Advertisement

Unidirectional influence of vision on locomotion in multimodal spatial representations acquired from navigation

  • Yu DuEmail author
  • Weimin MouEmail author
  • Lei Zhang
Original Article
  • 36 Downloads

Abstract

Visual and idiothetic information is coupled in forming multimodal spatial representations during navigation (Tcheang et al. in Proc Natl Acad Sci USA 108(3):1152–1157, 2011). We investigated whether idiothetic representations activate visual representations but not vice versa (unidirectional coupling) or whether these two representations activate each other (bidirectional coupling). In a virtual reality environment, participants actively rotated in place to face certain orientations to become adapted to a new vision–locomotion relationship (gain). In particular, the visual turning angle was equal to 0.7 times the physical turning angle. After adaptation, participants walked a path with a turn in darkness (idiothetic input only) or watched a video of the traversed path (visual input only). Then, the participants pointed to the origin of the path. The participants who were presented with only idiothetic input showed that their pointing responses were influenced by the new gain (adaptation effect). By contrast, the participants who were presented with only visual input did not show any adaptation effect. These results suggest that idiothetic input contributed to spatial representations indirectly via the coupling, which resulted in the adaptation effect, whereas vision alone contributed to spatial representations directly, which did not result in the adaptation effect. Hence, the coupling between vision and locomotion is unidirectional.

Notes

Acknowledgements

We thank Benson Ng, Janina Valencia, and Nim Binning for their contribution in data collection.

Funding

This research was funded by the Natural Sciences and Engineering Research Council of Canada to Weimin Mou.

Compliance with ethical standards

Ethical approval

All procedures performed in the reported study involving human participants were in accordance with the ethical standards of the University of Alberta Research Ethics Boards and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

Author Yu Du declares that she has no conflict of interest. Author Weimin Mou declares that he has no conflict of interest. Author Lei Zhang declares that she has no conflict of interest.

