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Models of Path Integration in the Hippocampal Complex

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Space,Time and Memory in the Hippocampal Formation

Abstract

Path integration is the process of summing up information about direction and distance traveled, in order to keep track of one’s relative position. Path integration is hypothesized to be the basis for the formation of the “place code” the hippocampus uses to encode spatial memories. In this chapter, we discuss models of how the hippocampal system may implement path integration. First, we explain the relationship of path integration to the hippocampal system, compare path integration to other navigation strategies, and discuss evidence for its use in creating the place cell code. Then, we examine path integration models for the creation and updating of a place cell map representation. We compare two major classes of such models and discuss experimental tests of their predictions to date. Finally, we briefly discuss the role of associations between place cell activity and sensory information in resetting the path integrator systems upon visits to familiar locations and how those associations can modify the structure of the hippocampal map with experience.

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References

  • Alyan SH (2010) Evidence for resetting the directional component of path integration in the house mouse (Mus musculus). Ethology 102(4):629–638. doi:10.1111/j.1439-0310.1996.tb01154.x

    Google Scholar 

  • Alyan SH, McNaughton BL (1999) Hippocampectomized rats are capable of homing by path integration. Behav Neurosci 113(1):19–31

    CAS  PubMed  Google Scholar 

  • Amit D, Tsodyks M (1991) Quantitative study of attractor neural network retrieving at low spike rates: I Substrate-spikes, rates and neuronal gain. Netw Comput Neural Syst 2:259–273

    Google Scholar 

  • Andersen RA, Snyder LH, Bradley DC, Xing J (1997) Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu Rev Neurosci 20:303–30. doi:10.1146/annurev.neuro.20.1.303

    CAS  PubMed  Google Scholar 

  • Barnes CA, Suster MS, Shen J, McNaughton BL (1997) Multistability of cognitive maps in the hippocampus of old rats. Nature 388(6639):272–275. doi:10.1038/40859

    CAS  PubMed  Google Scholar 

  • Barry C, Hayman R, Burgess N, Jeffery KJ (2007) Experience-dependent rescaling of entorhinal grids. Nat Neurosci 10(6):682–4. doi:10.1038/nn1905

    CAS  PubMed  Google Scholar 

  • Battaglia F, Treves A (1998) Attractor neural networks storing multiple space representations: A model for hippocampal place fields. Phys Rev E 58(6):7738–7753. doi:10.1103/PhysRevE.58.7738

    CAS  Google Scholar 

  • Blair HT, Welday AC, Zhang K (2007) Scale-invariant memory representations emerge from moiré interference between grid fields that produce theta oscillations: a computational model. J Neurosci 27(12):3211–29. doi:10.1523/JNEUROSCI.4724-06.2007

    CAS  PubMed  Google Scholar 

  • Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Moser M-B et al (2013) Grid cells require excitatory drive from the hippocampus. Nat Neurosci 16(3):309–17. doi:10.1038/nn.3311

    CAS  PubMed  Google Scholar 

  • Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hasselmo ME (2011) Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science (New York, NY) 332(6029):595–9. doi:10.1126/science.1201652

    CAS  Google Scholar 

  • Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP, Moser EI, Moser M-BB (2008) Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18(12):1200–1212. doi:10.1002/hipo.20504

    PubMed  Google Scholar 

  • Burak Y, Fiete IR (2006) Do we understand the emergent dynamics of grid cell activity? J Neurosci 26(37):9352–9354. doi:10.1523/JNEUROSCI.2857-06.2006

    CAS  PubMed  Google Scholar 

  • Burak Y, Fiete IR (2009) Accurate path integration in continuous attractor network models of grid cells. PLoS Comput Biol 5(2):e1000291. doi:10.1371/journal.pcbi.1000291

    PubMed Central  PubMed  Google Scholar 

  • Bures J, Fenton AA, Kaminsky Y, Rossier J, Sacchetti B, Zinyuk L (1997) Dissociation of exteroceptive and idiothetic orientation cues: effect on hippocampal place cells and place navigation. Philos Trans R Soc Lond B Biol Sci 352(1360):1515–24. doi:10.1098/rstb.1997.0138

    CAS  PubMed Central  PubMed  Google Scholar 

  • Burgess N (2008) Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18(12):1157–1174. doi:10.1002/hipo.20518

    PubMed Central  PubMed  Google Scholar 

  • Burgess N, Recce M, O’Keefe J (1994) A model of hippocampal function. Neural Network 7(6–7):1065–1081

    Google Scholar 

  • Burgess N, Barry C, O’Keefe J (2007) An oscillatory interference model of grid cell firing. Hippocampus 17(9):801–812. doi:10.1002/hipo.20327

