Experimental Brain Research

, Volume 233, Issue 8, pp 2421–2431 | Cite as

Inter-hemispheric desynchronization of the human MT+ during visually induced motion sickness

  • Jungo Miyazaki
  • Hiroki Yamamoto
  • Yoshikatsu Ichimura
  • Hiroyuki Yamashiro
  • Tomokazu Murase
  • Tetsuya Yamamoto
  • Masahiro Umeda
  • Toshihiro Higuchi
Research Article


Visually induced motion sickness (VIMS) is triggered in susceptible individuals by stationary viewing of moving visual scenes. VIMS is often preceded by an illusion of self-motion (vection) and/or by inappropriate optokinetic nystagmus (OKN) responses associated with increased activity in the human motion-sensitive middle temporal area (MT+). Neuroimaging studies have reported predominant right hemispheric activation in MT+ during both vection and OKN, suggesting that VIMS may result from desynchronization of activity between left and right MT+ cortices. However, this possibility has not been directly tested. To this end, we presented VIMS-free and VIMS-inducing movies in that order while measuring the temporal correlations between corresponding left and right visual cortices (including MT+) using functional magnetic resonance imaging. The inter-hemispheric correlation was reduced significantly during the viewing of the VIMS-inducing movie compared to the control VIMS-free movie in the MT+ of subjects reporting VIMS, but not in insusceptible subjects. In contrast, there were no significant inter-hemispheric differences within VIMS-free or VIMS-inducing movie exposure for visual area V1, V2, V3, V3A or V7. Our findings provide the first evidence for an association between asynchronous bilateral MT+ activation and VIMS. Desynchronization of left and right MT+ regions may reflect hemispheric asymmetry in the activities of functional networks involved in eye movement control, vection perception and/or postural control.


Human visual cortex Optokinetic nystagmus (OKN) Vection Functional magnetic resonance imaging (fMRI) Visual motion 



We thank Yoshimichi Ejima and Shigeko Takahashi for their helpful comments. We also thank anonymous reviewers for their constructive comments and suggestions. This study was supported by a Grant-in-Aid for Scientific Research on Innovative Areas “Shitsukan” (23135517, 25135720) from the Ministry of Education, Culture, Sports, Science and Technology of Japan and Grants-in-Aid for Scientific Research (22530793) from the Japan Society for the Promotion of Science (JSPS) to H. Yamamoto.

Supplementary material

Supplementary material 1 (MOV 7773 kb)

Supplementary material 2 (MOV 7906 kb)

221_2015_4312_MOESM3_ESM.pdf (6.4 mb)
Supplementary material 3 (PDF 6514 kb)
221_2015_4312_MOESM4_ESM.pdf (1.2 mb)
Supplementary material 4 (PDF 1231 kb)
221_2015_4312_MOESM5_ESM.pdf (106 kb)
Supplementary material 5 (PDF 106 kb)


