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 mapping and temporal sequencing of episodic memory to propose that high-level cognitive processes like mental time travel and conceptual mapping 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.
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References
Aronov D, Tank DW (2014) Engagement of neural circuits underlying 2D spatial navigation in a rodent virtual reality system. Neuron 84:442–456
Aronov D, Nevers R, Tank DW (2017) Mapping of a non-spatial dimension by the hippocampal/entorhinal circuit. Nature 543:719–722
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
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
Bellmund JLS, Gärdenfors P, Moser EI, Doeller CF (2018) Navigating cognition: spatial codes for human thinking. Science 362:eaat6766
Bellmund JLS, Deuker L, Doeller CF (2019) Mapping sequence structure in the human lateral entorhinal cortex. Elife 8:e45333
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
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
Bjerknes TL, Moser EI, Moser MB (2014) Representation of geometric borders in the developing rat. Neuron 82:71–78
Blankeship SL, Redcay E, Dougherty LR, Riggins T (2016) Development of hippocampal functional connectivity during childhood. Hum Brain Mapp 38:182–201
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
Brown AA, Spetch ML, Hurd PL (2007) Growing in circles: rearing environment alters spatial navigation in fish. Psychol Sci 18:569–573
Brunec IK, Moscovitch M, Barense MD (2018) Boundaries shape cognitive representations of spaces and events. Trends Cogn Sci 22:637–650
Burgess N (2014) The 2014 Nobel Prize in physiology or medicine: a spatial model for cognitive neuroscience. Neuron 84:1120–1125
Burgess N, Maguire EA, O’Keefe J (2007) The human hippocampus and spatial and episodic memory. Neuron 35:625–641
Bush D, Barry C, Burgess N (2014) What do grid cells contribute to place cell firing? Trends Neurosci 37:136–145
Buzsáki G, Tingley D (2018) Space and time: the hippocampus as a sequence generator. Trends Cogn Sci 22:853–869
Cheng K (1986) A purely geometric module in the rat’s spatial representation. Cognition 23:149–178
Cheng K (2008) Whither geometry? Troubles of the geometric module. Trends Cogn Sci 12:355–361
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
Chiandetti C, Vallortigara G (2010) Experience and geometry: controlled-rearing studies with chicks. Anim Cogn 2013:463–470
Clayton NS, Griffiths DP, Emery NJ, Dickinson A (2001) Elements of episodic-like memory in animals. Philos Transact 356:1483–1491
Constantinescu AO, O’Reilly JX, Behrens TEJ (2016) Organizing conceptual knowledge in humans with a gridlike code. Science 352:1464–1468
Crystal JD (2010) Episodic-like memory in animals. Behav Brain Res 215:235–243
DeMaster DM, Ghetti S (2012) Developmental differences in hippocampal and cortical contributions to episodic retrieval. Cortex 49:1482–1493
Descartes R (2008) Meditations on first philosophy: with selections from the objections and replies (m. moriarty trans.). Oxford University Press, Oxford
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
Eichenbaum H (2014) Time cells in the hippocampus: a new dimension for mapping memories. Nature Rev Neurosci 15:732–744
Eichenbaum H (2017) The role of the hippocampus in navigation is memory. J Neurophysiol 117:1785–1796
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
Ekstrom AD, Ranganath C (2018) Space, time, and episodic memory: the hippocampus is all over the cognitive map. Hippocampus 28:680–687
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
El Haj M, Kapogiannis D (2016) Time distortions in Alzheimer’s disease: a systematic review and theoretical integration. Npj Aging Mech Dis 2:16016
Epstein RA, Patai EZ, Julian JB, Spiers HJ (2017) The cognitive map in humans: spatial navigation and beyond. Nat Neurosci 20:1504–1513
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
Ferrara K, Landau B (2015) Geometric and featural systems, separable and combined: evidence from reorientation in people with Williams syndrome. Cognition 144:123–133
Ferrara K, Park S (2016) Neural representation of scene boundaries. Neuropsychologia 2016(89):180–190
Ferrara K, Landau B, Park S (2019) Impaired behavioral and neural representation of scenes in Williams syndrome. Cortex 121:264–276
Foster D (2017) Replay comes of age. Annu Rev Neurosci 40:581–602
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
Fyhn M, Hafting T, Treves A, Moser MB, Moser EI (2007) Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446:190–194
