Skip to main content
SpringerLink
Log in
Book cover

Space,Time and Memory in the Hippocampal Formation pp 373–407Cite as

How Does the Brain Solve the Computational Problems of Spatial Navigation?

  • Chapter
  • First Online:

Abstract

Flexible navigation in the real world involves the ability to maintain an ongoing estimate of one’s location in the environment, to use landmarks to help navigate, and to construct shortcuts and paths between locations. In mammals, these functions are believed to be performed by a circuit that includes the hippocampus and associated cortical areas. The physiological characterization of the neural substrates for navigation has progressed rapidly in the last four decades, together with plausible mechanistic models for the generation of such activity. However, questions about how the various components of the circuit interact to perform the overall computations that account for the navigational ability of mammals remain largely unsolved. We review physiological and anatomical data as well as models of hippocampal map building and self-localization to establish what is understood about the brain’s navigational circuits from a computational perspective. We discuss major areas where our understanding is incomplete.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aimone JB, Deng W, Gage FH (2011) Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70:589–596

    CAS  PubMed Central  PubMed  Google Scholar 

  • Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3–22

    PubMed Central  PubMed  Google Scholar 

  • Amit D (1994) The Hebbian paradigm reintegrated: local reverberations as internal representations. Behav Brain Res 18:617–626

    Google Scholar 

  • Anderson P, Morris RG, Amaral D, Bliss T, O’Keefe J (eds) (2007) The hippocampus book. Oxford University Press, Oxford

    Google Scholar 

  • Arleo A, Gerstner W (2000) Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity. Biol Cybern 83:287–299

    CAS  PubMed  Google Scholar 

  • Balakrishnan K, Bousquet O, Honavar V (1999) Spatial learning and localization in rodents: a computational model of the hippocampus and its implications for mobile robots. Adapt Behav 7:173–216

    Google Scholar 

  • Barnes CA, McNaughton BL, Mizumori SJ, Leonard BW, Lin LH (1990) Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83:287–300

    CAS  PubMed  Google Scholar 

  • Barry C, Lever C, Hayman R, Hartley T, Burton S, O’Keefe J, Jeffery K, Burgess N (2006) The boundary vector cell model of place cell firing and spatial memory. Rev Neurosci 17:71–97

    PubMed Central  PubMed  Google Scholar 

  • Barry C, Hayman R, Burgess N, Jeffery KJ (2007) Experience-dependent rescaling of entorhinal grids. Nat Neurosci 10:682–684

    CAS  PubMed  Google Scholar 

  • Benhamou S, Bovet P, Poucet B (1995) A model of place navigation in mammals. J Theor Biol 173:163–178

    Google Scholar 

  • Ben-Yishai R, Bar-Or RL, Sompolinsky H (1995) Theory of orientation tuning in visual cortex. Proc Natl Acad Sci USA 92:3844–3848

    CAS  PubMed Central  PubMed  Google Scholar 

  • Blair HT, Gupta K, Zhang K (2008) Conversion of a phase- to a rate-coded position signal by a three-stage model of theta cells, grid cells, and place cells. Hippocampus 18:1239–1255

    PubMed Central  PubMed  Google Scholar 

  • Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser M-B (2010) Grid cells in pre- and parasubiculum. Nat Neurosci 13:987–994

    CAS  PubMed  Google Scholar 

  • Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Roudi Y, Moser E, Moser M (2013) Grid cells require excitatory drive from the hippocampus. Nat Neurosci 16:309–317

    CAS  PubMed  Google Scholar 

  • Bostock E, Muller RU, Kubie JL (1991) Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1:193–206

    CAS  PubMed  Google Scholar 

  • Boucheny C, Brunel N, Arleo A (2005) A continuous attractor network model without recurrent excitation: maintenance and integration in the head direction cell system. J Comput Neurosci 18:205–227

    PubMed  Google Scholar 

  • Brandon M, Bogaard A, Libby C, Connerney M, Gupta K, Hasselmo M (2011) Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332:595–599

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brown EN, Frank LM, Tang D, Quirk MC, Wilson MA (1998) A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J Neurosci 18:7411–7425

    CAS  PubMed  Google Scholar 

  • Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP, Moser E, Moser M (2008) Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18:1200–1212

    PubMed  Google Scholar 

  • Burak Y, Fiete I (2006) Do we understand the emergent dynamics of grid cell activity. J Neurosci 26:9352–9354

    CAS  PubMed  Google Scholar 

  • Burak Y, Fiete IR (2009) Accurate path integration in continuous attractor network models of grid cells. PLoS Comput Biol 5:e1000291

    PubMed Central  PubMed  Google Scholar 

  • Burgess N, Recce M, O’Keefe J (1994) A model of hippocampal function. Neural Netw 7:1065–1081

