Intensified visual clutter induces increased sympathetic signalling, poorer postural control, and faster torsional eye movements during visual rotation


Autoři: Tobias Wibble aff001;  Ulrika Södergård aff001;  Frank Träisk aff001;  Tony Pansell aff001
Působiště autorů: Division of Ophthalmology and Vision, Department of Clinical Neuroscience, Marianne Bernadotte Centre, Karolinska Institutet, Stockholm, Sweden aff001;  St Erik Eye Hospital, Stockholm, Sweden aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227370

Souhrn

Many dizzy patients express a hypersensitivity to visual motion and clutter. This study aims to investigate how exposure to rotating visual clutter affects ocular torsion, vertical skewing, body-sway, the autonomic pupillary response, and the subjective feeling of discomfort to the stimulation. Sixteen healthy subjects were exposed to 20 seconds rotational visual stimulation (72 deg/s; 50 deg visual field). Visual stimuli were comprised of black lines on a white background, presented at low and high intensity levels of visual clutter, holding 19 lines and 38 lines respectively. Ocular torsion and vertical skewing were recorded using the Chronos Eye Tracker, which also measured pupil size as a reflection of the autonomic response. Postural control was evaluated by measuring body-sway area on the Wii Balance Board. Values were compared to data retrieved 20 seconds before and after the optokinetic stimulation, as subjects viewed the stationary visual scene. The high intensity stimulus resulted in significantly higher torsional velocities. Subjects who were exposed to low intensity first exhibited higher velocities for both intensities. Both pupil size and body sway increased for the higher intensity to both the moving and stationary visual scene, and were positively correlated to torsional velocity. In conclusion, exposure to visual clutter was reflected in the eye movement response, changes in postural control, and the autonomic response. This response may hold clinical utility when assessing patients suffering from visual motion hypersensitivity, while also providing some context as to why some healthy people feel discomfort in visually cluttered surroundings.

Klíčová slova:

Balance and falls – Eye movements – Hypersensitivity – Motion – Postural control – Pupil – Vertigo – Vision


Zdroje

1. Saber Tehrani AS, Coughlan D, Hsieh YH, Mantokoudis G, Korley FK, Kerber KA, et al. Rising annual costs of dizziness presentations to U.S. emergency departments. Acad Emerg Med. 2013;20(7):689–96. doi: 10.1111/acem.12168 23859582

2. Tinetti ME, Williams CS, Gill TM. Dizziness among older adults: a possible geriatric syndrome. Annals of internal medicine. 2000;132(5):337–44. doi: 10.7326/0003-4819-132-5-200003070-00002 10691583

3. Skoien AK, Wilhemsen K, Gjesdal S. Occupational disability caused by dizziness and vertigo: a register-based prospective study. Br J Gen Pract. 2008;58(554):619–23. doi: 10.3399/bjgp08X330744 18801279

4. Bronstein AM, Pavlou M. Balance. Handb Clin Neurol. 2013;110:189–208. doi: 10.1016/B978-0-444-52901-5.00016-2 23312641

5. Reason JT. Motion sickness adaptation: a neural mismatch model. J R Soc Med. 1978;71(11):819–29. 731645

6. Neuhauser HK, Radtke A, von Brevern M, Lezius F, Feldmann M, Lempert T. Burden of dizziness and vertigo in the community. Archives of internal medicine. 2008;168(19):2118–24. doi: 10.1001/archinte.168.19.2118 18955641

7. Bronstein AM. The visual vertigo syndrome. Acta Otolaryngol Suppl. 1995;520 Pt 1:45–8.

8. Bronstein AM. Visual vertigo syndrome: clinical and posturography findings. J Neurol Neurosurg Psychiatry. 1995;59(5):472–6. doi: 10.1136/jnnp.59.5.472 8530928

9. Mueller M, Strobl R, Jahn K, Linkohr B, Peters A, Grill E. Burden of disability attributable to vertigo and dizziness in the aged: results from the KORA-Age study. Eur J Public Health. 2014;24(5):802–7. doi: 10.1093/eurpub/ckt171 24213583

10. Brandt T, Dieterich M. Skew deviation with ocular torsion: a vestibular brainstem sign of topographic diagnostic value. Ann Neurol. 1993;33(5):528–34. doi: 10.1002/ana.410330518 8498829

11. Wibble T, Pansell T. Vestibular Eye Movements Are Heavily Impacted by Visual Motion and Are Sensitive to Changes in Visual Intensities. Investigative Ophthalmology & Visual Science. 2019;60(4):1021–7.

