SpringerLink
Log in

Navigational roots of spatial and temporal memory structure

  • Review
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Our minds are constantly in transit, from the present to the past to the future, across places we have and have not directly experienced. Nevertheless, memories of our mental time travel are not organized continuously and are adaptively chunked into contexts and episodes. In this paper, I will review evidence that suggests that spatial boundary representations play a critical role in providing structure to both our spatial and temporal memories. I will illustrate the intimate connection between hippocampal spatial map** and temporal sequencing of episodic memory to propose that high-level cognitive processes like mental time travel and conceptual map** are rooted in basic navigational mechanisms that we humans and nonhuman animals share. Our neuroscientific understanding of hippocampal function across species may provide new insight into the origins of even the most uniquely human cognitive abilities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data availability

Data availability statement: Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

References

  • Aronov D, Tank DW (2014) Engagement of neural circuits underlying 2D spatial navigation in a rodent virtual reality system. Neuron 84:442–456

    Article  CAS  Google Scholar 

  • Aronov D, Nevers R, Tank DW (2017) Map** of a non-spatial dimension by the hippocampal/entorhinal circuit. Nature 543:719–722

    Article  CAS  Google Scholar 

  • Baratti G, Potrich D, Lee SA, Morandi-Raikova A, Sovrano VA (2022) The geometric world of fishes: a synthesis on spatial reorientation in teleosts. Animals 12:881

    Article  Google Scholar 

  • Bellassen V, Iglói K, de Souza LC, Dubois B, Rondi-Reig L (2011) Temporal order memory assessed during spatiotemporal navigation cs a behavioral cognitive marker for differential Alzheimer’s disease diagnosis. J Neurosci 32:1942–1952

    Article  Google Scholar 

  • Bellmund JLS, Gärdenfors P, Moser EI, Doeller CF (2018) Navigating cognition: spatial codes for human thinking. Science 362:eaat6766

    Article  Google Scholar 

  • Bellmund JLS, Deuker L, Doeller CF (2019) Map** sequence structure in the human lateral entorhinal cortex. Elife 8:e45333

    Article  Google Scholar 

  • Bird CM, Capponi C, King JA, Doeller CF, Burgess N (2010a) Establishing the boundaries: the hippocampal contribution to imagining scenes. J Neurosci 30:11688–11695

    Article  CAS  Google Scholar 

  • Bird CM, Chan D, Hartley T, Pijnenburg YA, Rossor MN, Burgess N (2010b) Topographical short-term memory differentiates Alzheimer’s disease from frontotemporal lobar degeneration. Hippocampus 20:1154–1169

    Article  Google Scholar 

  • Bjerknes TL, Moser EI, Moser MB (2014) Representation of geometric borders in the develo** rat. Neuron 82:71–78

    Article  CAS  Google Scholar 

  • Blankeship SL, Redcay E, Dougherty LR, Riggins T (2016) Development of hippocampal functional connectivity during childhood. Hum Brain Mapp 38:182–201

    Article  Google Scholar 

  • Brandon MP, Koenig J, Leutgeb JK, Leutgeb S (2014) New and distinct hippocampal place codes are generated in a new environment during septal inactivation. Neuron 82:789–796

    Article  CAS  Google Scholar 

  • Brown AA, Spetch ML, Hurd PL (2007) Growing in circles: rearing environment alters spatial navigation in fish. Psychol Sci 18:569–573

    Article  Google Scholar 

  • Brunec IK, Moscovitch M, Barense MD (2018) Boundaries shape cognitive representations of spaces and events. Trends Cogn Sci 22:637–650

    Article  Google Scholar 

  • Burgess N (2014) The 2014 Nobel Prize in physiology or medicine: a spatial model for cognitive neuroscience. Neuron 84:1120–1125

    Article  CAS  Google Scholar 

  • Burgess N, Maguire EA, O’Keefe J (2007) The human hippocampus and spatial and episodic memory. Neuron 35:625–641

    Article  Google Scholar 

  • Bush D, Barry C, Burgess N (2014) What do grid cells contribute to place cell firing? Trends Neurosci 37:136–145