    Google Scholar 

  • Burgess N, Jackson A, Hartley T, O’Keefe J (2000) Predictions derived from modelling the hippocampal role in navigation. Biol Cybern 83:301–312

    CAS  PubMed  Google Scholar 

  • Burgess N, Barry C, O’Keefe J (2007) An oscillatory interference model of grid cell firing. Hippocampus 17:801–812

    PubMed Central  PubMed  Google Scholar 

  • Buzsáki G (2006) Rhythms of the brain. Oxford University Press, New York, NY

    Google Scholar 

  • Buzsáki G, Moser E (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130–138

    PubMed  Google Scholar 

  • Caballero-Bleda M, Witter MP (1994) Projections from the presubiculum and the parasubiculum to morphologically characterized entorhinal-hippocampal projection neurons in the rat. Exp Brain Res 101:93–108

    CAS  PubMed  Google Scholar 

  • Chawla MK, Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL, Marriott LK, Worley PF, McNaughton BL, Barnes CA (2005) Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15:579–586

    CAS  PubMed  Google Scholar 

  • Clelland CD, Choi M, Romberg C, Clemenson GD, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210–213

    CAS  PubMed Central  PubMed  Google Scholar 

  • Colgin LL, Moser E, Moser M (2008) Understanding memory through hippocampal remapping. Trends Neurosci 31:469–477

    CAS  PubMed  Google Scholar 

  • Colgin LL, Leutgeb S, Jezek K, Leutgeb JK, Moser E, McNaughton B, Moser M (2010) Attractor-map versus autoassociation based attractor dynamics in the hippocampal network. J Neurophysiol 104:35–50

    PubMed Central  PubMed  Google Scholar 

  • Couey JJ, Witoelar A, Zhang S, Zheng K, Ye J, Dunn B, Czajkowski R, Moser M, Moser E, Roudi Y, Witter M (2013) Recurrent inhibitory circuitry as a mechanism for grid formation. Nat Neurosci 16:318–324

    CAS  PubMed  Google Scholar 

  • Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ (2010) Running enhances spatial pattern separation in mice. Proc Natl Acad Sci USA 107:2367–2372

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dabaghian Y, Mémoli F, Frank L, Carlsson G (2012) A topological paradigm for hippocampal spatial map formation using persistent homology. PLoS Comput Biol 8:e1002581

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davidson TJ, Kloosterman F, Wilson MA (2009) Hippocampal replay of extended experience. Neuron 63:497–507

    CAS  PubMed  Google Scholar 

  • Dayan P, Daw ND (2008) Decision theory, reinforcement learning, and the brain. Cogn Affect Behav Neurosci 8:429–453

    PubMed  Google Scholar 

  • Derdikman D (2009) Are the boundary-related cells in the subiculum boundary-vector cells? J Neurosci 29:13429–13431

    CAS  PubMed  Google Scholar 

  • Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T, Moser M, Moser E (2009) Frag-mentation of grid cell maps in a multicompartment environment. Nat Neurosci 12:1325–1332

    CAS  PubMed  Google Scholar 

  • Deshmukh SS, Knierim JJ (2011) Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front Behav Neurosci 5:1–33

    Google Scholar 

  • Deshmukh SS, Knierim JJ (2013) Inuence of local objects on hippocampal representations: landmark vectors and memory. Hippocampus 23:253–267

    PubMed  Google Scholar 

  • Diba K, Buzsáki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10:1241–1242

    CAS  PubMed Central  PubMed  Google Scholar 

  • Domnisoru C, Kinkhabwala AA, Tank DA (2013) Membrane potential dynamics of grid cells. Nature 495:199–204

    CAS  PubMed  Google Scholar 

  • Dragoi G, Tonegawa S (2011) Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469:397–401

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dudchenko PA, Taube JS (1997) Correlation between head direction cell activity and spatial behavior on a radial arm maze. Behav Neurosci 111:3–19

    CAS  PubMed  Google Scholar 

  • Durrant-Whyte H, Bailey T (2006) Simultaneous localization and mapping (SLAM): part 1 the essential algorithms. Robot Autom Mag 13:99–110

    Google Scholar 

  • Eichenbaum H, Lipton PA (2008) Towards a functional organization of the medial temporal lobe memory system: role of the parahippocampal and medial entorhinal cortical areas. Hippocampus 18:1314–1324

    PubMed Central  PubMed  Google Scholar 

  • Eilam D, Golani I (1989) Home base behavior of rats (rattus norvegicus) exploring a novel environment. Behav Brain Res 34:199–211

    CAS  PubMed  Google Scholar 

  • Ferbinteanu J, Holsinger RM, McDonald RJ (1999) Lesions of the medial or lateral perforant path have different effects on hippocampal contributions to place learning and on fear conditioning to context. Behav Brain Res 101:65–84

