Behavior Research Methods

, Volume 51, Issue 1, pp 96–107 | Cite as

A virtual reality approach identifies flexible inhibition of motion aftereffects induced by head rotation

  • Jianying Bai
  • Min BaoEmail author
  • Tao Zhang
  • Yi Jiang


As we move in space, our retinae receive motion signals from two causes: those resulting from motion in the world and those resulting from self-motion. Mounting evidence has shown that vestibular self-motion signals interact with visual motion processing profoundly. However, most contemporary methods arguably lack portability and generality and are incapable of providing measurements during locomotion. Here we developed a virtual reality approach, combining a three-space sensor with a head-mounted display, to quantitatively manipulate the causality between retinal motion and head rotations in the yaw plane. Using this system, we explored how self-motion affected visual motion perception, particularly the motion aftereffect (MAE). Subjects watched gratings presented on a head-mounted display. The gratings drifted at the same velocity as head rotations, with the drifting direction being identical, opposite, or perpendicular to the direction of head rotations. We found that MAE lasted a significantly shorter time when subjects’ heads rotated than when their heads were kept still. This effect was present regardless of the drifting direction of the gratings, and was also observed during passive head rotations. These findings suggest that the adaptation to retinal motion is suppressed by head rotations. Because the suppression was also found during passive head movements, it should result from visual–vestibular interaction rather than from efference copy signals. Such visual–vestibular interaction is more flexible than has previously been thought, since the suppression could be observed even when the retinal motion direction was perpendicular to head rotations. Our work suggests that a virtual reality approach can be applied to various studies of multisensory integration and interaction.


