Development of spatial orientation skills: an fMRI study

  • Kara MuriasEmail author
  • Edward Slone
  • Sana Tariq
  • Giuseppe Iaria


The ability to orient and navigate in spatial surroundings is a cognitive process that undergoes a prolonged maturation with progression of skills, strategies and proficiency over much of childhood. In the present study, we used functional Magnetic Resonance Imaging (fMRI) to investigate the neurological mechanisms underlying the ability to orient in a virtual interior environment in children aged 10 to 12 years of age, a developmental stage in which children start using effective spatial orientation strategies in large-scale surroundings. We found that, in comparison to young adults, children were not as proficient at the spatial orientation task, and revealed increased neural activity in areas of the brain associated with visuospatial processing and navigation (left cuneus and mid occipital area, left inferior parietal region and precuneus, right inferior parietal cortex, right precentral gyrus, cerebellar vermis and bilateral medial cerebellar lobes). When functional connectivity analyses of resting state fMRI data were performed, using seed areas that were associated with performance, increased connectivity was seen in the adults from the right hippocampal/parahippocampal gyrus to the contralateral caudate, the insular cortex, and the posterior supramarginal gyrus; children had increased connectivity from the right paracentral lobule to the right superior frontal gyrus as compared to adults. These findings support the hypothesis that, as children are maturing in their navigation abilities, they are refining and increasing the proficiency of visuospatial skills with a complimentary increase in connectivity of longer-range distributed networks allowing for flexible use of efficient and effective spatial orientation strategies.


Children Cognitive Hippocampus Memory Navigation 



This study was financially supported by a Discovery grants from Natural Sciences and Engineering Council of Canada (NSERC) awarded to Guiseppe Iaria. Kara Murias was supported by Alberta Children’s Hospital Foundation through ACHRI and Alberta Innovates-Health Solutions.

Compliance with ethical standards

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation.


Kara Murias, Edward Slone, Sana Tariq, and Giuseppe Iaria declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all patients for being included in the study.