References

  1. Arthur, J. C., Philbeck, J. W., & Chichka, D. (2007). Spatial memory enhances the precision of angular self-motion updating. Experimental Brain Research, 183, 557–568.  https://doi.org/10.1007/s00221-007-1075-0.CrossRefPubMedGoogle Scholar
  2. Avraam, S., Hatzipanayioti, A., & Avraamides, M. N. (2018). Orientation-dependent spatial memories for scenes viewed on mobile devices. Psychological Research Psychologische Forschung.  https://doi.org/10.1007/s00426-018-1069-5.CrossRefPubMedGoogle Scholar
  3. Avraamides, M. N., & Kelly, J. W. (2008). Multiple systems of spatial memory and action. Cognitive Processing, 9, 93–106.  https://doi.org/10.1007/s10339-007-0188-5.CrossRefPubMedGoogle Scholar
  4. Avraamides, M. N., Sarrou, M., & Kelly, J. W. (2014). Cross-sensory reference frame transfer in spatial memory: The case of proprioceptive learning. Memory & Cognition, 42, 496–507.  https://doi.org/10.3758/s13421-013-0373-y.CrossRefGoogle Scholar
  5. Bassett, J. P., Wills, T. J., & Cacucci, F. (2018). Self-organized attractor dynamics in the developing head direction circuit. Current Biology, 28, 609–615.  https://doi.org/10.1016/j.cub.2018.01.010.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Berkeley, G. (1709). An essay towards a new theory of vision. Dublin: Aaron Rhames.Google Scholar
  7. Bremner, J. G., Hatton, F., Foster, K. A., & Mason, U. (2011). The contribution of visual and vestibular information to spatial orientation by 6- to 14-month-old infants and adults. Developmental Science, 14, 1033–1045.  https://doi.org/10.1111/j.1467-7687.2011.01051.x.CrossRefPubMedGoogle Scholar
  8. Bruggeman, H., Zosh, W., & Warren, W. H. (2007). Optic flow drives human visuo-locomotor adaptation. Current Biology, 17, 2035–2040.  https://doi.org/10.1016/j.cub.2007.10.059.CrossRefPubMedGoogle Scholar
  9. Campos, J. L., Butler, J. S., & Bülthoff, H. H. (2014). Contributions of visual and proprioceptive information to travelled distance estimation during changing sensory congruencies. Experimental Brain Research, 232(10), 3277–3289.  https://doi.org/10.1007/s00221-014-4011-0.CrossRefPubMedGoogle Scholar
  10. Chen, X., McNamara, T. P., Kelly, J. W., & Wolbers, T. (2017). Cue combination in human spatial navigation. Cognitive Psychology, 95, 105–144.  https://doi.org/10.1016/j.cogpsych.2017.04.003.CrossRefPubMedGoogle Scholar
  11. Cheng, K., Shettleworth, S. J., Huttenlocher, J., & Rieser, J. J. (2007). Bayesian integration of spatial information. Psychological Bulletin, 133, 625–637.  https://doi.org/10.1037/0033-2909.133.4.625.CrossRefPubMedGoogle Scholar
  12. Chihak, B. J., Grechkin, T. Y., Kearney, J. K., Cremer, J. F., & Plumert, J. M. (2014). How children and adults learn to intercept moving gaps. Journal of Experimental Child Psychology, 122, 134–152.  https://doi.org/10.1016/j.jecp.2013.12.006.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ellard, C. G., & Shaughnessy, S. C. (2003). A comparison of visual and nonvisual sensory inputs to walked distance in a blind-walking task. Perception, 32, 567–578.  https://doi.org/10.1068/p5041.CrossRefPubMedGoogle Scholar
  14. Gallistel, C. R. (2009). The importance of proving the null. Psychological Review, 116(2), 439–453.  https://doi.org/10.1037/a0015251.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Giudice, N. A., Betty, M. R., & Loomis, J. M. (2011). Functional equivalence of spatial images from touch and vision: Evidence from spatial updating in blind and sighted individuals. Journal of Experimental Psychology: Learning, Memory, and Cognition, 37, 621–634.  https://doi.org/10.1037/a0022331.CrossRefPubMedGoogle Scholar
  16. Glass, G. V., McGaw, B., & Smith, M. L. (1981). Meta-analysis in social research. New York: Sage Publications.Google Scholar
  17. Harris, C. S. (1963). Adaptation to displaced vision: Visual, motor, or proprioceptive change? Science, 140, 812–813.  https://doi.org/10.1126/science.140.3568.812.CrossRefPubMedGoogle Scholar
  18. Kearns, M. J., Warren, W. H., Duchon, A. P., & Tarr, M. J. (2002). Path integration from optic flow and body senses in a homing task. Perception, 31, 349–374.  https://doi.org/10.1068/p3311.CrossRefPubMedGoogle Scholar
  19. Klatzky, R. L., Loomis, J. M., Beall, A. C., Chance, S. S., & Golledge, R. G. (1998). Spatial updating of self-position and orientation during real, imagined, and virtual locomotion. Psychological Science, 9(4), 293–298.  https://doi.org/10.1111/1467-9280.00058.CrossRefGoogle Scholar
  20. Loomis, J. M., Klatzky, R. L., & Giudice, N. A. (2013). Representing 3D space in working memory: Spatial images from vision, hearing, touch, and language. In S. Lacey & R. Lawson (Eds.), Multisensory imagery (1st ed., pp. 131–155). New York: Springer.  https://doi.org/10.1007/978-1-4614-5879-1.CrossRefGoogle Scholar
  21. Loomis, J. M., Klatzky, R. L., Golledge, R. G., Cicinelli, J. G., Pellegrino, J. W., & Fry, P. A. (1993). Nonvisual navigation by blind and sighted: Assessment of path integration ability. Journal of Experimental Psychology: General, 122(1), 73–91.  https://doi.org/10.1037/0096-3445.122.1.73.CrossRefGoogle Scholar
  22. Loomis, J. M., Klatzky, R. L., Golledge, R. G., & Philbeck, J. W. (1999). Human navigation by path integration. In R. G. Golledge (Ed.), Wayfinding behavior: Cognitive mapping and other spatial processes (pp. 125–151). Baltimore: John Hopkins University Press.Google Scholar