    CAS  PubMed  Google Scholar 

  • Fiete IR (2010) Losing phase. Neuron 66:331–334

    CAS  PubMed  Google Scholar 

  • Fiete IR, Burak Y, Brookings T (2008) What grid cells convey about rat location. J Neurosci 28:6858–6871

    CAS  PubMed  Google Scholar 

  • Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680–683

    CAS  PubMed  Google Scholar 

  • Frank LM, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27:169–178

    CAS  PubMed  Google Scholar 

  • Franzius M, Vollgraf R, Wiskott L (2007) From grids to places. J Comput Neurosci 22:297–299

    CAS  PubMed  Google Scholar 

  • Fuhs MC, Touretzky DS (2006) A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26:4266–4276

    CAS  PubMed  Google Scholar 

  • Fuhs MC, Vanrhoads SR, Casale A, McNaughton B, Touretzky D (2005) Inuence of path integration versus environmental orientation on place cell remapping between visually identical environments. J Neurophysiol 94:2603–2616

    PubMed  Google Scholar 

  • Fyhn M, Molden S, Witter M, Moser E, Moser M (2004) Spatial representation in the entorhinal cortex. Science 305:1258–1264

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gilbert PE, Kesner RP, Lee I (2001) Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus 11:626–636

    CAS  PubMed  Google Scholar 

  • Giocomo LM, Zilli EA, Fransen E, Hasselmo ME (2007) Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315:1719–1722

    CAS  PubMed Central  PubMed  Google Scholar 

  • Giocomo LM, Moser M, Moser E (2011) Computational models of grid cells. Neuron 71:589–603

    CAS  PubMed  Google Scholar 

  • Golani I, Benjamini Y, Eilam D (1993) Stopping behavior: constraints on exploration in rats (rattus norvegicus). Behav Brain Res 53:21–33

    CAS  PubMed  Google Scholar 

  • Goodrich-Hunsaker NJ, Hunsaker MR, Kesner RP (2008) The interactions and dissociations of the dorsal hippocampus subregions: how the dentate gyrus, CA3, and CA1 process spatial information. Behav Neurosci 122:16–26

    PubMed  Google Scholar 

  • Gothard K, Skaggs W, McNaughton B (1996) Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J Neurosci 16:8027–8040

    CAS  PubMed  Google Scholar 

  • Grossberg S (1969) A global prediction (or learning) theory for some nonlinear functional-differential equations. Stud Appl Math 5:64–70

    Google Scholar 

  • Grossberg S (1971) Pavlovian pattern learning by nonlinear neural networks. Proc Natl Acad Sci USA 68:828–831

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guanella A, Kiper D, Verschure P (2007) A model of grid cells based on a twisted torus topology. Int J Neural Syst 17:231–240

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610–614

    CAS  PubMed  Google Scholar 

  • Hartley T, Burgess N, Lever C, Cacucci F, O’Keefe J (2000) Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10:369–379

    CAS  PubMed  Google Scholar 

  • Hasselmo ME (2008) Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18:1213–1229

    PubMed Central  PubMed  Google Scholar 

  • Hasselmo ME (2012) How we remember: brain mechanisms of episodic memory. MIT Press, Cambridge, MA

    Google Scholar 

  • Hasselmo ME, Wyble BP (1997) Free recall and recognition in a network model of the hippocampus: simulating effects of scopolamine on human memory function. Behav Brain Res 89:1–34

    CAS  PubMed  Google Scholar 

  • Hasselmo ME, Giocomo LM, Zilli EA (2007) Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17:1252–1271

    PubMed Central  PubMed  Google Scholar 

  • Hayman RM, Jeffery KJ (2008) How heterogeneous place cell responding arises from homogeneous grids-a contextual gating hypothesis. Hippocampus 18:1301–1313

    PubMed  Google Scholar 

  • Hayman RMA, Chakraborty S, Anderson MI, Jeffery KJ (2003) Context-specific acquisition of location discrimination by hippocampal place cells. Eur J Neurosci 18:2825–2834

    PubMed  Google Scholar 

  • Hebb DO (1949) The organization of behavior. Wiley-Interscience, New York, NY

    Google Scholar 

  • Henze DA, Wittner L, Buzsáki G (2002) Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5:790–795

    CAS  PubMed  Google Scholar 

  • Hopfield JJ (1982) Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci USA 79:2554–2558

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jadhav SP, Kemere C, German PW, Frank LM (2012) Awake hippocampal sharp-wave ripples support spatial memory. Science 336:1454–1458

    CAS  PubMed  Google Scholar 

  • Jeffery KJ, Donnett JG, Burgess N, O’Keefe J (1997) Directional control of hippocampal place fields. Exp Brain Res 117:131–142

    CAS  PubMed  Google Scholar 

  • Johnson A, Redish AD (2007) Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci 27:12176–12189