Head movement Adaptation Motion aftereffect Multisensory Virtual reality 


  1. Billington, J., & Smith, A. T. (2015). Neural mechanisms for discounting head-roll-induced retinal motion. Journal of Neuroscience, 35, 4851–4856. CrossRefGoogle Scholar
  2. Blake, R., Tadin, D., Sobel, K. V., Raissian, T. A., & Chong, S. C. (2006). Strength of early visual adaptation depends on visual awareness. Proceedings of the National Academy of Sciences, 103, 4783–4788. CrossRefGoogle Scholar
  3. Brainard, D. H. (1997). The Psychophysics Toolbox. Spatial Vision, 10, 433–436. CrossRefGoogle Scholar
  4. Bridgeman, B. (2007). Efference copy and its limitations. Computers in Biology and Medicine, 37, 924–929. CrossRefGoogle Scholar
  5. Brooks, J. X., Carriot, J., & Cullen, K. E. (2015). Learning to expect the unexpected: Rapid updating in primate cerebellum during voluntary self-motion. Nature Neuroscience, 18, 1310–1317. CrossRefGoogle Scholar
  6. Chan, Y. S., Kasper, J., & Wilson, V. J. (1987). Dynamics and directional sensitivity of neck muscle spindle responses to head rotation. Journal of Neurophysiology, 57, 1716–1729. CrossRefGoogle Scholar
  7. Cuturi, L. F., & MacNeilage, P. R. (2014). Optic flow induces nonvisual self-motion aftereffects. Current Biology, 24, 2817–2821. CrossRefGoogle Scholar
  8. DeAngelis, G. C., & Angelaki, D. E. (2012). Visual–vestibular integration for self-motion perception. In M. M. Murray & M. T. Wallace (Eds.), The neural bases of multisensory processes (pp. 629–650). Boca Raton: CRC Press.Google Scholar
  9. Dong, X., Engel, S. A., & Bao, M. (2014). The time course of contrast adaptation measured with a new method: Detection of ramped contrast. Perception, 43, 427–437. CrossRefGoogle Scholar
  10. Dong, X., Gao, Y., Lv, L., & Bao, M. (2016). Habituation of visual adaptation. Scientific Reports, 6, 19152. CrossRefGoogle Scholar
  11. Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119, 593–609. CrossRefGoogle Scholar
  12. Garzorz, I. T., & MacNeilage, P. R. (2017). Visual–vestibular conflict detection depends on fixation. Current Biology, 27, 2856–2861 e2854. Google Scholar
  13. Greenlee, M. W., Frank, S. M., Kaliuzhna, M., Blanke, O., Bremmer, F., Churan, J., … Smith, A. T. (2016). Multisensory integration in self motion perception. Multisensory Research, 29, 525–556. CrossRefGoogle Scholar
  14. Greenlee, M. W., Georgeson, M. A., Magnussen, S., & Harris, J. P. (1991). The time course of adaptation to spatial contrast. Vision Research, 31, 223–236. CrossRefGoogle Scholar
  15. Gu, Y., Angelaki, D. E., & Deangelis, G. C. (2008). Neural correlates of multisensory cue integration in macaque MSTd. Nature Neuroscience, 11, 1201–1210. CrossRefGoogle Scholar
  16. Gu, Y., Watkins, P. V., Angelaki, D. E., & DeAngelis, G. C. (2006). Visual and nonvisual contributions to three-dimensional heading selectivity in the medial superior temporal area. Journal of Neuroscience, 26, 73–85. CrossRefGoogle Scholar
  17. Haarmeier, T., Thier, P., Repnow, M., & Petersen, D. (1997). False perception of motion in a patient who cannot compensate for eye movements. Nature, 389, 849–852. CrossRefGoogle Scholar
  18. Haggard, P., Iannetti, G. D., & Longo, M. R. (2013). Spatial sensory organization and body representation in pain perception. Current Biology, 23, R164–R176. CrossRefGoogle Scholar
  19. Harris, L. R., Morgan, M. J., & Still, A. W. (1981). Moving and the motion after-effect. Nature, 293, 139–141.CrossRefGoogle Scholar
  20. Hebb, D. O. (1949). The organization of behavior. New York: Wiley.Google Scholar
  21. Huk, A. C., Ress, D., & Heeger, D. J. (2001). Neuronal basis of the motion aftereffect reconsidered. Neuron, 32, 161–172. CrossRefGoogle Scholar
  22. Jaekl, P. M., Jenkin, M. R., & Harris, L. R. (2005). Perceiving a stable world during active rotational and translational head movements. Experimental Brain Research, 163, 388–399. CrossRefGoogle Scholar
  23. Kaliuzhna, M., Prsa, M., Gale, S., Lee, S. J., & Blanke, O. (2015). Learning to integrate contradictory multisensory self-motion cue pairings. Journal of Vision, 15(1), 10. CrossRefGoogle Scholar
  24. Keck, M. J., Palella, T. D., & Pantle, A. (1976). Motion aftereffect as a function of the contrast of sinusoidal gratings. Vision Research, 16, 187–191.CrossRefGoogle Scholar
  25. Kim, J., Chung, C. Y., Nakamura, S., Palmisano, S., & Khuu, S. K. (2015). The Oculus Rift: A cost-effective tool for studying visual-vestibular interactions in self-motion perception. Frontiers in Psychology, 6, 248. Google Scholar
  26. Konkle, T., Wang, Q., Hayward, V., & Moore, C. I. (2009). Motion aftereffects transfer between touch and vision. Current Biology, 19, 745–750. CrossRefGoogle Scholar
  27. Kovacs, G., Raabe, M., & Greenlee, M. W. (2008). Neural correlates of visually induced self-motion illusion in depth. Cerebral Cortex, 18, 1779–1787. CrossRefGoogle Scholar