    PubMed Central  PubMed  Google Scholar 

  • Burke SN, Wallace JL, Hartzell AL, Nematollahi S, Plange K, Barnes CA (2011) Age-associated deficits in pattern separation functions of the perirhinal cortex: a cross-species consensus. Behav Neurosci 125(6):836–47. doi:10.1037/a0026238

    PubMed Central  PubMed  Google Scholar 

  • Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser EI (2009) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462(7271):353–7. doi:10.1038/nature08573

    CAS  PubMed  Google Scholar 

  • Colgin LL, Leutgeb S, Jezek K, Leutgeb JK, Moser EI, McNaughton BL, Moser M-B (2010) Attractor-map versus autoassociation based attractor dynamics in the hippocampal network. J Neurophysiol 104(1):35–50. doi:10.1152/jn.00202.2010

    PubMed Central  PubMed  Google Scholar 

  • Collett TS, Cartwright BA, Smith BA (1986) Landmark learning and visuo-spatial memories in gerbils. J Comp Physiol A 158(6):835–851

    CAS  PubMed  Google Scholar 

  • Couey JJ, Witoelar A, Zhang S-J, Zheng K, Ye J, Dunn B, Witter MP (2013) Recurrent inhibitory circuitry as a mechanism for grid formation. Nat Neurosci 16(3):318–24. doi:10.1038/nn.3310

    CAS  PubMed  Google Scholar 

  • De Almeida L, Idiart M, Lisman JE (2009) The input–output transformation of the hippocampal granule cells: from grid cells to place fields. J Neurosci 29(23):7504–12. doi:10.1523/JNEUROSCI.6048-08.2009

    PubMed Central  PubMed  Google Scholar 

  • Derdikman D, Moser EI (2010) A manifold of spatial maps in the brain. Trends Cogn Sci 14(12):561–9. doi:10.1016/j.tics.2010.09.004

    PubMed  Google Scholar 

  • Derdikman D, Moser EI (2014) Spatial maps in the entorhinal cortex and adjacent structures. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, Heidelberg

    Google Scholar 

  • Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T, Moser M-B, Moser EI (2009) Fragmentation of grid cell maps in a multicompartment environment. Nat Neurosci 12(10):1325–32. doi:10.1038/nn.2396

    CAS  PubMed  Google Scholar 

  • Dhillon A, Jones RS (2000) Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99(3):413–422

    CAS  PubMed  Google Scholar 

  • Doeller CF, Barry C, Burgess N (2010) Evidence for grid cells in a human memory network. Nature 463(7281):657–61. doi:10.1038/nature08704

    CAS  PubMed Central  PubMed  Google Scholar 

  • Domnisoru C, Kinkhabwala AA, Tank DW (2013) Membrane potential dynamics of grid cells. Nature 495(7440):199–204. doi:10.1038/nature11973

    CAS  PubMed  Google Scholar 

  • Etienne AS (1992) Navigation of a small mammal by dead reckoning and local cues. Curr Dir Psychol Sci 1(2):48–52

    Google Scholar 

  • Fenton AA, Lytton WW, Barry JM, Lenck-Santini P-P, Zinyuk LE, Kubík S, Olypher AV (2010) Attention-like modulation of hippocampus place cell discharge. J Neurosci 30(13):4613–25. doi:10.1523/JNEUROSCI.5576-09.2010

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fernandez FR, White JA (2008) Artificial synaptic conductances reduce subthreshold oscillations and periodic firing in stellate cells of the entorhinal cortex. J Neurosci 28(14):3790–803. doi:10.1523/JNEUROSCI.5658-07.2008

    CAS  PubMed  Google Scholar 

  • Foster DJ, Wilson MA (2007) Hippocampal theta sequences. Hippocampus 17(11):1093–1099. doi:10.1002/hipo.20345

    PubMed  Google Scholar 

  • Foster TC, Castro CA, McNaughton BL (1989) Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement. Science 244(4912):1580–1582

    CAS  PubMed  Google Scholar 

  • Frank LM, Stanley GB, Brown EN (2004) Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 24(35):7681–9. doi:10.1523/JNEUROSCI.1958-04.2004

    CAS  PubMed  Google Scholar 

  • Fuhs MC, Touretzky DS (2006) A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26(16):4266–76. doi:10.1523/JNEUROSCI.4353-05.2006

    CAS  PubMed  Google Scholar 

  • Fuhs MC, Vanrhoads SR, Casale AE, McNaughton B, Touretzky DS (2005) Influence of path integration versus environmental orientation on place cell remapping between visually identical environments. J Neurophysiol 94(4):2603–16. doi:10.1152/jn.00132.2005