    Article  CAS  Google Scholar 

  • Buzsáki G, Tingley D (2018) Space and time: the hippocampus as a sequence generator. Trends Cogn Sci 22:853–869

    Article  Google Scholar 

  • Cheng K (1986) A purely geometric module in the rat’s spatial representation. Cognition 23:149–178

    Article  CAS  Google Scholar 

  • Cheng K (2008) Whither geometry? Troubles of the geometric module. Trends Cogn Sci 12:355–361

    Article  Google Scholar 

  • Cheng K, Huttenlocher J, Newcombe NS (2013) 25 years of research on the use of geometry in spatial reorientation: a current theoretical perspective. Psychon Bull Rev 20:1033–1054

    Article  Google Scholar 

  • Chiandetti C, Vallortigara G (2010) Experience and geometry: controlled-rearing studies with chicks. Anim Cogn 2013:463–470

    Article  Google Scholar 

  • Clayton NS, Griffiths DP, Emery NJ, Dickinson A (2001) Elements of episodic-like memory in animals. Philos Transact 356:1483–1491

    Article  CAS  Google Scholar 

  • Constantinescu AO, O’Reilly JX, Behrens TEJ (2016) Organizing conceptual knowledge in humans with a gridlike code. Science 352:1464–1468

    Article  CAS  Google Scholar 

  • Crystal JD (2010) Episodic-like memory in animals. Behav Brain Res 215:235–243

    Article  Google Scholar 

  • DeMaster DM, Ghetti S (2012) Developmental differences in hippocampal and cortical contributions to episodic retrieval. Cortex 49:1482–1493

    Article  Google Scholar 

  • Descartes R (2008) Meditations on first philosophy: with selections from the objections and replies (m. moriarty trans.). Oxford University Press, Oxford

    Google Scholar 

  • Doeller CF, King JA, Burgess N (2008) Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc Natl Acad Sci 105:5915–5920

    Article  CAS  Google Scholar 

  • Eichenbaum H (2014) Time cells in the hippocampus: a new dimension for map** memories. Nature Rev Neurosci 15:732–744

    Article  CAS  Google Scholar 

  • Eichenbaum H (2017) The role of the hippocampus in navigation is memory. J Neurophysiol 117:1785–1796

    Article  Google Scholar 

  • Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H (1999) The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23:209–226

    Article  CAS  Google Scholar 

  • Ekstrom AD, Ranganath C (2018) Space, time, and episodic memory: the hippocampus is all over the cognitive map. Hippocampus 28:680–687

    Article  Google Scholar 

  • Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I (2003) Cellular networks underlying human spatial navigation. Nature 425:184–187

    Article  CAS  Google Scholar 

  • El Haj M, Kapogiannis D (2016) Time distortions in Alzheimer’s disease: a systematic review and theoretical integration. Npj Aging Mech Dis 2:16016

    Article  Google Scholar 

  • Epstein RA, Patai EZ, Julian JB, Spiers HJ (2017) The cognitive map in humans: spatial navigation and beyond. Nat Neurosci 20:1504–1513

    Article  CAS  Google Scholar 

  • Fellini L, Schachner M, Morellini F (2006) Adult but not aged C57BL/6 male mice are capable of using geometry for orientation. Learn Mem 13:472–481

    Article  Google Scholar 

  • Ferrara K, Landau B (2015) Geometric and featural systems, separable and combined: evidence from reorientation in people with Williams syndrome. Cognition 144:123–133

    Article  Google Scholar 

  • Ferrara K, Park S (2016) Neural representation of scene boundaries. Neuropsychologia 2016(89):180–190

    Article  Google Scholar 

  • Ferrara K, Landau B, Park S (2019) Impaired behavioral and neural representation of scenes in Williams syndrome. Cortex 121:264–276

    Article  Google Scholar 

  • Foster D (2017) Replay comes of age. Annu Rev Neurosci 40:581–602

    Article  CAS  Google Scholar 

  • Fotowat H, Lee C, Jun JJ, Maler L (2019) Neural activity in a hippocampus-like region of the teleost pallium is associated with active sensing and navigation. Elife 8:e44119