Gallistel CR (1990) The organization of learning. MIT Press, Cambridge
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
Georgopolous A, Lurito JT, Petrides M, Schwartz AB, Massey JT (1989) Mental rotation of the neuronal population vector. Science 243:234–236
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 developing role of transparent surfaces in children’s spatial representation. Cogn Psychol 105:39–52
Giocomo LM (2015) Environmental boundaries as a mechanism for correcting and anchoring spatial maps. J Physiol 594:6501–6511
Gouteux S, Spelke ES (2001) Children’s use of geometry and landmarks to reorient in an open space. Cognition 81:119–148
Grieves RM, Duvelle E, Wood ER, Dudchenko PA (2017) Field repetition and local mapping in the hippocampus and the medial entorhinal cortex. J Neurophysiol 118:2378–2388
Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806
Hardcastle K, Ganguli S, Giocomo LM (2015) Environmental boundaries as an error correction mechanism for grid cells. Neuron 86:827–839
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
Hermer L, Spelke ES (1994) A geometric process for spatial orientation in young children. Nature 370:57–59
Hermer L, Spelke E (2016) Modularity and development: the case of spatial reorientation. Cognition 61:195–232
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
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
Horner AJ, Bisby JA, Wang A, Bogus K, Burgess N (2016a) The role of spatial boundaries in shaping long-term event representations. Cognition 154:151–164
Horner AJ, Bisby JA, Zotow E, Bush D, Burgess N (2016b) Grid-like processing of imagined navigation. Curr Biol 26:842–847
Huttenlocher J, Lourenco SF (2007) Coding location in enclosed spaces: is geometry the principle? Dev Sci 10:741–746
Jacobs J, Sav L (2016) Spatial cognition: grid cells support imagined navigation. Curr Biol 26:R277–R279
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
Julian JB, Kamps FS, Epstein RA, Dilks DD (2019) Dissociable spatial memory systems revealed by typical and atypical human development. Dev Sci 22:e12737
Keinath AT, Julian JB, Epstein RA, Muzzio IA (2017) Environmental geometry aligns the hippocampal map during spatial reorientation. Curr Biol 27:309–317
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
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
Kosslyn SM, Pick HL, Fariello GR (1974) Cognitive maps in children and men. Child Dev 45:707–716
Krupic J, Bauza M, Burton S, Barry C, O’Keefe J (2015) Grid cell symmetry is shaped by environmental geometry. Nature 518:232–235
Lakusta L, Dessalegn B, Landau B (2010) Impaired geometric reorientation caused by genetic defect. Proc Natl Acad Sci USA 107:2813–2817
Learmonth AE, Nadel L, Newcombe NS (2003) Children’s use of landmarks: implications for modularity theory. Psychol Sci 13:337–341
Lee SA (2017) The boundary-based view of spatial cognition: a synthesis. Curr Opin Behav Sci 16:58–65
Lee SA, Spelke ES (2008) Children’s use of geometry for reorientation. Dev Sci 11:743–749
Lee SA, Spelke ES (2010a) A modular geometric mechanism for reorientation in children. Cogn Psychol 61:152–176
Lee SA, Spelke ES (2010b) Two systems of spatial representation underlying navigation. Exp Brain Res 206:179–188
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
Lee SA, Shusterman A, Spelke ES (2006) Reorientation and landmark- guided search by young evidence for two systems. Psychol Sci 17:577–582
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
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
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
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
Lee SA, Ferrari A, Vallortigara G, Sovrano VA (2015a) Boundary primacy in spatial mapping: evidence from zebrafish (Danio rerio). Behav Processes 119:116–122
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
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
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
Lee SM, Jin 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
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
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
Lourenco SF, Huttenlocher J (2006) How do young children determine location? Evidence from disorientation tasks. Cognition 100:511–529
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
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
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
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