    PubMed  Google Scholar 

  • Fyhn M, Molden S, Witter MP, Moser EI, Moser M-B (2004) Spatial representation in the entorhinal cortex. Science (New York, NY) 305(5688):1258–64. doi:10.1126/science.1099901

    CAS  Google Scholar 

  • Fyhn M, Hafting T, Treves A, Moser M-B, Moser EI (2007) Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446(7132):190–4. doi:10.1038/nature05601

    CAS  PubMed  Google Scholar 

  • Giocomo LM, Hasselmo ME (2008) Time constants of h current in layer ii stellate cells differ along the dorsal to ventral axis of medial entorhinal cortex. J Neurosci 28(38):9414–25. doi:10.1523/JNEUROSCI.3196-08.2008

    CAS  PubMed Central  PubMed  Google Scholar 

  • Giocomo LM, Zilli EA, Fransén E, Hasselmo ME (2007) Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science (New York, NY) 315(5819):1719–22. doi:10.1126/science.1139207

    CAS  Google Scholar 

  • Gothard KM, Skaggs WE, McNaughton BL (1996) Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J Neurosci 16(24):8027–8040

    CAS  PubMed  Google Scholar 

  • Gothard KM, Hoffman KL, Battaglia FP, McNaughton BL (2001) Dentate gyrus and ca1 ensemble activity during spatial reference frame shifts in the presence and absence of visual input. J Neurosci 21(18):7284–7292

    CAS  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(4):231–240

    PubMed  Google Scholar 

  • Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052):801–6. doi:10.1038/nature03721

    CAS  PubMed  Google Scholar 

  • Hafting T, Fyhn M, Bonnevie T, Moser M-B, Moser EI (2008) Hippocampus-independent phase precession in entorhinal grid cells. Nature 453(7199):1248–52. doi:10.1038/nature06957

    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(4):369–79. doi:10.1002/1098-1063(2000)10:4<369::AID-HIPO3>3.0.CO;2–0

    CAS  PubMed  Google Scholar 

  • Hebb DO (1949) The organization of behavior: a neuropsychological theory. Wiley, New York

    Google Scholar 

  • Hetherington PA, Shapiro ML (1997) Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. Behav Neurosci 111(1):20–34

    CAS  PubMed  Google Scholar 

  • Hill AJ (1978) First occurrence of hippocampal spatial firing in a new environment. Exp Neurol 62(2):282–297

    CAS  PubMed  Google Scholar 

  • Hjorth-Simonsen A (1972) Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J Comp Neurol 146(2):219–232. doi:10.1002/cne.901460206

    CAS  PubMed  Google Scholar 

  • Hopfield JJ (1982) Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci U S A 79(8):2554–2558

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hopfield JJ (2010) Neurodynamics of mental exploration. Proc Natl Acad Sci U S A 107(4):1648–53. doi:10.1073/pnas.0913991107

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huxter JR, Senior TJ, Allen K, Csicsvari J (2008) Theta phase-specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat Neurosci 11(5):587–94. doi:10.1038/nn.2106

    CAS  PubMed  Google Scholar 

  • Itskov V, Pastalkova E, Mizuseki K, Buzsaki G, Harris KD (2008) Theta-mediated dynamics of spatial information in hippocampus. J Neurosci 28(23):5959–64. doi:10.1523/JNEUROSCI.5262-07.2008

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jander R (1957) Die optische Richungsorientierung der Roten Waldameise (Formica rufa L.). Z Vergl Physiol 40:162–238

    Google Scholar 

  • Jensen O, Lisman JE (1996) Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3(2–3):279–287

    CAS  PubMed  Google Scholar 

  • Jezek K, Henriksen EJ, Treves A, Moser EI, Moser M-B (2011) Theta-paced flickering between place-cell maps in the hippocampus. Nature 478(7368):246–9. doi:10.1038/nature10439

    CAS  PubMed  Google Scholar 

  • Jung MW, Wiener SI, McNaughton BL (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14(12):7347–7356

    CAS  PubMed  Google Scholar 

  • Kelemen E, Fenton AA (2010) Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. PLoS Biol 8(6):e1000403. doi:10.1371/journal.pbio.1000403

    PubMed Central  PubMed  Google Scholar 

  • Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, Muller RV (1998) Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280(5372):2121–2126

    CAS  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 (New York, NY) 332(6029):592–5. doi:10.1126/science.1201685

    CAS  Google Scholar 

  • Krupic J, Burgess N, O’Keefe J (2012) Neural representations of location composed of spatially periodic bands. Science 337(August):853–857