    Article  CAS  Google Scholar 

  • Fyhn M, Hafting T, Treves A, Moser MB, Moser EI (2007) Hippocampal remap** and grid realignment in entorhinal cortex. Nature 446:190–194

    Article  CAS  Google Scholar 

  • Gallistel CR (1990) The organization of learning. MIT Press, Cambridge

    Google Scholar 

  • Garrad-Cole F, Lew AR, Bremner JG, Whitaker CJ (2001) Use of configurational geometry for spatial orientation in human infants (Homo sapiens). J Comp Psychol 115(3):317–320

    Article  CAS  Google Scholar 

  • Georgopolous A, Lurito JT, Petrides M, Schwartz AB, Massey JT (1989) Mental rotation of the neuronal population vector. Science 243:234–236

    Article  Google Scholar 

  • Gianni E, Lee SA (2018) Defining spatial boundaries: a developmental study. In: Fogliaroni P, Ballatore A & Clementini E (eds) Proceedings of Workshops and Posters at the 13th International Conference on Spatial Information Theory. Lecture Notes in Geoinformation and Cartography. Springer

  • Gianni E, de Zorzi L, Lee SA (2018) The develo** role of transparent surfaces in children’s spatial representation. Cogn Psychol 105:39–52

    Article  Google Scholar 

  • Giocomo LM (2015) Environmental boundaries as a mechanism for correcting and anchoring spatial maps. J Physiol 594:6501–6511

    Article  Google Scholar 

  • Gouteux S, Spelke ES (2001) Children’s use of geometry and landmarks to reorient in an open space. Cognition 81:119–148

    Article  CAS  Google Scholar 

  • Grieves RM, Duvelle E, Wood ER, Dudchenko PA (2017) Field repetition and local map** in the hippocampus and the medial entorhinal cortex. J Neurophysiol 118:2378–2388

    Article  Google Scholar 

  • Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806

    Article  CAS  Google Scholar 

  • Hardcastle K, Ganguli S, Giocomo LM (2015) Environmental boundaries as an error correction mechanism for grid cells. Neuron 86:827–839

    Article  CAS  Google Scholar 

  • Harland B, Grieves RM, Bett D, Stentiford R, Wood ER, Dudchenko PA (2017) Lesions of the head direction cell system increase hippocampal place field repetition. Curr Biol 27:2706–2712

    Article  CAS  Google Scholar 

  • Hermer L, Spelke ES (1994) A geometric process for spatial orientation in young children. Nature 370:57–59

    Article  CAS  Google Scholar 

  • Hermer L, Spelke E (2016) Modularity and development: the case of spatial reorientation. Cognition 61:195–232

    Article  CAS  Google Scholar 

  • Hermer-Vazquez L, Spelke ES, Katsnelson A (1999) Sources of flexibility in human cognition: dual-task studies of space and language. Cogn Psychol 39:3–36

    Article  CAS  Google Scholar 

  • Hori E, NishioY KK, Umeno K, Tabuchi E, Sasaki K, Endo S, Ono T, Nishijo T (2005) Place-related neural responses in the monkey hippocampal formation in a virtual space. Hippocampus 15:991–996

    Article  Google Scholar 

  • Horner AJ, Bisby JA, Wang A, Bogus K, Burgess N (2016a) The role of spatial boundaries in sha** long-term event representations. Cognition 154:151–164

    Article  Google Scholar 

  • Horner AJ, Bisby JA, Zotow E, Bush D, Burgess N (2016b) Grid-like processing of imagined navigation. Curr Biol 26:842–847

    Article  CAS  Google Scholar 

  • Huttenlocher J, Lourenco SF (2007) Coding location in enclosed spaces: is geometry the principle? Dev Sci 10:741–746

    Article  Google Scholar 

  • Jacobs J, Sav L (2016) Spatial cognition: grid cells support imagined navigation. Curr Biol 26:R277–R279