  1. Bates D, Maechler M, Bolker BM, Walker S (2014) lme4: Linear mixed-effects models using eigen and S4. Submitted to J Stat Softw. arxiv:1406.5823
  2. Bos JE, Bles W (1998) Modelling motion sickness and subjective vertical mismatch detailed for vertical motions. Brain Res Bull 47(5):537–542PubMedCrossRefGoogle Scholar
  3. Brandt T, Bartenstein P, Janek A, Dieterich M (1998) Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. Brain 121(Pt 9):1749–1758PubMedCrossRefGoogle Scholar
  4. Bullmore E, Long C, Suckling J, Fadili J, Calvert G, Zelaya F, Brammer M (2001) Colored noise and computational inference in neurophysiological (fMRI) time series analysis: resampling methods in time and wavelet domains. Hum Brain Mapp 12(2):61–78PubMedCrossRefGoogle Scholar
  5. Cheung BSK, Howard IP, Money KE (1991) Visually-induced sickness in normal and bilateral labyrinthine-defective subjects. Aviat Space Environ Med 62:527–531PubMedGoogle Scholar
  6. Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162–173PubMedCrossRefGoogle Scholar
  7. De Rosario-Martinez H (2013) phia: Post-hoc interaction analysis. R package version 0.1-3Google Scholar
  8. De Yoe EA, Carman GJ, Bandettini P, Glickman S, Wieser J, Cox R, Miller D, Neitz J (1996) Mapping striate and extrastriate visual areas in human cerebral cortex. Proc Nat Acad Sci (USA) 93:2382–2386CrossRefGoogle Scholar
  9. Dieterich M, Bucher SF, Seelos KC, Brandt T (1998) Horizontal or vertical optokinetic stimulation activates visual motion-sensitive, ocular motor and vestibular cortex areas with right hemispheric dominance. An fMRI study. Brain 121(8):1479–1495PubMedCrossRefGoogle Scholar
  10. Dieterich M, Bense S, Stephan T, Yousry TA, Brandt T (2003) fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation. Exp Brain Res 148(1):117–127PubMedCrossRefGoogle Scholar
  11. Ebenholtz S (1992) Motion sickness and oculomotor systems in virtual environments. Presence Teleoper Virtual Environ 1(3):302–305Google Scholar
  12. Ebenholtz SM, Cohen MM, Linder BJ (1994) The possible role of nystagmus in motion sickness: a hypothesis. Aviat Space Environ Med 65(11):1032–1035PubMedGoogle Scholar
  13. Ellis SR (1991) Nature and origins of virtual environments: a bibliographical essay. Comput Syst Eng 2(4):321–347CrossRefGoogle Scholar
  14. Engel SA, Rumelhart DE, Wandell BA, Lee AT, Glover GH, Chichilnisky EJ, Shadlen MN (1994) fMRI of human visual cortex. Nature 369:525PubMedCrossRefGoogle Scholar
  15. Flanagan MB, May JG, Dobie TG (2004) The role of vection, eye movements and postural instability in the etiology of motion sickness. J Vestib Res 14(4):335–346PubMedGoogle Scholar
  16. Golding JF (2006) Motion sickness susceptibility. Auton Neurosci 129(1):67–76PubMedCrossRefGoogle Scholar
  17. Griffin MJ (1990) Handbook of human vibration. Academic Press, LondonGoogle Scholar
  18. Hasson U, Avidan G, Gelbard H (2009) Shared and idiosyncratic cortical activation patterns in autism revealed under continuous real-life viewing conditions. Autism Res 2:220–231PubMedCentralPubMedCrossRefGoogle Scholar
  19. Hettinger LJ, Berbaum KS, Kennedy RS, Dunlap WP, Nolan MD (1990) Vection and simulator sickness. Mil Psychol 2(3):171–181PubMedCrossRefGoogle Scholar
  20. Huk AC, Dougherty RF, Heeger DJ (2002) Retinotopy and functional subdivision of human areas MT and MST. J Neurosci 22(16):7195–7205PubMedGoogle Scholar
  21. Kennedy RS, Graybiel A, McDonough RC, Beekwith FD (1968) Symptomatology under storm conditions in the North Atlantic in control subjects and in persons with bilateral labyrinthine defects. Acta-Oto-Laryngol 66:533–540CrossRefGoogle Scholar
  22. Kennedy RS, Fowlkes J, Lilienthal M (1993a) Postural and performance changes following exposures to flight simulators. Aviat Space Environ Med 64(10):912–920PubMedGoogle Scholar
  23. Kennedy RS, Lane NE, Berbaum KS, Lilienthal MG (1993b) Simulator sickness questionnaire: an enhanced method for quantifying simulator sickness. Int J Aviat Psychol 3(3):203–220CrossRefGoogle Scholar
  24. Kennedy RS, Drexler J, Kennedy RC (2010) Research in visually induced motion sickness. Appl Ergon 41(4):494–503PubMedCrossRefGoogle Scholar
