Functional near-infrared spectroscopy during optic flow with and without fixation

Carrie W Hoppes, Patrick J Sparto, Susan L Whitney, Joseph M Furman, Theodore J Huppert, Carrie W Hoppes, Patrick J Sparto, Susan L Whitney, Joseph M Furman, Theodore J Huppert

Abstract

Background and purpose: Individuals with visual vertigo describe symptoms of dizziness, disorientation, and/or impaired balance in environments with conflicting visual and vestibular information or complex visual stimuli. Physical therapists often prescribe habituation exercises using optic flow to treat these symptoms, but there are no evidence-based guidelines for delivering optic flow and it is unclear how the brain processes such stimuli. The purposes of this study were to use functional near-infrared spectroscopy (fNIRS) to explore cerebral activation during optic flow, and determine if visual fixation had a modulating effect on brain activity.

Methods: Fifteen healthy participants (7 males and 8 females; mean age 41 years old) stood in a virtual reality environment and viewed optic flow moving unidirectionally in the yaw plane with and without fixation. Changes in cerebral activation were recorded from the bilateral fronto-temporo-parietal and occipital lobes using fNIRS.

Results: Cerebral activation was greater with visual motion than while viewing a stationary scene. Greater cerebral activation in the bilateral fronto-temporo-parietal lobes was observed when optic flow was viewed with fixation.

Discussion and conclusions: Optic flow activates the bilateral fronto-temporo-parietal regions of the cerebral cortex. This activation is greater while viewing optic flow and a fixation target, providing preliminary evidence supporting the use of a fixation target during habituation exercises.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Virtual reality environment.
Fig 1. Virtual reality environment.
The participant was exposed to optic flow in a three-screen wide field-of-view virtual reality environment. Participants faced the front screen that was 1.5 meters away, and were tethered to the ceiling to prevent falls.
Fig 2. fNIRS head cap.
Fig 2. fNIRS head cap.
The participant wore a fNIRS head cap that consisted of 11 sources (capital letters A-K) and 20 detectors (numbers 1–20) on the scalp, distributed between the left fronto-temporo-parietal (left), occipital (center), and right fronto-temporo-parietal (right) regions.
Fig 3. Estimated spatial maps.
Fig 3. Estimated spatial maps.
Estimated spatial maps (T-test) of the oxyhemoglobin data collected using fNIRS for the change in cerebral activation between fixation and no fixation conditions using all source-detector combinations. The color bar represents the results of the T-statistic (T-score). Areas in red indicate greater cerebral activation (increased oxyhemoglobin) and areas in blue indicate lesser cerebral activation (decreased oxyhemoglobin) during the comparison. Thick lines indicate areas with significant activation (p < 0.05).

