Abstract
When we move toward a novel environment we may learn it in different ways, i.e., by walking around or studying a map. Both types of learning seem to be very effective in daily life navigation and correspond to two different types of mental representation of space: route and survey representation. In the present study, we investigated the neural basis of route and survey perspectives during learning and retrieval of novel environments. The study was carried out over 5 days, during which participants learned two paths from a different perspective (i.e., route learning and survey learning). Then participants had to retrieve these paths using a survey or route perspective during fMRI scans, on the first and fifth day. We found that the left inferior temporal lobe and right angular gyrus (AG) were activated more during recall of paths learned in a survey perspective than in a route perspective. We also found a session by perspective interaction effect on neural activity in brain areas classically involved in navigation such as the parahippocampal place area (PPA) and the retrosplenial cortex (RSC). A set of frontal, parietal and temporal areas showed different patterns of activity according to the type of retrieval perspective. We tested the context-dependent connectivity of right PPA, RSC and AG, finding that these areas showed different patterns of connectivity in relation to the learning and recalling perspective. Our results shed more light on the segregation of neural circuits involved in the acquisition of a novel environment and navigational strategies.
Similar content being viewed by others
References
Berthoz A (1997) Parietal and hippocampal contribution to topokinetic and topographic memory. Philos Trans R Soc Lond Ser B Biol Sci 352:1437–1448. doi:10.1098/rstb.1997.0130
Boccia M, Nemmi F, Guariglia C (2014) Neuropsychology of environmental navigation in humans: review and meta-analysis of FMRI studies in healthy participants. Neuropsychol Rev 24:236–251. doi:10.1007/s11065-014-9247-8
Boccia M, Piccardi L, Palermo L, Nemmi F, Sulpizio V, Galati G, Guariglia C (2015) A penny for your thoughts! Patterns of fMRI activity reveal the content and the spatial topography of visual mental images. Hum Brain Mapp 36:945–958. doi:10.1002/hbm.22678
Bonda E, Petrides M, Frey S, Evans A (1995) Neural correlates of mental transformations of the body-in-space. Proc Natl Acad Sci USA 92:11180–11184
Byrne P, Becker S, Burgess N (2007) Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol Rev 114:340–375. doi:10.1037/0033-295X.114.2.340
Epstein RA (2008) Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cognitive Sci 12:388–396. doi:10.1016/j.tics.2008.07.004
Epstein RA, Morgan LK (2012) Neural responses to visual scenes reveals inconsistencies between fMRI adaptation and multivoxel pattern analysis. Neuropsychologia 50:530–543. doi:10.1016/j.neuropsychologia.2011.09.042
Epstein RA, Parker WE, Feiler AM (2007) Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J Neurosci 27:6141–6149. doi:10.1523/JNEUROSCI.0799-07.2007
Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuro Image 6:218–229. doi:10.1006/nimg.1997.0291
Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuro Image 15:870–878. doi:10.1006/nimg.2001.1037
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. Neuro Rep 8:739–744
Gron G, Wunderlich AP, Spitzer M, Tomczak R, Riepe MW (2000) Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat Neurosci 3:404–408
Hartley T, Maguire EA, Spiers HJ, Burgess N (2003) The well-worn route and the path less traveled: distinct neural bases of route following and way finding in humans. Neuron 37:877–888
Hassabis D, Kumaran D, Maguire EA (2007) Using imagination to understand the neural basis of episodic memory. J Neurosci 27:14365–14374. doi:10.1523/Jneurosci.4549-07.2007
Hirshhorn M, Grady C, Rosenbaum RS, Winocur G, Moscovitch M (2012) The hippocampus is involved in mental navigation for a recently learned, but not a highly familiar environment: a longitudinal fMRI study. Hippocampus 22:842–852. doi:10.1002/Hipo.20944
Hotting K, Holzschneider K, Stenzel A, Wolbers T, Roder B (2013) Effects of a cognitive training on spatial learning and associated functional brain activations. BMC neuroscience 14:73. doi:10.1186/1471-2202-14-73
Iaria G, Chen JK, Guariglia C, Ptito A, Petrides M (2007) Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps. Eur J Neurosci 25:890–899. doi:10.1111/j.1460-9568.2007.05371.x