12. Collewijn H, Van der Steen J, Ferman L, Jansen TC. Human ocular counterroll: assessment of static and dynamic properties from electromagnetic scleral coil recordings. Exp Brain Res. 1985;59(1):185–96. doi: 10.1007/bf00237678 4018196

13. Pansell T, Sverkersten U, Ygge J. Visual spatial clues enhance ocular torsion response during visual tilt. Exp Brain Res. 2006;175(3):567–74. doi: 10.1007/s00221-006-0574-8 16791595

14. Lubeck AJ, Bos JE, Stins JF. Interaction between depth order and density affects vection and postural sway. PloS one. 2015;10(12):e0144034. doi: 10.1371/journal.pone.0144034 26630658

15. Van Ombergen A, Lubeck AJ, Van Rompaey V, Maes LK, Stins JF, Van de Heyning PH, et al. The effect of optokinetic stimulation on perceptual and postural symptoms in visual vestibular mismatch patients. PloS one. 2016;11(4):e0154528. doi: 10.1371/journal.pone.0154528 27128970

16. Guerraz M, Yardley L, Bertholon P, Pollak L, Rudge P, Gresty MA, et al. Visual vertigo: symptom assessment, spatial orientation and postural control. Brain. 2001;124(Pt 8):1646–56. doi: 10.1093/brain/124.8.1646 11459755

17. Partala T, Surakka V. Pupil size variation as an indication of affective processing. International journal of human-computer studies. 2003;59(1–2):185–98.

18. Pedrotti M, Mirzaei MA, Tedesco A, Chardonnet J-R, Mérienne F, Benedetto S, et al. Automatic stress classification with pupil diameter analysis. International Journal of Human-Computer Interaction. 2014;30(3):220–36.

19. MacNeilage PR, Turner AH, Angelaki DE. Canal–Otolith Interactions and Detection Thresholds of Linear and Angular Components During Curved-Path Self-Motion. Journal of Neurophysiology. 2010;104(2):765–73. doi: 10.1152/jn.01067.2009 20554843

20. Park DS, Lee G. Validity and reliability of balance assessment software using the Nintendo Wii balance board: usability and validation. J Neuroeng Rehabil. 2014;11:99. doi: 10.1186/1743-0003-11-99 24912769

21. Adlerton AK, Moritz U. Does calf‐muscle fatigue affect standing balance? Scandinavian journal of medicine & science in sports. 1996;6(4):211–5.

22. Wollseifen T. Different methods of calculating body sway area. Pharmaceutical Programming. 2011;4(1–2):91–106.

23. Guerraz M, Bronstein AM. Mechanisms underlying visually induced body sway. Neuroscience letters. 2008;443(1):12–6. doi: 10.1016/j.neulet.2008.07.053 18672020

24. Lee MD, Wagenmakers E-J. Bayesian cognitive modeling: A practical course: Cambridge university press; 2014.

25. Cheung B, Howard I. Optokinetic torsion: dynamics and relation to circularvection. Vision research. 1991;31(7–8):1327–35. doi: 10.1016/0042-6989(91)90054-9 1891821

26. Cheung BS, Howard IP. Optokinetic torsion: dynamics and relation to circularvection. Vision Res. 1991;31(7–8):1327–35. doi: 10.1016/0042-6989(91)90054-9 1891821

27. Dichgans J, Brandt T. Optokinetic motion sickness and pseudo-Coriolis effects induced by moving visual stimuli. Acta oto-laryngologica. 1973;76(1–6):339–48.

28. Kennedy RS, Hettinger LJ, Harm DL, Ordy JM, Dunlap WP. Psychophysical scaling of circular vection (CV) produced by optokinetic (OKN) motion: individual differences and effects of practice. Journal of Vestibular Research. 1996;6(5):331–41. 8887891

29. Brown B. Dynamic visual acuity, eye movements and peripheral acuity for moving targets. Vision research. 1972;12(2):305–21. doi: 10.1016/0042-6989(72)90120-4 5033692

30. Brandt T, Dichgans J, Büchele W. Motion habituation: Inverted self-motion perception and optokinetic after-nystagmus. Experimental Brain Research. 1974;21(4):337–52. doi: 10.1007/bf00237897 4442493

31. Yokota Y, Aoki M, Mizuta K, Ito Y, Isu N. Motion sickness susceptibility associated with visually induced postural instability and cardiac autonomic responses in healthy subjects. Acta oto-laryngologica. 2005;125(3):280–5. doi: 10.1080/00016480510003192 15966698

32. Bradley MM, Miccoli L, Escrig MA, Lang PJ. The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology. 2008;45(4):602–7. doi: 10.1111/j.1469-8986.2008.00654.x 18282202

33. Newton R. Balance and falls among older people. Generations. 2003;27(1):27–31.

34. Baldassi S, Megna N, Burr DC. Visual clutter causes high-magnitude errors. PLoS biology. 2006;4(3):e56. doi: 10.1371/journal.pbio.0040056 16494527

35. Heerwagen JH, Heubach JG, Montgomery J, Weimer WC. Environmental design, work, and well being: managing occupational stress through changes in the workplace environment. Aaohn Journal. 1995;43(9):458–68. 7545995

36. Dannenbaum E, Chilingaryan G, Fung J. Visual vertigo analogue scale: an assessment questionnaire for visual vertigo. Journal of Vestibular Research. 2011;21(3):153–9. doi: 10.3233/VES-2011-0412 21558640

37. Bronstein AM. Vision and vertigo: some visual aspects of vestibular disorders. J Neurol. 2004;251(4):381–7. doi: 10.1007/s00415-004-0410-7 15083281


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2020 Číslo 1