    CAS  PubMed  Google Scholar 

  • Jung MW, McNaughton BL (1993) Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165–182

    CAS  PubMed  Google Scholar 

  • Kamondi A, Acsády L, Wang X, Buzsáki G (1998) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8:244–261

    CAS  PubMed  Google Scholar 

  • Karlsson MP, Frank L (2009) Awake replay of remote experiences in the hippocampus. Nat Neurosci 12:913–918

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kesner RP (2007) A behavioral analysis of dentate gyrus function. Prog Brain Res 163:567–576

    PubMed  Google Scholar 

  • Kesner RP (2013) An analysis of the dentate gyrus function. Behav Brain Res 163:567–576

    Google Scholar 

  • Kheirbek MA, Tannenholz L, Hen R (2012) NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J Neurosci 32:8696–8702

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim SM, Ganguli S, Frank LM (2012) Spatial information outflow from the hippocampal circuit: distributed spatial coding and phase precession in the subiculum. J Neurosci 32:11539–11558

    CAS  PubMed Central  PubMed  Google Scholar 

  • Knierim JJ, Kudrimoti HS, McNaughton BL (1995) Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15:1648–1659

    CAS  PubMed  Google Scholar 

  • Knierim JJ, Kudrimoti HS, McNaughton BL (1996) Neuronal mechanisms underlying the interaction between visual landmarks and path integration in the rat. Int J Neural Syst 7:213–218

    CAS  PubMed  Google Scholar 

  • Knierim JJ, Lee I, Hargreaves E (2006) Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus 16:755–764

    PubMed  Google Scholar 

  • Koenig J, Linder AN, Leutgeb JK, Leutgeb S (2011) The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332:592–595

    CAS  PubMed  Google Scholar 

  • Komorowski RW, Manns JR, Eichenbaum H (2009) Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. J Neurosci 29:9918–9929

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kropff E, Treves A (2008) The emergence of grid cells: intelligent design or just adaptation? Hippocampus 18:1256–1269

    PubMed  Google Scholar 

  • Lansner A (2009) Associative memory models: from the cell-assembly theory to biophysically detailed cortex simulations. Trends Neurosci 32:178–186

    CAS  PubMed  Google Scholar 

  • Lee I, Kesner RP (2002) Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nat Neurosci 5:162–168

    CAS  PubMed  Google Scholar 

  • Lee I, Rao G, Knierim J (2004a) A double dissociation between hippocampal subfields: differential time course of CA3 and CA1 place cells for processing changed environments. Neuron 42:803–815

    CAS  PubMed  Google Scholar 

  • Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004b) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430:456–459

    CAS  PubMed  Google Scholar 

  • Lengyel M, Szatmáry Z, Erdi P (2003) Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13:700–714

    PubMed  Google Scholar 

  • Leutgeb S, Leutgeb JK (2007) Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learn Mem 14:745–757

    PubMed  Google Scholar 

  • Leutgeb S, Leutgeb J, Treves A, Moser M, Moser E (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295–1298

    CAS  PubMed  Google Scholar 

  • Leutgeb S, Leutgeb J, Barnes C, Moser E, McNaughton B, Moser M (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309:619–623

    CAS  PubMed  Google Scholar 

  • Leutgeb S, Leutgeb J, Moser E, Moser M (2006) Fast rate coding in hippocampal CA3 cell ensembles. Hippocampus 16:765–774

    PubMed  Google Scholar 

  • Leutgeb JK, Leutgeb S, Moser M, Moser E (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961–966

    CAS  PubMed  Google Scholar 

  • Lever C, Wills T, Cacucci F, Burgess N, O’Keefe J (2002) Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416:90–94

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lisman J (2007) Role of the dual entorhinal inputs to hippocampus: a hypothesis based on cue/action (non-self/self) couplets. Prog Brain Res 163:615–625

    PubMed  Google Scholar 

  • Lu L, Leutgeb JK, Tsao A, Henriksen EJ, Leutgeb S, Barnes CA, Witter MP, Moser MB, Moser EI (2013) Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex. Nat Neurosci 16:1085–1093

    CAS  PubMed  Google Scholar 

  • Magee JC (2001) Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons. J Neurophysiol 86:528–532

    CAS  PubMed  Google Scholar 

  • Manns JR, Eichenbaum H (2009) A cognitive map for object memory in the hippocampus. Learn Mem 16:616–624

    PubMed Central  PubMed  Google Scholar 

  • Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc B 262:23–81

    CAS  Google Scholar 

  • Marrone DF, Adams AA, Satvat E (2011) Increased pattern separation in the aged fascia dentata. Neurobiol Aging 32:2317.e23–2317.e32

    Google Scholar 

  • McClelland JL, Rumelhart DE (1985) Distributed memory and the representation of general and specific information. J Exp Psychol Gen 114:159–197