Montchal ME, Reagh ZM, Yassa MA (2019) Precise temporal memories are supported by the lateral entorhinal cortex in humans. Nat Neurosci 22:284–288
Mullally SL, Maguire EA (2013) Memory, imagination, and predicting the future: a common brain mechanism? Neuroscientist 20:220–234
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
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
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
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
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, Oxford
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
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
Payne HL, Lynch G, Aronov D (2021) Neural representations of space in the hippocampus of a food-caching bird. Science 373:343–348
Peer M, Epstein RA (2021) The human brain uses spatial schemas to represent segmented environments. Curr Biol 31:4677–4688
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
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
Rah YJ, Kim J, Lee SA (2022) Effects of spatial boundaries on episodic memory development. Child Dev 93:1574–1583
Ratliff KR, Newcombe NS (2008) Is language necessary for human spatial reorientation? Reconsidering evidence from dual task paradigms. Cogn Psychol 56:142–163
Robin J (2018) Spatial scaffold effects in event memory and imagination. Wiley Interdiscip Rev 9:e1462
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
Savelli F, Yoganarasimha D, Knierim JJ (2008) Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18:1270–1282
Schlesiger MI, Boublil BL, Hales JB, Leutgeb JK, Leutgeb S (2018) Hippocampal global remapping can occur without input from the medial entorhinal cortex. Cell Rep 22:3152–3159
Shepard R, Meltzer J (1971) Mental rotation of three-dimensional objects. Science 171:701–703
Shettleworth S (2001) Animal cognition and animal behaviour. Anim Behav 61:277–286
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
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
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
Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322:1865–1868
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
Spelke ES (1994) Innate knowledge: six suggestions. Cognition 50:431–445
Spelke ES, Lee SA (2012) Core system of geometry in animal minds. Philos Trans R Soc B 367:2784–2793
Spelke E, Lee SA, Izard V (2010) Beyond core knowledge: natural geometry. Cogn Sci 34:863–884
Spiers HJ, Hayman RMA, Jovalekic A, Marozzi E, Jeffrey KJ (2015) Place field repetition and purely local remapping in a multicompartment environment. Cereb Cortex 25:10–25 (More Doorways)
Stensola T, Stensola H, Moser M-B, Moser EI (2015) Shearing-induced asymmetry in entorhinal grid cells. Nature 518:207–212
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
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
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
Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208
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
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
Udwin O, Yule WA (1991) A cognitive and behavioral phenotype in Williams syndrome. J Clin Exp Neuropsychol 13:232–244
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
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
Vargas JP, Petruso EJ, Bingman VP (2004) Hippocampal formation is required for geometric navigation in pigeons. Eur J Neurosci 20(7):1937–1944
Vicari S, Brizzolara D, Carlesimo GA, Pezzini G, Volterra V (1996) Memory abilities in children with Williams syndrome. Cortex 32:503–514
Watson JB (1913) Psychology as the behaviorist views it. Psychol Rev 20:158–178
Whittington JCR et al (2020) The Tolman-Eichenbaum machine: unifying space and relational memory through generalization in the hippocampal formation. Cell 183:1249–1263
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
Xu Y, Regier T, Newcombe NS (2017) An adaptive cue combination model of spatial reorientation. Cognition 163:56–66
Yartsev MM, Ulanovsky N (2013) Representation of three-dimensional space in the hippocampus of flying bats. Science 340:367–372
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This research was supported by government-funded grants to SAL from IITP (Grant No. 2019-0-01371-003) and NRF (Grant No. 2021M3E5D2A01023891).
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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
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DOI: https://doi.org/10.1007/s10071-022-01726-1