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Experimental Brain Research

, Volume 194, Issue 4, pp 541–552 | Cite as

Selective influence of prior allocentric knowledge on the kinesthetic learning of a path

  • Matthieu LafonEmail author
  • Manuel Vidal
  • Alain Berthoz
Research Article

Abstract

Spatial cognition studies have described two main cognitive strategies involved in the memorization of traveled paths in human navigation. One of these strategies uses the action-based memory (egocentric) of the traveled route or paths, which involves kinesthetic memory, optic flow, and episodic memory, whereas the other strategy privileges a survey memory of cartographic type (allocentric). Most studies have dealt with these two strategies separately, but none has tried to show the interaction between them in spite of the fact that we commonly use a map to imagine our journey and then proceed using egocentric navigation. An interesting question is therefore: how does prior allocentric knowledge of the environment affect the egocentric, purely kinesthetic navigation processes involved in human navigation? We designed an experiment in which blindfolded subjects had first to walk and memorize a path with kinesthetic cues only. They had previously been shown a map of the path, which was either correct or distorted (consistent shrinking or growing). The latter transformations were studied in order to observe what influence a distorted prior knowledge could have on spatial mechanisms. After having completed the first learning travel along the path, they had to perform several spatial tasks during the testing phase: (1) pointing towards the origin and (2) to specific points encountered along the path, (3) a free locomotor reproduction, and (4) a drawing of the memorized path. The results showed that prior cartographic knowledge influences the paths drawn and the spatial inference capacity, whereas neither locomotor reproduction nor spatial updating was disturbed. Our results strongly support the notion that (1) there are two independent neural bases underlying these mechanisms: a map-like representation allowing allocentric spatial inferences, and a kinesthetic memory of self-motion in space; and (2) a common use of, or a switching between, these two strategies is possible. Nevertheless, allocentric representations can emerge from the experience of kinesthetic cues alone.

Keywords

Spatial memory Kinesthesia Prior knowledge Allocentric Egocentric Path integration 

Notes

Acknowledgments

The authors wish to thank Halim Hicheur, France Maloumian and Guillaume Thibault for their technical help and/or comments on this manuscript. The authors thank Marios Avraamides and two anonymous reviewer for the helpful comments on this manuscript. This study was supported by CNES (France). Matthieu Lafon is in receipt of a 3-year EDF R&D grant and a ‘CIFRE’ grant from the French Government for his doctoral research.