    CAS  PubMed  Google Scholar 

  • McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317:94–99

    CAS  PubMed  Google Scholar 

  • McNaughton BL, Barnes CA (1977) Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat. J Comput Neurosci 175:439–453

    CAS  Google Scholar 

  • McNaughton BL, Morris RG (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415

    Google Scholar 

  • McNaughton BL, Barnes CA, Gerrard K, Gothard KM, Jung MW, Knierim JJ, Kudrimoti HS, Qin Y, Skaggs WE, Suster M, Weaver KL (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199:173–185

    CAS  PubMed  Google Scholar 

  • McNaughton BL, Battaglia F, Jensen O, Moser E, Moser M (2006) Path integration and the neural basis of the cognitive map. Nat Rev Neurosci 7:663–678

    CAS  PubMed  Google Scholar 

  • Meyer JA, Filliat D (2003) Map-based navigation in mobile robots: II. A review of map-learning and path-planning strategies. Cogn Syst Res 4:283–317

    Google Scholar 

  • Mhatre H, Gorchetchnikov A, Grossberg S (2010) Grid cell hexagonal patterns formed by fast self-organized learning within entorhinal cortex. Hippocampus 22:320–334

    PubMed  Google Scholar 

  • Milford M, Wyeth G (2010) Persistent navigation of mapping using a biologically inspired SLAM system. Int J Robot Res 29:1131–1153

    Google Scholar 

  • Mizumori SJ, Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13:4015–4028

    CAS  PubMed  Google Scholar 

  • Mizuseki K, Sirota A, Pastalkova E, Buzsáki G (2009) Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64:267–280

    CAS  PubMed Central  PubMed  Google Scholar 

  • Monaco JD, Abbott LF, Abbott LF (2011) Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J Neurosci 31:9414–9425

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morris AM, Churchwell JC, Kesner RP, Gilbert PE (2012) Selective lesions of the dentate gyrus produce disruptions in place learning for adjacent spatial locations. Neurobiol Learn Mem 97:326–331

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Muller RU, Stead M, Pach J (1996) The hippocampus as a cognitive graph. J Gen Physiol 107:663–694

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez-Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188–201

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakazawa K, Sun LD, Quirk MC, Rondi-Reig L, Wilson MA, Tonegawa S (2003) Hip-pocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38:305–315

    CAS  PubMed  Google Scholar 

  • Neunuebel JP, Knierim JJ (2012) Spatial firing correlates of physiologically distinct cell types of the rat dentate gyrus. J Neurosci 32:3848–3858

    CAS  PubMed Central  PubMed  Google Scholar 

  • O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78–109

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • O’Keefe J, Burgess N (2005) Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15:853–866

    PubMed Central  PubMed  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

    PubMed  Google Scholar 

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

    Google Scholar 

  • O’Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–330

    PubMed  Google Scholar 

  • O’Reilly RC, McClelland JL (1994) Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 4:661–682

    PubMed  Google Scholar 

  • Parron C, Save E (2004a) Evidence for entorhinal and parietal cortices involvement in path integration in the rat. Exp Brain Res 159:349–359

    PubMed  Google Scholar 

  • Parron C, Save E (2004b) Comparison of the effects of entorhinal and retrosplenial cortical lesions on habituation, reaction to spatial and non-spatial changes during object exploration in the rat. Neurobiol Learn Mem 82:1–11

    CAS  PubMed  Google Scholar 

  • Pastoll H, Solanka L, van Rossum MCW, Nolan MF (2013) Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Cell 77:141–154

    CAS  Google Scholar 

  • Piatti VC, Ewell LA, Leutgeb JK (2013) Neurogenesis in the dentate gyrus: carrying the message or dicating the tone. Front Neurosci 7:50

    PubMed Central  PubMed  Google Scholar 

  • Prescott TJ (1996) Spatial representation for navigation in animats. Adapt Behav 4:85–123

    Google Scholar 

  • Quirk GJ, Muller RU, Kubie JL (1990) The firing of hippocampal place cells in the dark depends on the rat’s recent experience. J Neurosci 10:2008–2017

    CAS  PubMed  Google Scholar 

  • Quirk GJ, Muller RU, Kubie JL, Ranck JB (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945–1963

    CAS  PubMed  Google Scholar 

  • Ranck JB (1984) Head-direction cells in the deep cell layers of dorsal presubiculum in freely moving rats. In SFN Poster

    Google Scholar 

  • Redish DA (1999) Beyond the cognitive map. MIT Press, Cambridge, MA

    Google Scholar 

  • Redish DA, Touretzky DS (1997) Cognitive maps beyond the hippocampus. Hippocampus 7:15–35

    CAS  PubMed  Google Scholar 

  • Redish DA, Touretzky DS (1998) The role of the hippocampus in solving the morris water maze. Neural Comput 10:73–111