    Article  CAS  Google Scholar 

  • Julian JB, Ryan J, Hamilton RH, Epstein RA (2016) The occipital place area is causally involved in representing environmental boundaries during navigation. Curr Biol 26:1104–1109

    Article  CAS  Google Scholar 

  • Julian JB, Kamps FS, Epstein RA, Dilks DD (2019) Dissociable spatial memory systems revealed by typical and atypical human development. Dev Sci 22:e12737

    Article  Google Scholar 

  • Keinath AT, Julian JB, Epstein RA, Muzzio IA (2017) Environmental geometry aligns the hippocampal map during spatial reorientation. Curr Biol 27:309–317

    Article  CAS  Google Scholar 

  • Kelly DM, Spetch ML, Heth CD (1998) Pigeons’ (Columba livia) encoding of geometric and featural properties of a spatial environment. J Comp Psychol 112:259–269

    Article  Google Scholar 

  • Knight R, Hayman R, Ginzberg LL, Jeffery K (2011) Geometric cues influence head direction cells only weakly in nondisoriented rats. J Neurosci 31:15681–15692

    Article  CAS  Google Scholar 

  • Kosslyn SM, Pick HL, Fariello GR (1974) Cognitive maps in children and men. Child Dev 45:707–716

    Article  CAS  Google Scholar 

  • Krupic J, Bauza M, Burton S, Barry C, O’Keefe J (2015) Grid cell symmetry is shaped by environmental geometry. Nature 518:232–235

    Article  CAS  Google Scholar 

  • Lakusta L, Dessalegn B, Landau B (2010) Impaired geometric reorientation caused by genetic defect. Proc Natl Acad Sci USA 107:2813–2817

    Article  CAS  Google Scholar 

  • Learmonth AE, Nadel L, Newcombe NS (2003) Children’s use of landmarks: implications for modularity theory. Psychol Sci 13:337–341

    Article  Google Scholar 

  • Lee SA (2017) The boundary-based view of spatial cognition: a synthesis. Curr Opin Behav Sci 16:58–65

    Article  Google Scholar 

  • Lee SA, Spelke ES (2008) Children’s use of geometry for reorientation. Dev Sci 11:743–749

    Article  Google Scholar 

  • Lee SA, Spelke ES (2010a) A modular geometric mechanism for reorientation in children. Cogn Psychol 61:152–176

    Article  Google Scholar 

  • Lee SA, Spelke ES (2010b) Two systems of spatial representation underlying navigation. Exp Brain Res 206:179–188

    Article  Google Scholar 

  • Lee SA, Spelke ES (2011) Young children reorient by computing layout geometry, not by matching images of the environment. Psychon Bull Rev 18:192–198

    Article  Google Scholar 

  • Lee SA, Shusterman A, Spelke ES (2006) Reorientation and landmark- guided search by young evidence for two systems. Psychol Sci 17:577–582

    Article  Google Scholar 

  • Lee SA, Sovrano VA, Spelke ES (2012a) Navigation as a source of geometric knowledge: Young children’s use of length, angle, distance, and direction in a reorientation task. Cognition 123:144–161

    Article  Google Scholar 

  • Lee SA, Spelke ES, Vallortigara G (2012b) Chicks, like children, spontaneously reorient by three-dimensional environmental geometry, not by image matching. Biol Lett 8:492–494

    Article  Google Scholar 

  • Lee SA, Winkler-Rhoades N, Spelke ES (2012c) Spontaneous reorientation is guided by perceived surface distance, not by image matching or comparison. PLoS ONE 7:e51373

    Article  CAS  Google Scholar 

  • Lee SA, Vallortigara G, Fiore M, Spelke ES, Sovrano VA (2013) Navigation by environmental geometry: the use of zebrafish as a model. J Exp Biol 216:3693–3699

    Google Scholar 

  • Lee SA, Ferrari A, Vallortigara G, Sovrano VA (2015a) Boundary primacy in spatial map**: evidence from zebrafish (Danio rerio). Behav Processes 119:116–122