  23. Mou, W., McNamara, T. P., & Zhang, L. (2013). Global frames of reference organize configural knowledge of paths. Cognition, 129, 180–193.  https://doi.org/10.1016/j.cognition.2013.06.015.CrossRefPubMedGoogle Scholar
  24. Nardini, M., & Cowie, D. (2012). The development of multisensory balance, locomotion, orientation and navigation. In A. J. Bremner, D. J. Lewkowicz, & C. Spencer (Eds.), Multisensory development. Oxford: Oxford University Press.  https://doi.org/10.1093/acprof.CrossRefGoogle Scholar
  25. Nardini, M., Jones, P., Bedford, R., & Braddick, O. (2008). Development of cue integration in human navigation. Current Biology, 18, 689–693.  https://doi.org/10.1016/j.cub.2008.04.021.CrossRefPubMedGoogle Scholar
  26. Philbeck, J. W., Klatzky, R. L., Berhrman, M., Loomis, J. M., & Goodridge, J. (2001). Active control of locomotion facilities nonvisual navigation. Journal of Experimental Psychology: Human Learning and Memory, 27(1), 141–153.Google Scholar
  27. Philbeck, J. W., & O’Leary, S. (2005). Remembered landmarks enhance the precision of path integration. Psicologica, 26, 7–24.Google Scholar
  28. Pick, H. L., Rieser, J. J., Wagner, D., & Garing, A. E. (1999). The recalibration of rotational locomotion. Journal of Experimental Psychology: Human Perception and Performance, 25(5), 1179–1188.Google Scholar
  29. Rieser, J. J. (1989). Access to knowledge of spatial structure at novel points of observation. Journal of Experimental Psychology: Learning, Memory, and Cognition, 15(6), 1157–1165.  https://doi.org/10.1037/0278-7393.15.6.1157.CrossRefPubMedGoogle Scholar
  30. Rieser, J. J. (1999). Dynamic spatial orientation and the coupling of representation and action. In R. G. Golledge (Ed.), Wayfinding behavior: Cognitive mapping and other spatial processes (pp. 168–190). Baltimore: JHU Press.Google Scholar
  31. Rieser, J. J., Guth, D. A., & Hill, E. W. (1986). Sensitivity to perspective structure while walking without vision. Perception, 15, 173–188.CrossRefGoogle Scholar
  32. Rieser, J. J., & Heiman, M. L. (1982). Spatial self-reference systems and shortest-route behavior in toddlers. Child Development, 53(2), 524–533.CrossRefGoogle Scholar
  33. Rieser, J. J., & Pick, H. L. (2007). Using locomotion to update spatial orientation: What changes with learning and development? In J. M. Plumert & J. P. Spencer (Eds.), The emerging spatial mind (pp. 77–103). New York: Oxford University Press.CrossRefGoogle Scholar
  34. Rieser, J. J., Pick, H. L., Ashmead, D. H., & Garing, A. E. (1995). Calibration of human locomotion and models of perceptual-motor organization. Journal of Experimental Psychology: Human Perception and Performance, 21, 480–497.PubMedGoogle Scholar
  35. Rouder, J. N., Speckman, P. L., Sun, D., Morey, R. D., & Iverson, G. (2009). Bayesian t tests for accepting and rejecting the null hypothesis. Psychonomic Bulletin & Review, 16(2), 225–237.  https://doi.org/10.3758/PBR.16.2.225.CrossRefGoogle Scholar
  36. Shelton, A. L., & McNamara, T. P. (2001). Systems of spatial reference in human memory. Cognitive Psychology, 43, 274–310.  https://doi.org/10.1006/cogp.2001.0758.CrossRefPubMedGoogle Scholar
  37. Tan, H. M., Bassett, J. P., O’Keefe, J., Cacucci, F., & Wills, T. J. (2015). The development of the head direction system before eye opening in the rat. Current Biology, 25, 479–483.  https://doi.org/10.1016/j.cub.2014.12.030.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Tcheang, L., Bülthoff, H. H., & Burgess, N. (2011). Visual influence on path integration in darkness indicates a multimodal representation of large-scale space. Proceedings of the National Academy of Sciences of the United States of America, 108(3), 1152–1157.  https://doi.org/10.1073/pnas.1011843108.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Thinus-Blanc, C., & Gaunet, F. (1997). Representation of space in blind persons: Vision as a spatial sense? Psychological Bulletin, 121(1), 20–42.  https://doi.org/10.1037//0033-2909.121.1.20.CrossRefPubMedGoogle Scholar
  40. Warren, D. H. (1970). Intermodality interactions in spatial localization. Cognitive Psychology, 1(2), 114–133.  https://doi.org/10.1016/0010-0285(70)90008-3.CrossRefGoogle Scholar
  41. Yamamoto, N., Meléndez, J. A., & Menzies, D. T. (2014). Homing by path integration when a locomotion trajectory crosses itself. Perception, 43, 1049–1060.  https://doi.org/10.1068/p7624.CrossRefPubMedGoogle Scholar
  42. Yamamoto, N., & Shelton, A. L. (2005). Visual and proprioceptive representations in spatial memory. Memory & Cognition, 33(1), 140–150.  https://doi.org/10.3758/BF03195304.CrossRefGoogle Scholar
  43. Yamamoto, N., & Shelton, A. L. (2009). Orientation dependence of spatial memory acquired from auditory experience. Psychonomic Bulletin & Review, 16, 301–305.  https://doi.org/10.3758/PBR.16.2.301.CrossRefGoogle Scholar
  44. Zhao, M., & Warren, W. H. (2015). How you get there from here: Interaction of visual landmarks and path integration in human navigation. Psychological Science, 26, 1–10.CrossRefGoogle Scholar
  45. Ziemer, C. J., Branson, M. J., Chihak, B. J., Kearney, J. K., Cremer, J. F., & Plumert, J. M. (2013). Manipulating perception versus action in recalibration tasks. Attention, Perception, & Psychophysics, 75, 1260–1274.  https://doi.org/10.3758/s13414-013-0473-6.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of AlbertaEdmontonCanada

Personalised recommendations