    CAS  PubMed  Google Scholar 

  • Redish DA, Elga AN, Touretzky DS (1996) A coupled attractor model of the rodent direction system. Netw Comput Neural Syst 7:671–685

    Google Scholar 

  • Reifenstein ET, Kempter R, Schreiber S, Stemmler MB, Herz AVM (2012) Grid cells in rat entorhinal cortex encode physical space with independent firing fields and phase precession at the single-trial level. Proc Natl Acad Sci USA 109:6301–6306

    CAS  PubMed Central  PubMed  Google Scholar 

  • Remme MWH, Lengyel M, Gutkin BS (2010) Democracy-independence trade-off in oscillating dendrites and its implications for grid cells. Neuron 66:429–437

    CAS  PubMed Central  PubMed  Google Scholar 

  • Renaudineau S, Poucet B, Save E (2007) Flexible use of proximal objects and distal cues by hippocampal place cells. Hippocampus 17:381–395

    PubMed  Google Scholar 

  • Rolls ET, Stringer SM, Elliot T (2006) Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Netw Comput Neural Syst 447:447–465

    Google Scholar 

  • Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC, Buzsáki G (2012) Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 15:769–775

    CAS  PubMed  Google Scholar 

  • Sahay A, Scobie KN, Hill AS, O’Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466–470

    CAS  PubMed Central  PubMed  Google Scholar 

  • Samsonovich A, McNaughton BL (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17:5900–5920

    CAS  PubMed  Google Scholar 

  • Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser M, Moser E (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–762

    CAS  PubMed  Google Scholar 

  • Satvat E, Schmidt B, Argraves M, Marrone DF, Markus EJ (2011) Changes in task demands alter the pattern of zif268 expression in the dentate gyrus. J Neurosci 31:7163–7167

    CAS  PubMed  Google Scholar 

  • Savelli F, Knierim JJ (2010) Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. J Neurophysiol 103:3167–3183

    PubMed Central  PubMed  Google Scholar 

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

    PubMed Central  PubMed  Google Scholar 

  • Schmajuk NA (1990) Role of the hippocampus in temporal and spatial navigation: an adaptive neural network. Behav Brain Res 39:205–229

    CAS  PubMed  Google Scholar 

  • Schmajuk NA, Blair HT (1993) Place learning and the dynamics of spatial navigation: a neural network approach. Adapt Behav 1:353–385

    Google Scholar 

  • Schmidt B, Marrone DF, Markus EJ (2012) Disambiguating the similar: the dentate gyrus and pattern separation. Behav Brain Res 226:56–65

    PubMed  Google Scholar 

  • Schmidt-Hieber C, Hausser M (2013) Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat Neurosci 16:325–331

    CAS  PubMed  Google Scholar 

  • Seung HS (1996) How the brain keeps the eyes still. Proc Natl Acad Sci USA 93:13339–13344

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sharp PE (1991) Computer simulation of hippocampal place cells. Psychobiology 19:103–115

    Google Scholar 

  • Sharp PE (2006) Subicular place cells generate the same “map” for different environments: comparison with hippocampal cells. Behav Brain Res 174:206–214

    CAS  PubMed  Google Scholar 

  • Sharp PE, Green C (1994) Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci 14:2339–2356

    CAS  PubMed  Google Scholar 

  • Siegel JJ, Neunuebel JP, Knierim JJ (2008) Dominance of the proximal coordinate frame in determining the locations of hippocampal place cell activity during navigation. J Neurophysiol 99:60–76

    PubMed Central  PubMed  Google Scholar 

  • Sik A, Ylinen A, Penttonen M, Buzsáki G (1994) Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 265:1722–1724

    CAS  PubMed  Google Scholar 

  • Skaggs W, Knierim JJ, Kudrimoti HS, McNaughton BL (1995) A model of the neural basis of the rat’s sense of direction. Adv Neural Inf Process Syst 7:173–180

    CAS  PubMed  Google Scholar 

  • Solstad T, Moser E, Einevoll GT (2006) From grid cells to place cells: a mathematical model. Hippocampus 16:1026–1031

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sreenivasan S, Fiete I (2011) Grid cells generate an analog error-correcting code for singularly precise neural computation. Nat Neurosci 14:1330–1337

    CAS  PubMed  Google Scholar 

  • Stackman RW, Taube JS (1997) Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17:4349–4358

    CAS  PubMed Central  PubMed  Google Scholar 

  • Steffenach H-A, Witter M, Moser M-B, Moser EI (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45:301–313

    CAS  PubMed  Google Scholar 

  • Stensola H, Stensola T, Solstad T, Frøland K, Moser M, Moser E (2012) The entorhinal grid map is discretized. Nature 492:72–78