    Article  Google Scholar 

  • Lee SA, Tucci V, Sovrano VA, Vallortigara G (2015b) Working memory and reference memory tests of spatial navigation in mice (Mus musculus). J Comp Psychol 192:189–197

    Article  Google Scholar 

  • Lee JK, Wendelken C, Bunge SA, Ghetti S (2015c) A time and place for everything: Developmental differences in the building blocks of episodic memory. Child Dev 87:194–210

    Article  Google Scholar 

  • Lee SA, Miller JF, Watrous AJ, Sperling MR, Sharan A, Worrell GA, Berry BM, Aronson JP, Davis KA, Gross RE, Lega B, Sheth S, Das SR, Stein JM, Gorniak R, Rizzuto DS, Jacobs J (2018) Electrophysiological signatures of spatial boundaries in the human subiculum. J Neurosci 38(13):3216–3217

    Article  Google Scholar 

  • Lee SM, ** SW, Park SB, Park EH, Lee CH, Lee HW, Lim HY, Yoo SW, Ahn JR, Shin J, Lee SA, Lee I (2021) Goal-directed interaction of stimulus and task demand in the parahippocampal region. Hippocampus 3:717–736

    Article  Google Scholar 

  • Leonard K, Vasylkiv V, Kelly DM (2020) Reorientation by features and geometry: effects of healthy and degenerative age-related cognitive decline. Learn Behav 48:124–134

    Article  Google Scholar 

  • Lever C, Burton S, Jeewajee A, O’Keefe J, Burgess N (2009) Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci 29:9771–9777

    Article  CAS  Google Scholar 

  • Lourenco SF, Huttenlocher J (2006) How do young children determine location? Evidence from disorientation tasks. Cognition 100:511–529

    Article  Google Scholar 

  • Macdonald CJ, Carrow S, Place R, Eichenbaum H (2013) Distinct hippocampal time cell sequences represent odor memories in immobilized rats. J Neuroscience 33:14607–14616

    Article  CAS  Google Scholar 

  • Mastrogiuseppe M, Bertelsen N, Bedeschi MF, Lee SA (2019) The spatiotemporal organization of episodic memory and its disruption in a neurodevelopmental disorder. Sci Rep 9:18447

    Article  CAS  Google Scholar 

  • Mayer U, Pecchia T, Bingman VP et al (2016) Hippocampus and medial striatum dissociation during goal navigation by geometry or features in the domestic chick: an immediate early gene study. Hippocampus 26:27–40

    Article  CAS  Google Scholar 

  • Mayer U, Bhushan R, Vallortigara G, Lee SA (2018) Representation of environmental shape in the hippocampal formation of the domestic chick (Gallus gallus). Brain Struct Funct 223:941–953

    Article  CAS  Google Scholar 

  • Montchal ME, Reagh ZM, Yassa MA (2019) Precise temporal memories are supported by the lateral entorhinal cortex in humans. Nat Neurosci 22:284–288

    Article  CAS  Google Scholar 

  • Mullally SL, Maguire EA (2013) Memory, imagination, and predicting the future: a common brain mechanism? Neuroscientist 20:220–234

    Article  Google Scholar 

  • Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7:1951–1968

    Article  CAS  Google Scholar 

  • Negen J, Sandri A, Lee SA, Nardini M (2020) Boundaries in spatial cognition: looking like a boundary is more important than being a boundary. J Exp Psychol Learn Mem Cogn 46:1007–1021

    Article  Google Scholar 

  • Newcombe NS, Ratliff KR (2007) Explaining the development of spatial reorientation: modularity-plus-language versus the emergence of adaptive combination. In The Emerging Spatial Mind, Plumer J, Spencer J (eds) Oxford University Press, Oxford

  • O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428

    Article  Google Scholar 

  • O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175

    Article  Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, Oxford

    Google Scholar 

  • Olson IR and Newcombe NS (2014) Binding together the elements of episodes: relational memory and the developmental trajectory of the hippocampus. The Wiley Handbook and the Development of Children’s Memory, Volume I/II. Patricia J. Bauer and Robyn Fivush.

