Abstract
Spatial navigation from memory can rely on two different strategies: a mental simulation of a kinesthetic spatial navigation (egocentric route strategy) or visual-spatial memory using a mental map (allocentric survey strategy). We hypothesized that a previously performed “oculomotor navigation” on a map could be used by the brain to perform a locomotor memory task. Participants were instructed to (1) learn a path on a map through a sequence of vertical and horizontal eyes movements and (2) walk on the slabs of a “magic carpet” to recall this path. The main results showed that the anisotropy of ocular movements (horizontal ones being more efficient than vertical ones) influenced performances of participants when they change direction on the central slab of the magic carpet. These data suggest that, to find their way through locomotor space, subjects mentally repeated their past ocular exploration of the map, and this visuo-motor memory was used as a template for the locomotor performance.
Similar content being viewed by others
References
Andersen NE, Dahmani L, Konishi K, Bohbot VD (2012) Eye tracking, strategies, and sex differences in virtual navigation. Neurobiol Learn Mem 97(1):81–89
Berthoz A (1997) Parietal and hippocampal contribution to topokinetic and topographic memory. Philos Trans R Soc 352(1360):1437–1448
Brunyé TT, Mahoney CR, Augustyn JS, Taylor HA (2009) Horizontal saccadic eye movements enhance the retrieval of landmark shape and location information. Brain Cogn 70(3):279–288
Burgess N (2006) Spatial memory: how egocentric and allocentric combine. Trends Cogn Sci 10(12):551–557
Galati G, Pelle G, Berthoz A, Committeri G (2010) Multiple reference frames used by the human brain for spatial perception and memory. Exp Brain Res 206:109–120
Gentilucci M, Daprati E, Gangitano M (1998) Haptic information differentially interferes with visual analysis in reaching-grasping control and in perceptual processes. NeuroRep 9(5):887–891
Grönqvist H, Gredebäck G, von Hofsten C (2006) Developmental asymmetries between horizontal and vertical tracking. Vis Res 46(11):1754–1761
Heremans E, Helsen WF, Feys P (2008) The eyes as a mirror of our thoughts: quantification of motor imagery of goal-directed movements through eye movement registration. Behav Brain Res 187(2):351–360
Heremans E, Smits-Engelsman B, Caeyenberghs K, Vercruysse S, Nieuwboer A, Feys P, Helsen WF (2011) Keeping an eye on imagery: the role of eye movements during motor imagery training. Neurosci 195:37–44
Hesslow G (2012) The current status of the simulation theory of cognition. Brain Res 1428:71–79
Höllinger P, Beisteiner R, Lang W, Lindinger G, Berthoz A (1999) Mental representations of movements. Brain potentials associated with imagination of eye movements. Clin Neurophysiol 110:799–805
Hoyek N, Champely S, Collet C, Fargier P, Guillot A (2009) Age and gender-related differences in the temporal congruence development between motor imagery and motor performance. Learn Individ Differ 19(4):555–560
Hutton JT, Nagel JA, Loewenson RB (1983) Variables affecting eye tracking performance. Electroencephalogr Clin Neurophysiol 56(5):414–419
Ingster-Moati I, Vaivre-Douret L, Bui Quoc E, Albuisson E, Dufier J-L, Golse B (2009) Vertical and horizontal smooth pursuit eye movements in children: a neuro-developmental study. Eur J Paediatr Neurol 13(4):362–366
Kimura D (1999) Sex and cognition. MIT Press, Cambridge
Klatzky RL (1998) Allocentric and egocentric spatial representations: definitions, distinctions, and interconnections. In: Freksa C, Habel C, Wender KF (eds) Spatial cognition, an interdisciplinary approach to representing and processing spatial knowledge. Springer, Berlin, pp 1–18
Kunz BR, Creem-Regehr SH, Thompson WB (2009) Evidence for motor simulation in imagined locomotion. J Exp Psychol Hum Percept Perform 35(5):1458–1471
Laeng B, Teodorescu D-S (2002) Eye scanpaths during visual imagery reenact those of perception of the same visual scene. Cogn Sci 26:207–231
Lafon M, Vidal M, Berthoz A (2009) Selective influence of prior allocentric knowledge on the kinesthetic learning of a path. Exp Brain Res 194:541–552
Lambrey S, Berthoz A (2007) Gender differences in the use of external landmarks versus spatial representations updated by self-motion. J Integr Neurosci 6(3):1–23
Lang W, Petit L, Höllinger P, Pietrzyk U, Tzourio N, Mazoyer B, Berthoz A (1994) A positron emission tomography study of oculomotor imagery. NeuroRep 5:921–924
Meilinger T, Berthoz A, Wiener J (2011) The integration of spatial information across different viewpoints. Mem Cogn 39(6):1042–1054
Mellet E, Bricogne S, Tzourio-Mazoyer N, Ghaëm O, Petit L, Zago L, Etard O, Berthoz A, Mazoyer B, Denis M (2000) Neural correlates of topographic mental exploration: the impact of exocentric/egocentric perspective learning. NeuroImage 11(5 Suppl):S64
Nyberg L, Eriksson J, Larsson A, Marklund P (2006) Learning by doing versus learning by thinking: an fMRI study of motor and mental training. Neuropsychologia 44(5):711–717
Olivier G, Labiale G (2008) Ocular pursuit and visual memory of moving shapes. Neuropsychologia 46(11):2831–2835
Olivier G, Velay J-L, Labiale G, Celse C, Faure S (2004) Mental rotation and simulation of a reaching and grasping manual movement. Percept Mot Skills 98:1107–1116
Papaxanthis C, Pozzo T, Skoura X, Schieppati M (2002) Does order and timing performance of imagined and actual movements affect the motor imagery process? The duration of walking and writing task. Behav Brain Res 134:209–215
Piccardi L, Iaria G, Ricci M, Bianchini F, Zompanti L, Guariglia C (2008) Walking in the Corsi test: which type of memory do you need? Neurosci Lett 432(2):127–131
Piccardi L, Risetti M, Nori R, Tanzilli A, Bernardi L, Guariglia C (2011) Perspective changing in primary and secondary learning: a gender difference study. Learn Individ Differ 21(1):114–118
Pierrot-Deseilligny C, Müri RM, Ploner CJ, Gaymard B, Rivaud-Péchoux S (2003) Cortical control of ocular saccades in humans: a model for motricity. Prog Brain Res 142:3–17
Richardson D, Matlock T (2007) The integration of figurative language and static depictions: an eye movement study of fictive motion. Cognition 102(1):129–138
Rottach KG, Zivotofsky AZ, Das VE, Averbuch-Heller LEA, Discenna AO, Poonyathalang A, Leigh RJ (1996) Comparison of horizontal, vertical and diagonal smooth pursuit eye movements in normal human subjects. Vis Res 36(14):2189–2195
Vavrečka M (2009) The neural correlates of spatial reference frames processing. Cogn Process 10:342–345
Vieilledent S, Berthoz A, Kosslyn S, Giraudo MD (2003) Does mental simulation of following a path improve navigation performance without vision? Cogn Brain Res 16(2):238–249
Acknowledgments
We thank warmly Mahé Ben Hamed (BCL, CNRS, France) for revising the English.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Demichelis, A., Olivier, G. & Berthoz, A. Motor transfer from map ocular exploration to locomotion during spatial navigation from memory. Exp Brain Res 224, 605–611 (2013). https://doi.org/10.1007/s00221-012-3336-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-012-3336-9