    CAS  PubMed  Google Scholar 

  • Stringer SM, Trappenberg TP, Rolls ET, Araujo IET (2002) Self-organizing continuous attractor networks and path integration: one-dimensional models of head direction cells. Netw Comput Neural Syst 13:217–242

    CAS  Google Scholar 

  • Takahashi H, Magee JC (2009) Pathway interactions and synaptic plasticity in the dendritic tuftregions of CA1 pyramidal neurons. Neuron 62:102–111

    CAS  PubMed  Google Scholar 

  • Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86

    CAS  PubMed  Google Scholar 

  • Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Taube JS, Goodridge JP, Golob EJ, Dudchenko PA, Stackman RW (1996) Processing the head direction cell signal: a review and commentary. Brain Res Bull 40:477–484, discussion 484–6

    CAS  PubMed  Google Scholar 

  • Tchernichovski O, Benjamini Y, Golani I (1998) The dynamics of long-term exploration in the rat. Biol Cybern 78:423–432

    CAS  PubMed  Google Scholar 

  • Teyler TJ, DiScenna P (1986) The hippocampal memory indexing theory. Behav Neurosci 100:147–154

    CAS  PubMed  Google Scholar 

  • Teyler TJ, Rudy JW (2007) The hippocampal indexing theory and episodic memory: updating the index. Hippocampus 17:1158–1169

    PubMed  Google Scholar 

  • Tolman EC (1948) Cognitive maps in rats and men. Pschol Rev 4:189–208

    Google Scholar 

  • Tolman EC, Ritchie BF, Kalish D (1946) Studies in spatial learning. 1. Orientation and the short-cut. J Exp Psychol 36:13–24

    CAS  PubMed  Google Scholar 

  • Touretzky DS, Redish DA (1996) Theory of rodent navigation based on interacting representations of space. Hippocampus 6:247–270

    CAS  PubMed  Google Scholar 

  • Touretzky DS, Redish DA, Wan H (1993) Neural representation of space using sinusodial arrays. Neural Comput 5:869–884

    Google Scholar 

  • Treves A, Rolls ET (1992) Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2:189–199

    CAS  PubMed  Google Scholar 

  • Treves A, Tashiro A, Witter MP, Moser E (2008) What is the mammalian dentate gyrus good for? Neuroscience 154:1155–1172

    CAS  PubMed  Google Scholar 

  • Tronel S, Belnoue L, Grosjean N, Revest J, Piazza P, Koehl M, Abrous DN (2012) Adult-born neurons are necessary for extended contextual discrimination. Hippocampus 22:292–298

    PubMed  Google Scholar 

  • Tsodyks M, Sejnowski T (1995) Associative memory and hippocampal place cells. Int J Neural Syst 6:81–86

    Google Scholar 

  • Van Cauter T, Camon J, Alvernhe A, Elduayen C, Sargolini F, Save E (2012) Distinct roles of medial and lateral entorhinal cortex in spatial cognition. Cereb Cortex 23:451–459

    PubMed  Google Scholar 

  • van Groen T, Wyss JM (1990) The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections. Brain Res 529:165–177

    PubMed  Google Scholar 

  • VanElzakker M, Fevurly RD, Breindel T, Spencer RL (2008) Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex. Learn Mem 15:899–908

    PubMed Central  PubMed  Google Scholar 

  • Vazdarjanova A, Guzowski J (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489–6496

    CAS  PubMed  Google Scholar 

  • Wallace DG, Hamilton DA, Whishaw IQ (2006) Movement characteristics support a role for dead reckoning in organizing exploratory behavior. Anim Cogn 9:219–228

    PubMed  Google Scholar 

  • Wan H, Touretzky DS, Redish DA (1993) Towards a computational theory of rat navigation. In: Mozer M, Smolensky P, Touretzky DS, Elman J, Wigend A (eds) Proceedings of the 1993 connectionist models summer school. Lawrence Erlbaum Associates, Hillsdale, NJ, pp 11–19

    Google Scholar 

  • Wan H, Aggleton JP, Brown MW (1999) Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19:1142–1148

    CAS  PubMed  Google Scholar 

  • Welday AC, Shlifer IG, Bloom ML, Zhang K, Blair HT (2011) Cosine directional tuning of theta cell burst frequencies: evidence for spatial coding by oscillatory interference. J Neurosci 31:16157–16176

    CAS  PubMed Central  PubMed  Google Scholar 

  • Welinder PE, Burak Y, Fiete IR (2008) Grid cells: the position code, neural network models of activity, and the problem of learning. Hippocampus 18:1283–1300

    PubMed  Google Scholar 

  • Whishaw IQ, Gharbawie OA, Clark BJ, Lehmann H (2006) The exploratory behavior of rats in an open environment optimizes security. Behav Brain Res 171:230–239