  • Park JH, Lee SA (2021) The fragility of temporal memory in Alzheimer’s disease. J Alzheimer’s Dis 79:1631–1646

    Article  CAS  Google Scholar 

  • Park S, Brady TF, Greene MR, Oliva A (2011) Disentangling scene content from spatial boundary: complementary roles for the parahippocampal place area and lateral occipital complex in representing real-world scenes. J Neurosci 31:1333–1340

    Article  CAS  Google Scholar 

  • Payne HL, Lynch G, Aronov D (2021) Neural representations of space in the hippocampus of a food-caching bird. Science 373:343–348

    Article  CAS  Google Scholar 

  • Peer M, Epstein RA (2021) The human brain uses spatial schemas to represent segmented environments. Curr Biol 31:4677–4688

    Article  CAS  Google Scholar 

  • Poulter S, Lee SA, Dachtler J, Wills TJ, Lever C (2021) Vector trace cells in the subiculum of the hippocampal formation. Nat Neurosci 24:266–275

    Article  CAS  Google Scholar 

  • Radvansky GA, Copeland DE (2006) Walking through door—ways causes forgetting: situation models and experienced space. Mem Cognit 34:1150–1156. https://doi.org/10.3758/bf03193261

    Article  Google Scholar 

  • Rah YJ, Kim J, Lee SA (2022) Effects of spatial boundaries on episodic memory development. Child Dev 93:1574–1583

    Article  Google Scholar 

  • Ratliff KR, Newcombe NS (2008) Is language necessary for human spatial reorientation? Reconsidering evidence from dual task paradigms. Cogn Psychol 56:142–163

    Article  Google Scholar 

  • Robin J (2018) Spatial scaffold effects in event memory and imagination. Wiley Interdiscip Rev 9:e1462

    Google Scholar 

  • Rodriguez F, López C, Vargas JP, Broglio C, Gómez Y, Salas C (2002) Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish. Brain Res Bull 3–4:499–503

    Article  Google Scholar 

  • Savelli F, Yoganarasimha D, Knierim JJ (2008) Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18:1270–1282

    Article  Google Scholar 

  • Schlesiger MI, Boublil BL, Hales JB, Leutgeb JK, Leutgeb S (2018) Hippocampal global remap** can occur without input from the medial entorhinal cortex. Cell Rep 22:3152–3159

    Article  CAS  Google Scholar 

  • Shepard R, Meltzer J (1971) Mental rotation of three-dimensional objects. Science 171:701–703

    Article  CAS  Google Scholar 

  • Shettleworth S (2001) Animal cognition and animal behaviour. Anim Behav 61:277–286

    Article  Google Scholar 

  • Sheynikhovich D, Chavarriaga R, Strösslin T, Arleo A, Gerstner W (2009) Is there a geometric module for spatial orientation? Insights from a rodent navigation model. Psychol Rev 116:540–566

    Article  Google Scholar 

  • Shine JP, Valdés-Herrera JP, Tempelmann C, Wolbers T (2019) Evidence for allocentric boundary and goal direction information in the human entorhinal cortex and subiculum. Nat Commun 10:4004

    Article  CAS  Google Scholar 

  • Siegel JJ, Nitz D, Bingman VP (2005) Spatial specificity of single-units in the hippocampal formation of freely moving homing pigeons. Hippocampus 15:26–40

    Article  Google Scholar 

  • Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322:1865–1868

    Article  CAS  Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2003) Modularity as a fish (Xenotoca eiseni) views it: conjoining geometric and nongeometric information for spatial reorientation. J Exp Psychol Anim Behav Process 29:199–210

    Article  Google Scholar 

  • Spelke ES (1994) Innate knowledge: six suggestions. Cognition 50:431–445

    Article  CAS  Google Scholar 

  • Spelke ES, Lee SA (2012) Core system of geometry in animal minds. Philos Trans R Soc B 367:2784–2793

    Article  Google Scholar 

  • Spelke E, Lee SA, Izard V (2010) Beyond core knowledge: natural geometry. Cogn Sci 34:863–884