  1. Aguirre, G. K., Detre, J. A., Alsop, D. C., & D'Esposito, M. (1996). The parahippocampus subserves topographical learning in man. Cerebral cortex (New York, N.Y.: 1991), 6(6), 823–829.CrossRefGoogle Scholar
  2. Blankenship, S. L., Redclay, E., Dougherty, L. R., & Riggins, T. (2017). Development of hippocampal functional connectivity during childhood. Human Brain Mapping, 38, 182–201. Scholar
  3. Bohbot, V. D., Lerch, J., Thorndycraft, B., Iaria, G., & Zijdenbos, A. P. (2007). Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. The Journal of neuroscience : the official journal of the Society for Neuroscience, 27(38), 10078–10083. Scholar
  4. Bohbot, V. D., McKenzie, S., Konishi, K., Fouquet, C., Kurdi, V., Schachar, R., . . . Robaey, P. (2012). Virtual navigation strategies from childhood to senescence: Evidence for changes across the life span. Frontiers in Aging Neuroscience, 4, 28. Scholar
  5. Bullens, J., Igloi, K., Berthoz, A., Postma, A., & Rondi-Reig, L. (2010). Developmental time course of the acquisition of sequential egocentric and allocentric navigation strategies. Journal of Experimental Child Psychology, 107(3), 337–350. Scholar
  6. Burgess, N., Maguire, E. A., & O'Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron, 35(4), 625–641.CrossRefGoogle Scholar
  7. Chen, Q., Weidner, R., Vossel, S., Weiss, P. H., & Fink, G. R. (2012). Neural mechanisms of attentional reorienting in three-dimensional space. The Journal of Neuroscience, 32(39), 13352–13362. Scholar
  8. Dosenbach, N. U., Nardos, B., Cohen, A. L., Fair, D. A., Power, J. D., Church, J. A., . . . Schlaggar, B. L. (2010). Prediction of individual brain maturity using fMRI. Science (New York, N.Y.), 329(5997), 1358–1361. Scholar
  9. Dudchenko, P. (2010). Why People Get Lost: The Psychology and Neuroscience of Spatial Cognition. Great Britain: Oxford University Press.Google Scholar
  10. Ekstrom, A. D., Arnold, A. E., & Iaria, G. (2014). A critical review of the allocentric spatial representation and its neural underpinnings: toward a network-based perspective. Frontiers in Human Neuroscience, 8, 803. Scholar
  11. Fair, D. A., Cohen, A. L., Power, J. D., Dosenbach, N. U., Church, J. A., Miezin, F. M., . . . Petersen, S. E. (2009). Functional brain networks develop from a "local to distributed" organization. PLoS Computational Biology, 5(5), e1000381. Scholar
  12. Floegel, M., & Kell, C. A. (2017). Functional hemispheric asymmetries during the planning and manual control of virtual avatar movements. PLoS One, 12(9), e0185152. Scholar
  13. Goodale, M. A., & Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15(1), 20–25.CrossRefGoogle Scholar
  14. Hayne, H., Rovee-Collier, C., & Borza, M. A. (1991). Infant memory for place information. Memory & Cognition, 19(4), 378–386.CrossRefGoogle Scholar
  15. Hermer, L., Spelke, E. S. (1994). A geometric process for spatial reorientation in young children. Nature, Jul 7 370(6484),57–59.Google Scholar
  16. Hirnstein, M., Bayer, U., Ellison, A., & Hausmann, M. (2011). TMS over the left angular gyrus impairs the ability to discriminate left from right. Neuropsychologia, 49(1), 29–33. Scholar
  17. Huttenlocher, J., & Vasilyeva, M. (2003). How toddlers represent enclosed spaces. Cognitive Science, 27, 749–766. Scholar
  18. Iaria, G., Petrides, M., Dagher, A., Pike, B., & Bohbot, V. D. (2003). Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. The Journal of neuroscience : the official journal of the Society for Neuroscience, 23(13), 5945–5952.CrossRefGoogle Scholar
  19. Learmonth, A. E., Newcombe, N. S., Sheridan, N., & Jones, M. (2008). Why size counts: children's spatial reorientation in large and small enclosures. Developmental Science, 11(3), 414–426. Scholar
  20. Liu, I., Levy, R. M., Barton, J. J., & Iaria, G. (2011). Age and gender differences in various topographical orientation strategies. Brain Research, 1410, 112–119. Scholar
  21. Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: A network model of insula function. Brain Structure & Function, 214(5–6), 655–667. Scholar
  22. Muller, R. U., Ranck, J. B., Jr., & Taube, J. S. (1996). Head direction cells: Properties and functional significance. Current Opinion in Neurobiology, 6(2), 196–206.CrossRefGoogle Scholar
  23. Nardini, M., Atkinson, J., & Burgess, N. (2008). Children reorient using the left/right sense of coloured landmarks at 18-24 months. Cognition, 106(1), 519–527. Scholar