  25. Kleinschmidt A, Thilo KV, Büchel C, Gresty MA, Bronstein AM, Frackowiak RS (2002) Neural correlates of visual-motion perception as object-or self-motion. Neuroimage 16:873–882PubMedCrossRefGoogle Scholar
  26. Konen CS, Kleiser R, Seitz RJ, Bremmer F (2005) An fMRI study of optokinetic nystagmus and smooth-pursuit eye movements in humans. Exp Brain Res 165(2):203–216PubMedCrossRefGoogle Scholar
  27. Kovacs G, Raabe M, Greenlee MW (2008) Neural correlates of visually induced self-motion illusion in depth. Cereb Cortex 18(8):1779–1787PubMedCrossRefGoogle Scholar
  28. Napadow V, Li A, Loggia ML, Kim J, Schalock PC, Lerner E, Tran TN, Ring J, Rosen BR, Kaptchuk TJ, Pfab F (2012) The brain circuitry underlying the temporal evolution of nausea in humans. Cereb Cortex 23(4):806–813PubMedCentralPubMedCrossRefGoogle Scholar
  29. Napadow V, Sheehan J, Kim J, Dassatti A, Thurler AH, Surjanhata B, Vangel M, Makris N, Schaechter JD, Kuo B (2013) Brain white matter microstructure is associated with susceptibility to motion-induced nausea. Neurogastroenterol Motil 25(5):448-e303Google Scholar
  30. Nir Y, Mukamel R, Dinstein I, Privman E, Harel M, Fisch L, Malach R (2008) Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11(9):1100–1108PubMedCentralPubMedCrossRefGoogle Scholar
  31. Oman CM (1990) Motion sickness: a synthesis and evaluation of the sensory conflict theory. Can J Physiol Pharmacol 68(2):294–303PubMedCrossRefGoogle Scholar
  32. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; R Foundation for Statistical Computing. ISBN 3–900051–07–0.
  33. Reason JT (1978) Motion sickness adaptation: a neural mismatch model. J R Soc Med 71(11):819–829PubMedCentralPubMedGoogle Scholar
  34. Reason JT, Brand JJ (1975) Motion sickness. Academic Press, LondonGoogle Scholar
  35. Riccio GE, Stoffregen TA (1991) An ecological theory of motion sickness and postural instability. Ecol Psychol 3:195–240CrossRefGoogle Scholar
  36. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889–893PubMedCrossRefGoogle Scholar
  37. Shupak A, Gordon CR (2006) Motion sickness: advances in pathogenesis, prediction, prevention, and treatment. Aviat Space Environ Med 77(12):1213–1223PubMedGoogle Scholar
  38. Smith AT, Wall MB, Thilo KV (2012) Vestibular inputs to human motion-sensitive visual cortex. Cereb Cortex 22(5):1068–1077PubMedCrossRefGoogle Scholar
  39. Sterzer P, Kleinschmidt A (2010) Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct Funct 214(5–6):611–622PubMedCrossRefGoogle Scholar
  40. Wall MB, Smith AT (2008) The representation of egomotion in the human brain. Curr Biol 18:191–194PubMedCrossRefGoogle Scholar
  41. Yamamoto H, Ban H, Fukunaga M, Umeda M, Tanaka C, Ejima Y (2008) Large- and small-scale functional organization of visual field representation in the human visual cortex. In: Portocello TA, Velloti RB (eds) Visual cortex: new research. Nova Science Publisher, New York, pp 195–226Google Scholar
  42. Yamamoto T, Yamamoto H, Mano H, Umeda M, Tanaka C, Kawano K (2009) A new fMRI method for subdividing the human middle temporal complex into retinotopic areas. Neurosci Res 65:S173CrossRefGoogle Scholar
  43. Yamamoto H, Fukunaga M, Takahashi S, Mano H, Tanaka C, Umeda M, Ejima Y (2012) Inconsistency and uncertainty of the human visual area loci following surface-based registration: probability and entropy maps. Hum Brain Mapp 33:121–129PubMedCrossRefGoogle Scholar
  44. Zar JH (2009) Biostatistical Analysis, 5th edn. Pearson Education International, LondonGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jungo Miyazaki
    • 1
  • Hiroki Yamamoto
    • 2
  • Yoshikatsu Ichimura
    • 1
  • Hiroyuki Yamashiro
    • 3
  • Tomokazu Murase
    • 4
  • Tetsuya Yamamoto
    • 5
  • Masahiro Umeda
    • 4
  • Toshihiro Higuchi
    • 6
  1. 1.Corporate R&DCanon Inc.TokyoJapan
  2. 2.Graduate School of Human and Environmental StudiesKyoto UniversityKyotoJapan
  3. 3.Department of Medical EngineeringAino UniversityOsakaJapan
  4. 4.Department of Medical InformaticsMeiji University of Integrative MedicineKyotoJapan
  5. 5.Graduate School of EngineeringKyoto UniversityKyotoJapan
  6. 6.Department of NeurosurgeryMeiji University of Integrative MedicineKyotoJapan

Personalised recommendations