Iaria G, Fox CJ, Chen JK, Petrides M, Barton JJ (2008) Detection of unexpected events during spatial navigation in humans: bottom-up attentional system and neural mechanisms. Eur J Neurosci 27:1017–1025. doi:10.1111/j.1460-9568.2008.06060.x
Ino T, Inoue Y, Kage M, Hirose S, Kimura T, Fukuyama H (2002) Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus. Neurosci Lett 322:182–186. doi:10.1016/S0304-3940(02)00019-8
Kravitz DJ, Saleem KS, Baker CI, Mishkin M (2011) A new neural framework for visuospatial processing. Nat Rev Neurosci 12:217–230. doi:10.1038/nrn3008
Latini-Corazzini L et al (2010) Route and survey processing of topographical memory during navigation. Psychol Res 74:545–559. doi:10.1007/s00426-010-0276-5
Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O’Keefe J (1998) Knowing where and getting there: a human navigation network. Science 280:921–924
McLaren DG, Ries ML, Xu G, Johnson SC (2012) A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuro Image 61:1277–1286. doi:10.1016/j.neuroimage.2012.03.068
Montello DR (1998) A new framework for understanding the acquisition of spatial knowledge in large-scale environments. In: Egenhofer MJ, Golledge RG (eds) Spatial and temporal reasoning in geographic information systems. Oxford University Press, New York, pp 143–154
Nemmi F, Boccia M, Piccardi L, Galati G, Guariglia C (2013a) Segregation of neural circuits involved in spatial learning in reaching and navigational space. Neuropsychologia 51:1561–1570. doi:10.1016/j.neuropsychologia.2013.03.031
Nemmi F, Piras F, Peran P, Incoccia C, Sabatini U, Guariglia C (2013b) Landmark sequencing and route knowledge: an fMRI study. Cortex 49:507–519. doi:10.1016/j.cortex.2011.11.016
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press; Oxford University Press, Oxford, New York
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 432:127–131. doi:10.1016/j.neulet.2007.12.044
Piccardi L, Bianchini F, Iasevoli L, Giannone G, Guariglia C (2011) Sex differences in a landmark environmental re-orientation task only during the learning phase. Neurosci Lett 503:181–185. doi:10.1016/j.neulet.2011.08.031
Rosenbaum RS, Ziegler M, Winocur G, Grady CL, Moscovitch M (2004) ”I have often walked down this street before”: fMRI studies on the hippocampus and other structures during mental navigation of an old environment. Hippocampus 14:826–835. doi:10.1002/hipo.10218
Rosenbaum RS, Winocur G, Grady CL, Ziegler M, Moscovitch M (2007) Memory for familiar environments learned in the remote past: fMRI studies of healthy people and an amnesic person with extensive bilateral hippocampal lesions. Hippocampus 17:1241–1251. doi:10.1002/hipo.20354
Seemungal BM (2014) The cognitive neurology of the vestibular system. Curr Opin Neurol 27:125–132. doi:10.1097/WCO.0000000000000060
Shelton AL, Gabrieli JD (2002) Neural correlates of encoding space from route and survey perspectives. J Neurosci 22:2711–2717
Shelton AL, Gabrieli JD (2004) Neural correlates of individual differences in spatial learning strategies. Neuropsychology 18:442–449. doi:10.1037/0894-4105.18.3.442
Siegel AW, White SH (1975) The development of spatial representations of large-scale environments. In: Reese HW (ed) Advances in child development and behavior, vol 10. Academic Press, Amsterdam, pp 9–55
Spiers HJ, Maguire EA (2006) Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuro Image 31:1826–1840. doi:10.1016/j.neuroimage.2006.01.037
Taylor HA, Tversky B (1992) Spatial mental models derived from survey and route descriptions. J Mem Lang 31:261–292. doi:10.1016/0749-596x(92)90014-O
Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208
Vann SD, Aggleton JP, Maguire EA (2009) What does the retrosplenial cortex do? Nat Rev Neurosci 10:792–802. doi:10.1038/Nrn2733
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standard
All procedures performed in the study were in accordance with the ethical standards of the institutional and/or national research committee 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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Boccia, M., Guariglia, C., Sabatini, U. et al. Navigating toward a novel environment from a route or survey perspective: neural correlates and context-dependent connectivity. Brain Struct Funct 221, 2005–2021 (2016). https://doi.org/10.1007/s00429-015-1021-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-015-1021-z