Supplementary material

References

  1. Adamovich SV, Berkinblit MB, Fookson O, Poizner H (1998) Pointing in 3D space to remembered targets. I. Kinesthetic versus visual target presentation. J Neurophysiol 79(6):2833–2846PubMedGoogle Scholar
  2. Amorim MA, Glasauer S, Corpinot K, Berthoz A (1997) Updating an object’s orientation and location during nonvisual navigation: a comparison between two processing modes. Percept Psychophys 59:404–418PubMedGoogle Scholar
  3. Annett J (1995) Motor imagery: perception or action? Neuropsychologia 33(11):1395–1417PubMedCrossRefGoogle Scholar
  4. Avraamides MN, Kelly JW (2008) Multiple systems of spatial memory and action. Cogn Process 9(2):93–106PubMedCrossRefGoogle Scholar
  5. Avraamides MN, Klatzky RL, Loomis JM, Golledge RG (2004) Use of cognitive versus perceptual heading during imagined locomotion depends on the response mode. Psychol Sci 15:403–408PubMedCrossRefGoogle Scholar
  6. Berthoz A (1997) Parietal and hippocampal contribution to topokinetic and topographic memory. Philos Trans R Soc Lond B Biol Sci 352:1437–1448PubMedCrossRefGoogle Scholar
  7. Berthoz A, Viaud-Delmon I (1999) Multisensory integration in spatial orientation. Curr Opin Neurobiol 9(6):708–712PubMedCrossRefGoogle Scholar
  8. Burgess N (2006) Spatial memory: how egocentric and allocentric combines. Trends Cogn Sci 10(12):551–557PubMedCrossRefGoogle Scholar
  9. Committeri G, Galati G, Paradis AL, Pizzamiglio L, Berthoz A, LeBihan D (2004) Reference frames for spatial cognition: different brain areas are involved in viewer-, object-, and landmark-centered judgments about object location. J Cogn Neurosci 16:1517–1535PubMedCrossRefGoogle Scholar
  10. Daniel MP, Mores C, Carite L, Boyer P, Denis M (2006) Dysfunctions of spatial cognition: the case of schizophrenic patients. Cogn Process 7(Suppl 5):173CrossRefGoogle Scholar
  11. Durgin FH, Pelah A, Fox LF, Lewis J, Kane R, Walley KA (2005) Self-motion perception during locomotor recalibration: more than meets the eye. J Exp Psychol Hum Percept Perform 31(3):398–419PubMedCrossRefGoogle Scholar
  12. Easton RD, Sholl MJ (1995) Object-array structure, frames of reference, and retrieval of spatial knowledge. J Exp Psychol Learn Mem Cogn 21(2):483–500PubMedCrossRefGoogle Scholar
  13. Elliott D (1986) Continuous visual information may be important after all: a failure to replicate Thomson (1983). J Exp Psychol Hum Percept Perform 12:388–391PubMedCrossRefGoogle Scholar
  14. Elliott D (1987) The influence of walking speed and prior practice on locomotor distance estimation. J Mot Behav 19(4):476–485PubMedGoogle Scholar
  15. Gaunet F, Vidal M, Kemeny A, Berthoz A (2001) Active, passive and snapshot exploration in a virtual environment: influence on scene memory, reorientation and path memory. Brain Res Cogn Brain Res 11(3):409–420PubMedCrossRefGoogle Scholar
  16. Ghaem O, Mellet E, Crivello F, Tzourio N, Mazoyer B, Berthoz A, Denis M (1997) Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport 8:739–744PubMedCrossRefGoogle Scholar
  17. Glasauer S, Amorim MA, Vitte E, Berthoz A (1994) Goal-directed linear locomotion in normal and labyrinthine-defective subjects. Exp Brain Res 98:323–335PubMedCrossRefGoogle Scholar
  18. Jurgens R, Becker W (2006) Perception of angular displacement without landmarks: evidence for Bayesian fusion of vestibular, optokinetic, podokinesthetic, and cognitive information. Exp Brain Res 174(3):528–543PubMedCrossRefGoogle Scholar
  19. Kelly JW, Avraamides MN, Loomis JM (2008) Sensorimotor alignment effects in the learning environment and in novel environments. J Exp Psychol Learn Mem Cogn 33(6):1092–1107Google Scholar
  20. Klatzky RL (1999) Path completion after haptic exploration without vision: implications for haptic spatial representations. Percept Psychophys 61:220–235PubMedGoogle Scholar
  21. Klatzky RL, Loomis JM, Golledge RG, Cicinelli JG, Doherty S, Pellegrino JW (1990) Acquisition of route and survey knowledge in the absence of vision. J Mot Behav 22:19–43PubMedGoogle Scholar