  24. Nazareth, A., Weisberg, S. M., Margulis, K., & Newcombe, N. S. (2018). Charting the development of cognitive mapping. Journal of Experimental Child Psychology, 170, 86–106. Scholar
  25. Negen, J., & Nardini, M. (2015). Four-year-olds use a mixture of spatial reference frames. PLoS One, 10(7), e0131984. Scholar
  26. Newcombe, N. S., Ratliff, K. R., Shallcross, W. L., & Twyman, A. D. (2010). Young children's use of features to reorient is more than just associative: Further evidence against a modular view of spatial processing. Developmental Science, 13(1), 213–220. Scholar
  27. O'Keefe, J., & Nadel, L. (1978). The Hippocampus as a cognitive map. Oxford University Press.Google Scholar
  28. Pine, D. S., Grun, J., Maguire, E. A., Burgess, N., Zarahn, E., Koda, V., . . . Bilder, R. M. (2002). Neurodevelopmental aspects of spatial navigation: A virtual reality fMRI study. NeuroImage, 15(2), 396–406. Scholar
  29. Ptak, R. (2012). The frontoparietal attention network of the human brain: Action, saliency, and a priority map of the environment. Neuroscientist, 18(5), 502–515. Scholar
  30. Ptak, R., Schnider, A., & Fellrath, J. (2017). The dorsal Frontoparietal network: A Core system for emulated action. Trends in Cognitive Sciences, 21(8), 589–599. Scholar
  31. Ribordy, F., Jabes, A., Banta Lavenex, P., & Lavenex, P. (2013). Development of allocentric spatial memory abilities in children from 18 months to 5 years of age. Cognitive Psychology, 66(1), 1–29.
  32. Rochefort, C., Lefort, J. M., & Rondi-Reig, L. (2013). The cerebellum: A new key structure in the navigation system. Front Neural Circuits, 7, 35. Scholar
  33. Saluja, S., Chen, J., Gagnon, I. J., Keightley, M., & Ptito, A. (2015). Navigational memory functional magnetic resonance imaging: A test for concussion in children. Journal of Neurotrauma, 32, 712–722. Scholar
  34. Schedlbauer, A. M., Copara, M. S., Watrous, A. J., & Ekstrom, A. D. (2014). Multiple interacting brain areas underlie successful spatiotemporal memory retrieval in humans. Scientific Reports, 4, 6431.
  35. Seydell-Greenwald, A., Ferrara, K., Chambers, C. E., Newport, E. L., & Landau, B. (2017). Bilateral parietal activations for complex visual-spatial functions: Evidence from a visual-spatial construction task. Neuropsychologia, 106, 194–206. Scholar
  36. Siegel, A. W., & White, S. H. (1975). The development of spatial representations of large-scale environments. Advances in Child Development and Behavior, 10, 9–55.CrossRefGoogle Scholar
  37. Stock, O., Röder, B., Burke, M., Bien, S., & Rösler, F. (2009). Cortical activation patterns during long-term memory retrieval of visually or haptically encoded objects and locations. Journal of Cognitive Neuroscience, 21(1), 58–82. Scholar
  38. Takahashi, N., & Kawamura, M. (2002). Pure topographical disorientation--the anatomical basis of landmark agnosia. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 38(5), 717–725.CrossRefGoogle Scholar
  39. van Asselen, M., Kessels, R. P., Kappelle, L. J., Neggers, S. F., Frijns, C. J., & Postma, A. (2006). Neural correlates of human wayfinding in stroke patients. Brain Research, 1067(1), 229–238. Scholar
  40. van den Brink, D., & Janzen, G. (2013). Visual spatial cue use for guiding orientation in two-to-three-year-old children. Frontiers in psychology, 4, 904.
  41. van Ekert, J., Wegman, J., & Janzen, G. (2015). Neurocognitive development of memory of landmarks. Frontiers in Psychology. March, 6(224).
  42. Vogel, A. C., Power, J. D., Petersen, S. E., & Schlaggar, B. L. (2010). Development of the brain's functional network architecture. Neuropsychology Review, 20(4), 362–375. Scholar
  43. Waismeyer, A. S., & Jacobs, L. F. (2013). The emergence of flexible spatial strategies in young children. Developmental Psychology, 49(2), 232–242.
  44. Zhang, S., Ide, J. S., & Li, C. S. (2012). Resting-state functional connectivity of the medial superior frontal cortex. Cerebral Cortex, 22(1), 99–111. Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Developmental Pediatrics – Cumming School of MedicineOwerko Centre, University of CalgaryCalgaryCanada
  2. 2.Alberta Children’s Hospital Research InstituteCalgaryCanada
  3. 3.Neurolab (, Department of Psychology, Hotchkiss Brain Institute and Alberta Children’s Hospital Research InstituteUniversity of CalgaryCalgaryCanada

Personalised recommendations