    PubMed  Google Scholar 

  • Wikenheiser AM, Redish AD (2011) Changes in reward contingency modulate the trial-to-trial variability of hippocampal place cells. J Neurophysiol 106:589–598

    PubMed Central  PubMed  Google Scholar 

  • Wills T, Lever C, Cacucci F, Burgess N, O’Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308:873–876

    CAS  PubMed Central  PubMed  Google Scholar 

  • Witter MP, Amaral DG (2004) Hippocampal formation. In: Paxinos G (ed) The rat nervous system. Elsevier, San Diego, CA, pp 635–704

    Google Scholar 

  • Witter MP, Wouterlood FG, Naber PA, Van Haeften T (2006) Anatomical organization of the parahippocampal-hippocampal network. Ann N Y Acad Sci 911:1–24

    Google Scholar 

  • Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397:613–616

    CAS  PubMed  Google Scholar 

  • Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27:623–633

    CAS  PubMed  Google Scholar 

  • Yartsev MM, Witter MP, Ulanovsky N (2011) Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479:103–107

    CAS  PubMed  Google Scholar 

  • Yassa MA, Stark CEL (2011) Pattern separation in the hippocampus. Trends Neurosci 34:515–525

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoganarasimha D, Knierim JJ (2005) Coupling between place cells and head direction cells during relative translations and rotations of distal landmarks. Exp Brain Res 160:344–359

    CAS  PubMed  Google Scholar 

  • Yoganarasimha D, Yu X, Knierim JJ (2006) Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J Neurosci 26:622–631

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoganarasimha D, Rao G, Knierim JJ (2011) Lateral entorhinal neurons are not spatially selective in cue-rich environments. Hippocampus 21:1363–1374

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoon K, Buice MA, Barry C, Hayman R, Burgess N, Fiete IR (2013) Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat Neurosci 16:1077–1084

    CAS  PubMed Central  PubMed  Google Scholar 

  • Young BJ, Otto T, Fox GD, Eichenbaum H (1997) Memory representation within the parahip-pocampal region. J Neurosci 17:5183–5195

    CAS  PubMed  Google Scholar 

  • Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 15:2112–2126

    Google Scholar 

  • Zhang S, Ye J, Miao C, Tsao A, Cerniauskas I, Ledergerber D, Moser MB, Moser EI (2013) Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 340:1232627

    PubMed  Google Scholar 

  • Zhu XO, Brown MW, Aggleton JP (1995) Neuronal signalling of information important to visual recognition memory in rat rhinal and neighbouring cortices. Eur J Neurosci 7:753–765

    CAS  PubMed  Google Scholar 

  • Zilli EA (2012) Models of grid cell spatial firing published 2005–2011. Front Neural Circuits 6:16

    PubMed Central  PubMed  Google Scholar 

  • Zilli EA, Hasselmo ME (2010) Coupled noisy spiking neurons as velocity-controlled oscillators in a model of grid cell spatial firing. J Neurosci 30:13850–13860

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zilli EA, Yoshida M, Tahvildari B, Giocomo LM, Hasselmo ME (2009) Evaluation of the oscillatory interference model of grid cell firing through analysis and measured period variance of some biological oscillators. PLoS Comput Biol 5:e1000573

    PubMed Central  PubMed  Google Scholar 

  • Zipser D (1985) A computational model of hippocampal place fields. Behav Neurosci 99:1006–1018

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

John Widloski thanks Brian Gereke, Dong-oh Seo, Laura Colgin, and Jim Knierim for helpful discussions during the writing of the manuscript. Ila Fiete thanks Jeff Magee and Jim Knierim for useful discussions on the roles of CA1 and CA3 in navigation. Ila Fiete is a Sloan Foundation Fellow, a Searle Scholar, a McKnight Scholar, and acknowledges funding from the Office of Naval Research, through ONR MURI award N00014-10-1-0936.

Author information

Authors and Affiliations

  1. Center for Learning and Memory, University of Texas, Austin, TX, USA

    John Widloski & Ila Fiete

Authors
  1. John Widloski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ila Fiete
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ila Fiete .

Editor information

Editors and Affiliations

  1. Rappaport Faculty of Medicine, Technion- Israel Institute of Technology, Haifa, Israel

    Dori Derdikman

  2. The Solomon H. Snyder Dept. of Neurosc., John Hopkins University The Zanvyl Krieger Mind/Brain Institute, Baltimore, Maryland, USA

    James J. Knierim

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Wien

About this chapter

Cite this chapter

Widloski, J., Fiete, I. (2014). How Does the Brain Solve the Computational Problems of Spatial Navigation?. In: Derdikman, D., Knierim, J. (eds) Space,Time and Memory in the Hippocampal Formation. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1292-2_14

Download citation

Publish with us

Policies and ethics

Search

Navigation