  22. Klatzky RL, Loomis JM, Beall AC, Chance SS, Golledge RG (1998) Spatial updating of self-position and orientation during real, imagined, and virtual locomotion. Psychol Sci 9:293–298CrossRefGoogle Scholar
  23. Lambrey S, Berthoz A (2003) Combination of conflicting visual and non-visual information for estimating actively performed body turns in virtual reality. Int J Psychophysiol 50(1–2):101–115PubMedCrossRefGoogle Scholar
  24. Lambrey S, Viaud-Delmon I, Berthoz A (2002) Influence of a sensorimotor conflict on the memorization of a path travelled in virtual reality. Brain Res Cogn Brain Res 1:177–186CrossRefGoogle Scholar
  25. Loomis JM, Klatzky RL, Golledge RG, Cicinelli JG, Pellegrino JW, Fry PA (1993) Nonvisual navigation by blind and sighted: assessment of path integration ability. J Exp Psychol Gen 122:73–91PubMedCrossRefGoogle Scholar
  26. Loomis JM, Klatzky RL, Golledge RG (2001) Navigating without vision: basic and applied research. Optom Vis Sci 78:282–289PubMedCrossRefGoogle Scholar
  27. Mellet E, Briscogne S, Tzourio-Mazoyer N, Ghaem O, Petit L, Zago L, Etard O, Berthoz A, Mazoyer B, Denis M (2000) Neural correlates of topographic mental exploration: the impact of route versus survey perspective learning. Neuroimage 12:588–600PubMedCrossRefGoogle Scholar
  28. Mou W, McNamara TP, Valiquette CM, Rump B (2004) Allocentric and egocentric updating of spatial memories. J Exp Psychol Learn Mem Cogn 30(1):142–157PubMedCrossRefGoogle Scholar
  29. Mou W, Li X, McNamara TP (2008) Body- and environmental-stabilized processing of spatial knowledge. J Exp Psychol Learn Mem Cogn 34(2):415–421PubMedCrossRefGoogle Scholar
  30. Philbeck JW, Klatzky RL, Behrmann M, Loomis JM, Goodridge J (2001) Active control of locomotion facilitates nonvisual navigation. J Exp Psychol Hum Percept Perform 27:141–153PubMedCrossRefGoogle Scholar
  31. Rieser JJ, Lockman JJ, Pick HL Jr (1980) The role of visual experience in knowledge of spatial layout. Percept Psychophys 28:185–190PubMedGoogle Scholar
  32. Rieser JJ, Ashmead DH, Talor CR, Youngquist GA (1990) Visual perception and the guidance of locomotion without vision to previously seen targets. Perception 19:675–689PubMedCrossRefGoogle Scholar
  33. Salinas E (2004) Context-dependent selection of visuomotor maps. BMC Neurosci 5(1):47PubMedCrossRefGoogle Scholar
  34. Shelton AL, McNamara TP (2004) Orientation and perspective dependence in route and survey learning. J Exp Psychol Learn Mem Cogn 30:158–170PubMedCrossRefGoogle Scholar
  35. Steenhuis RE, Goodale MA (1988) The effects of time and distance on accuracy of target-directed locomotion: does an accurate short-term memory for spatial location exist? J Mot Behav 20:399–415PubMedGoogle Scholar
  36. Takei Y, Grasso R, Amorim MA, Berthoz A (1997) Circular trajectory formation during blind locomotion: a test for path integration and motor memory. Exp Brain Res 115:361–368PubMedCrossRefGoogle Scholar
  37. Thomson JA (1983) Is continuous visual monitoring necessary in visually guided locomotion? J Exp Psychol Hum Percept Perform 9(3):427–443PubMedCrossRefGoogle Scholar
  38. Thomson JA (1986) Intermittent versus continuous visual control: a reply to Elliott. J Exp Psychol Hum Percept Perform 12:392–393PubMedCrossRefGoogle Scholar
  39. Thorndyke PW, Hayes-Roth B (1982) Differences in spatial knowledge acquired from maps and navigation. Cogn Psychol 14(4):560–589PubMedCrossRefGoogle Scholar
  40. Vieilledent S, Kosslyn SM, Berthoz A, Giraudo MD (2003) Does mental simulation of following a path improve navigation performance without vision? Brain Res Cogn Brain Res 16:238–249PubMedCrossRefGoogle Scholar
  41. Waller D, Hodgson E (2006) Transient and enduring spatial representations under disorientation and self-rotation. J Exp Psychol Learn Mem Cogn 32(4):867–882PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Laboratoire de Physiologie de la Perception et de l’Action (LPPA)CNRS Collège de FranceParisFrance

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