References

    1. Bronstein A. Visual vertigo syndrome: clinical and posturography findings. Journal of Neurology, Neurosurgery & Psychiatry. 1995;59:472–6.
    1. Staab JP. Chronic Subjective Dizziness. CONTINUUM: Lifelong Learning in Neurology. 2012;18:1118–41. doi:
    1. Rábago CA, Wilken JM. Application of a mild traumatic brain injury rehabilitation program in a virtual realty environment: a case study. Journal of Neurologic Physical Therapy. 2011;35:185–93. doi:
    1. Hall C, Herdman S, Whitney S, Cass S, Clendaniel R, Fife T, et al. Vestibular rehabilitation for peripheral vestibular hypofunction: An evidence-based clinical practice guideline: From the AMerican Physical Therapy Association Neurology Section. Journal of Neurologic Physical Therapy. 2016;40:124–55. doi:
    1. Szturm T, Ireland D, Lessing-Turner M. Comparison of different exercise programs in the rehabilitation of patients with chronic peripheral vestibular dysfunction. Journal of Vestibular Research. 1994;4:461–79.
    1. Vitte E, Sémont A, Berthoz A. Repeated optokinetic stimulation in conditions of active standing facilitates recovery from vestibular deficits. Experimental Brain Research. 1994;102:141–8.
    1. Pavlou M. The Use of Optokinetic Stimulation in Vestibular Rehabilitation. Journal of Neurologic Physical Therapy. 2010;34:105–10. doi:
    1. Pavlou M, Bronstein A, Davies R. Randomized Trial of Supervised Versus Unsupervised Optokinetic Exercise in Persons With Peripheral Vestibular Disorders. Neurorehabilitation and Neural Repair. 2013;27:208–18. doi:
    1. Pavlou M, Lingeswaran A, Davies RA, Gresty MA, Bronstein AM. Simulator based rehabilitation in refractory dizziness. Journal of Neurology. 2004;251:983–95. doi:
    1. Brandt T, Bartenstein P, Janek A, Dieterich M. Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. Brain. 1998;121:1749–58.
    1. Kleinschmidt A, Thilo KV, Büchel C, Gresty MA, Bronstein AM, Frackowiak RSJ. Neural correlates of visual-motion perception as object- or self-motion. NeuroImage. 2002;16:873–82.
    1. Palmisano S, Allison RS, Schira MM, Barry RJ. Future challenges for vection research: definitions, functional significance, measures, and neural bases. Frontiers in Psychology. 2015;6.
    1. Tarita-Nistor L, González EG, Spigelman AJ, Steinbach MJ. Linear vection as a function of stimulus eccentricity, visual angle, and fixation. Journal of vestibular research: equilibrium & orientation. 2006;16:265.
    1. Stern RM, Hu S, Anderson RB, Leibowitz HW, Koch KL. The effects of fixation and restricted visual field on vection-induced motion sickness. Aviation, Space, and Environmental Medicine. 1990;61:712–5.
    1. Dieterich M, Bucher SF, Seelos KC, Brandt T. Horizontal or vertical optokinetic stimulation activates visual motion-sensitive, ocular motor and vestibular cortex areas with right hemispheric dominance. An fMRI study. Brain. 1998;121:1479–95.
    1. Fasold O, von Brevern M, Kuhberg M, Ploner CJ, Villringer A, Lempert T, et al. Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. NeuroImage. 2002;17:1384–93.
    1. Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M. Multisensory Cortical Signal Increases and Decreases During Vestibular Galvanic Stimulation (fMRI). Journal of Neurophysiology. 2001;85:886–99. doi:
    1. Lopez C, Blanke O. The thalamocortical vestibular system in animals and humans. Brain Research Reviews. 2011;67:119–46. doi:
    1. Indovina I, Riccelli R, Chiarella G, Petrolo C, Augimeri A, Giofrè L, et al. Role of the insula and vestibular system in patients with chronic subjective dizziness: An fMRI study using sound-evoked vestibular stimulation. Frontiers in Behavioral Neuroscience. 2015;9:1–12. doi:
    1. Van Ombergen A, Heine L, Jillings S, Roberts RE, Jeurissen B, Van Rompaey V, et al. Altered functional brain connectivity in patients with visually induced dizziness. NeuroImage: Clinical. 2017;14:538–45.
    1. Dieterich M, Bense S, Stephan T, Yousry TA, Brandt T. fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation. Experimental Brain Research. 2003;148:117–27. doi:
    1. Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, et al. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. NeuroImage. 2005;26:721–32. doi:
    1. Della-Justina HM, Gamba HR, Lukasova K, Nucci-da-Silva MP, Winkler AM, Amaro E. Interaction of brain areas of visual and vestibular simultaneous activity with fMRI. Experimental Brain Research. 2015;233:237–52. doi:
    1. Deutschländer A, Bense S, Stephan T, Schwaiger M, Brandt T, Dieterich M. Sensory system interactions during simultaneous vestibular and visual stimulation in PET. Human Brain Mapping. 2002;16:92–103.
    1. Deutschländer A, Bense S, Stephan T, Schwaiger M, Dieterich M, Brandt T. Rollvection versus linearvection: Comparison of brain activations in PET. Human Brain Mapping. 2004;21:143–53. doi:
    1. Becker-Bense S, Buchholz H-G, zu Eulenburg P, Best C, Bartenstein P, Schreckenberger M, et al. Ventral and dorsal streams processing visual motion perception (FDG-PET study). BMC Neuroscience. 2012;13:81–. doi:
    1. Smith AT, Wall MB, Williams AL, Singh KD. Sensitivity to optic flow in human cortical areas MT and MST. The European Journal of Neuroscience. 2006;23:561–9. doi:
    1. Deutschländer A, Hüfner K, Kalla R, Stephan T, Dera T, Glasauer S, et al. Unilateral vestibular failure suppresses cortical visual motion processing. Brain. 2008;131:1025–34. doi:
    1. Uesaki M, Ashida H. Optic-flow selective cortical sensory regions associated with self-reported states of vection. Frontiers in Psychology. 2015;6:1–9. doi:
    1. Karim H, Schmidt B, Dart D, Beluk N, Huppert T. Functional near-infrared spectroscopy (fNIRS) of brain function during active balancing using a video game system. Gait & Posture. 2012;35:367–72.
    1. Herold F, Orlowski K, Börmel S, Müller NG. Cortical activation during balancing on a balance board. Human Movement Science. 2017;51:51–8. doi:
    1. Mihara M, Miyai I, Hatakenaka M, Kubota K, Sakoda S. Role of the prefrontal cortex in human balance control. NeuroImage. 2008;43:329–36. doi:
    1. Miyai I, Tanabe HC, Sase I, Eda H, Oda I, Konishi I, et al. Cortical Mapping of Gait in Humans: A Near-Infrared Spectroscopic Topography Study. NeuroImage. 2001;14:1186–92. doi:
    1. Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, et al. Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. NeuroImage. 2004;23:1020–6. doi:
    1. Wijeakumar S, Shahani U, Simpson WA, McCulloch DL. Haemodynamic responses to radial motion in the visual cortex. Journal of Near Infrared Spectroscopy. 2013;21:231–6.
    1. Gianaros PJ, Muth ER, Mordkoff JT, Levine ME, Stern RM. A questionnaire for the assessment of the multiple dimensions of motion sickness. Aviation, Space, and Environmental Medicine. 2001;72:115
    1. Boas DA, Dale AM. Simulation study of magnetic resonance imaging–guided cortically constrained diffuse optical tomography of human brain function. Applied Optics. 2005;44:1957–68.
    1. Huppert T, Franceschini M, Boas D. Noninvasive Imaging of Cerebral Activation with Diffuse Optical Tomography In: Frostig RD, editor. In Vivo Optical Imaging of Brain Function. 2 ed. Boca Raton, FL: CRC Press; 2009. p. 393–433.
    1. Cope M, Delpy D, Reynolds E, Wray S, Wyatt J, Van der Zee P. Methods of quantitating cerebral near infrared spectroscopy data Oxygen Transport to Tissue X: Springer; 1988. p. 183–9.
    1. Strangman G, Franceschini MA, Boas DA. Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters. Neuroimage. 2003;18:865–79.
    1. Barker JW, Aarabi A, Huppert TJ. Autoregressive model based algorithm for correcting motion and serially correlated errors in fNIRS. Biomedical optics express. 2013;4:1366–79. doi:
    1. Huppert T. Commentary on the statistical properties of noise and its implication on general linear models in functional near-infrared spectroscopy. Neurophotonics. 2016;3.
    1. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological). 1995:289–300.
    1. Boff KR, Kaufman L, Thomas JP. Handbook of perception and human performance New York, N.Y: Wiley; 1986.
    1. Fushiki H, Takata S, Watanabe Y. Influence of fixation on circular vection. Journal of vestibular research: equilibrium & orientation. 2000;10:151.
    1. Seno T, Ito H, Sunaga S. Attentional load inhibits vection. Attention, Perception, & Psychophysics. 2011;73:1467–76.

Source: PubMed

3
Suscribir