  28. Leube, D. T., Knoblich, G., Erb, M., Grodd, W., Bartels, M., & Kircher, T. T. (2003). The neural correlates of perceiving one’s own movements. NeuroImage, 20, 2084–2090. CrossRefGoogle Scholar
  29. Mack, A., Goodwin, J., Thordarsen, H., Benjamin, D., Palumbo, D., & Hill, J. (1987). Motion aftereffects associated with pursuit eye movements. Vision Research, 27, 529–536.CrossRefGoogle Scholar
  30. Matsumiya, K., & Shioiri, S. (2014). Moving one’s own body part induces a motion aftereffect anchored to the body part. Current Biology, 24, 165–169. CrossRefGoogle Scholar
  31. McGovern, D. P., Roach, N. W., & Webb, B. S. (2012). Perceptual learning reconfigures the effects of visual adaptation. Journal of Neuroscience, 32, 13621–13629. CrossRefGoogle Scholar
  32. Mei, G., Dong, X., Dong, B., & Bao, M. (2015). Spontaneous recovery of effects of contrast adaptation without awareness. Frontiers in Psychology, 6, 1464. CrossRefGoogle Scholar
  33. Mesik, J., Bao, M., & Engel, S. A. (2013). Spontaneous recovery of motion and face aftereffects. Vision Research, 89, 72–78. CrossRefGoogle Scholar
  34. Miall, R. C., & Wolpert, D. M. (1996). Forward models for physiological motor control. Neural Networks, 9, 1265–1279. CrossRefGoogle Scholar
  35. Morgan, M. J., Ward, R. M., & Brussell, E. M. (1976). The aftereffect of tracking eye movements. Perception, 5, 309–317. CrossRefGoogle Scholar
  36. Petrov, A. A., & Van Horn, N. M. (2012). Motion aftereffect duration is not changed by perceptual learning: Evidence against the representation modification hypothesis. Vision Research, 61, 4–14.
  37. Pettorossi, V. E., & Schieppati, M. (2014). Neck proprioception shapes body orientation and perception of motion. Frontiers in Human Neuroscience, 8, 895. CrossRefGoogle Scholar
  38. Shirai, N., & Ichihara, S. (2012). Reduction in sensitivity to radial optic-flow congruent with ego-motion. Vision Research, 62, 201–208. CrossRefGoogle Scholar
  39. Sperry, R. W. (1950). Neural basis of the spontaneous optokinetic response produced by visual inversion. Journal of Comparative and Physiological Psychology, 43, 482–489.CrossRefGoogle Scholar
  40. Swanston, M. T., & Wade, N. J. (1992). Motion over the retina and the motion aftereffect. Perception, 21, 569–582. CrossRefGoogle Scholar
  41. Troncoso, X. G., McCamy, M. B., Jazi, A. N., Cui, J., Otero-Millan, J., Macknik, S. L., . . . Martinez-Conde, S. (2015). V1 neurons respond differently to object motion versus motion from eye movements. Nature Communication, 6, 8114. CrossRefGoogle Scholar
  42. Ventre-Dominey, J. (2014). Vestibular function in the temporal and parietal cortex: Distinct velocity and inertial processing pathways. Frontiers in Integrative Neuroscience, 8, 53. CrossRefGoogle Scholar
  43. Verstraten, F. A. J., Fredericksen, R. E., & van de Grind, W. A. (1994). Movement aftereffect of bi-vectorial transparent motion. Vision Research, 34, 349–358.
  44. von Holst, E., & Mittelstaedt, H. (1950). Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften, 37, 464–476.CrossRefGoogle Scholar
  45. Wallach, H. (1987). Perceiving a stable environment when one moves. Annual Review of Psychology, 38, 1–27. CrossRefGoogle Scholar
  46. Wallach, H., & Flaherty, E. W. (1975). Compensation for field expansion caused by moving forward. Perception & Psychophysics, 17, 445–449. CrossRefGoogle Scholar
  47. Wolpert, D. M., Ghahramani, Z., & Jordan, M. I. (1995). An internal model for sensorimotor integration. Science, 269, 1880–1882. CrossRefGoogle Scholar
  48. Wurtz, R. H. (2008). Neuronal mechanisms of visual stability. Vision Research, 48, 2070–2089. CrossRefGoogle Scholar
  49. Yuval-Greenberg, S., & Heeger, D. J. (2013). Continuous flash suppression modulates cortical activity in early visual cortex. Journal of Neuroscience, 33, 9635–9643. CrossRefGoogle Scholar
  50. Zhang, T., Heuer, H. W., & Britten, K. H. (2004). Parietal area VIP neuronal responses to heading stimuli are encoded in head-centered coordinates. Neuron, 42, 993–1001. CrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2018

Authors and Affiliations

  • Jianying Bai
    • 1
    • 2
    • 3
  • Min Bao
    • 1
    • 4
    • 5
    Email author
  • Tao Zhang
    • 4
    • 5
  • Yi Jiang
    • 4
    • 5
    • 6
  1. 1.CAS Key Laboratory of Behavioral Science, Institute of PsychologyChinese Academy of SciencesBeijingChina
  2. 2.Xinjiang Astronomical ObservatoryChinese Academy of SciencesUrumqiChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.State Key Laboratory of Brain and Cognitive ScienceBeijingChina
  5. 5.Department of PsychologyUniversity of Chinese Academy of SciencesBeijingChina
  6. 6.CAS Center for Excellence in Brain Science and Intelligence TechnologyShanghaiChina

Personalised recommendations