Pellizzer G. Beta-band activity during motor planning reflects response uncertainty. J Neurosci. 2010 Aug;30(34):11270–7.
- Helmchen C, Ye Z, Sprenger A, Munte TF. Changes in resting-state fMRI in vestibular neuritis. Brain Struct Funct. 2014 Nov;219(6):1889–900.
- Hong SK, Kim JH, Kim HJ, Lee HJ. Changes in the gray matter volume during compensation after vestibular neuritis: a longitudinal VBM study. Restor Neurol Neurosci. 2014;32(5):663–73.
- Dieterich M, Bauermann T, Best C, Stoeter P, Schlindwein P. Evidence for cortical visual substitution of chronic bilateral vestibular failure (an fMRI study) Brain. 2007 Aug;130(Pt 8):2108–16.
- Brandt T, Strupp M, Dieterich M. Five keys for diagnosing most vertigo, dizziness, and imbalance syndromes: an expert opinion. J Neurol. 2014 Jan;261(1):229–31.
- Schubert MC, Zee DS. Saccade and vestibular ocular motor adaptation. Restor Neurol Neurosci. 2010;28(1):9–18.
Source: PubMed