    Article  Google Scholar 

  • Spiers HJ, Hayman RMA, Jovalekic A, Marozzi E, Jeffrey KJ (2015) Place field repetition and purely local remap** in a multicompartment environment. Cereb Cortex 25:10–25 (More Doorways)

    Article  Google Scholar 

  • Stensola T, Stensola H, Moser M-B, Moser EI (2015) Shearing-induced asymmetry in entorhinal grid cells. Nature 518:207–212

    Article  CAS  Google Scholar 

  • Stewart S, Jeewajee A, Wills TJ, Burgess N, Lever C, Lever C (2013) Boundary coding in the rat subiculum. Philos Trans R Soc B 369:20120514

    Article  Google Scholar 

  • Taube JS, Muller RU, Ranck JB (1990a) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10:420–435

    Article  CAS  Google Scholar 

  • Taube JS, Muller RU, Ranck JB (1990b) Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10:436–447

    Article  CAS  Google Scholar 

  • Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208

    Article  CAS  Google Scholar 

  • Tsao A, Sugar J, Lu L, Wang C, Knierim JJ, Moser MB, Moser EI (2018) Integrating time from experience in the lateral entorhinal cortex. Nature 561:57–62

    Article  CAS  Google Scholar 

  • Twyman AD, Newcombe NS, Gould TJ (2009) Of mice (Mus musculus) and toddlers (Homo sapiens): evidence of species-general spatial reorientation. J Comp Psychol 123:342–345

    Article  Google Scholar 

  • Udwin O, Yule WA (1991) A cognitive and behavioral phenotype in Williams syndrome. J Clin Exp Neuropsychol 13:232–244

    Article  CAS  Google Scholar 

  • Vallortigara G (2009) Animals as natural geometers. In: Tommasi L, Peterson MA, Nadel L (eds) Cognitive biology: evolutionary and developmental perspectives on mind, brain, and behavior. MIT Press, Cambridge

    Google Scholar 

  • Vallortigara G, Zanforlin M, Pasti G (1990) Geometric modules in animals’ spatial representations: a test with chicks (Gallus gallus domesticus). J Comp Psychol 104:248–254

    Article  CAS  Google Scholar 

  • Vargas JP, Petruso EJ, Bingman VP (2004) Hippocampal formation is required for geometric navigation in pigeons. Eur J Neurosci 20(7):1937–1944

    Article  Google Scholar 

  • Vicari S, Brizzolara D, Carlesimo GA, Pezzini G, Volterra V (1996) Memory abilities in children with Williams syndrome. Cortex 32:503–514

    Article  CAS  Google Scholar 

  • Watson JB (1913) Psychology as the behaviorist views it. Psychol Rev 20:158–178

    Article  Google Scholar 

  • Whittington JCR et al (2020) The Tolman-Eichenbaum machine: unifying space and relational memory through generalization in the hippocampal formation. Cell 183:1249–1263

    Article  CAS  Google Scholar 

  • Wills TJ, Muessig L, Cacucci F (2014) Development of spatial behaviour and the hippocampal neural representation of space. Phil Trans Roy Soc B 369:20130409

    Article  Google Scholar 

  • Xu Y, Regier T, Newcombe NS (2017) An adaptive cue combination model of spatial reorientation. Cognition 163:56–66

    Article  Google Scholar 

  • Yartsev MM, Ulanovsky N (2013) Representation of three-dimensional space in the hippocampus of flying bats. Science 340:367–372

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by government-funded grants to SAL from IITP (Grant No. 2019-0-01371-003) and NRF (Grant No. 2021M3E5D2A01023891).

Author information

Authors and Affiliations

  1. Department of Brain and Cognitive Sciences, Seoul National University, Gwanak-Ro 1, Gwanak-Gu, Seoul, 08826, Korea

    Sang Ah Lee

Authors
  1. Sang Ah Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sang Ah Lee.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, S.A. Navigational roots of spatial and temporal memory structure. Anim Cogn 26, 87–95 (2023). https://doi.org/10.1007/s10071-022-01726-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-022-01726-1

Keywords

Search

Navigation