    CAS  PubMed  Google Scholar 

  • Kumar SS, Jin X, Buckmaster PS, Huguenard JR (2007) Recurrent circuits in layer II of medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 27(6):1239–46. doi:10.1523/JNEUROSCI.3182-06.2007

    CAS  PubMed  Google Scholar 

  • Las L, Ulanovsky N (2014) Hippocampal neurophysiology across species. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, Heidelberg

    Google Scholar 

  • Leutgeb S, Leutgeb JK (2014) Remapping to discriminate contexts with hippocampal population codes. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, Heidelberg

    Google Scholar 

  • Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser M-B (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science (New York, NY) 309(5734):619–23. doi:10.1126/science.1114037

    CAS  Google Scholar 

  • Leutgeb S, Leutgeb JK, Moser EI, Moser M-BB (2006) Fast rate coding in hippocampal CA3 cell ensembles. Hippocampus 16(9):765–774. doi:10.1002/hipo.20201

    PubMed  Google Scholar 

  • Maguire EA, Nannery R, Spiers HJ (2006) Navigation around London by a taxi driver with bilateral hippocampal lesions. Brain: A Journal of Neurology 129(Pt 11):2894–907. doi:10.1093/brain/awl286

    Google Scholar 

  • Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE (1994) Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4(4):410–421. doi:10.1002/hipo.450040404

    CAS  PubMed  Google Scholar 

  • Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15(11):7079–7094

    CAS  PubMed  Google Scholar 

  • Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262(841):23–81

    CAS  PubMed  Google Scholar 

  • Maurer AP, Vanrhoads SR, Sutherland GR, Lipa P, McNaughton BL (2005) Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus 15(7):841–852. doi:10.1002/hipo.20114

    PubMed  Google Scholar 

  • Maurer AP, Burke SN, Lipa P, Skaggs WE, Barnes CA (2012) Greater running speeds result in altered hippocampal phase sequence dynamics. Hippocampus 22(4):737–747. doi:10.1002/hipo.20936

    PubMed Central  PubMed  Google Scholar 

  • McDonald RJ, White NM (1993) A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci 107(1):3–22

    CAS  PubMed  Google Scholar 

  • McDonald RJ, White NM (1994) Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol 61(3):260–270

    CAS  PubMed  Google Scholar 

  • McDonald RJ, White NM (1995) Hippocampal and nonhippocampal contributions to place learning in rats. Behav Neurosci 109(4):579–593

    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 Comp Neurol 175(4):439–454. doi:10.1002/cne.901750404

    CAS  PubMed  Google Scholar 

  • McNaughton B, Barnes C, O’keefe J (1983) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 74(1):24–40

    Google Scholar 

  • McNaughton BL, Chen LL, Markus EJ (1991) “Dead reckoning”, landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J Cogn Neurosci 3(2):190–202

    CAS  PubMed  Google Scholar 

  • McNaughton B, Knierim J, Wilson M (1995) Vector encoding and the vestibular foundations of spatial cognition: neurophysiological and computational mechanisms. In: Gazzaniga MS (ed) The cognitive neurosciences. MIT Press, Cambridge, MA, pp 585–595

    Google Scholar 

  • McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Weaver KL (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199(Pt 1):173–185

    CAS  PubMed  Google Scholar 

  • McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B (2006) Path integration and the neural basis of the “cognitive map”. Nat Rev Neurosci 7(8):663–78. doi:10.1038/nrn1932

    CAS  PubMed  Google Scholar 

  • Mittelstaedt ML, Mittelstaedt H (1980) Homing by path integration in a mammal. Naturwissenschaften 67(11):566–567

    Google Scholar 

  • Morris RG, Garrud P, Rawlins JN, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297(5868):681–683

    CAS  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(7):1951–1968

    CAS  PubMed  Google Scholar 

  • Muller RU, Stead M, Pach J (1996) The hippocampus as a cognitive graph. J Gen Physiol 107(6):663–694

    CAS  PubMed Central  PubMed  Google Scholar 

  • Navratilova Z, Giocomo LM, Fellous J-M, Hasselmo ME, McNaughton BL (2012a) Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after-spike dynamics. Hippocampus 000(4):115–21. doi:10.1002/hipo.20939

    Google Scholar 

  • Navratilova Z, Hoang LT, Schwindel CD, Tatsuno M, McNaughton BL (2012b) Experience-dependent firing rate remapping generates directional selectivity in hippocampal place cells. Front Neural Circuits 6(February):6. doi:10.3389/fncir.2012.00006

    PubMed Central  PubMed  Google Scholar 

  • O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51(1):78–109

    PubMed  Google Scholar 

  • O’Keefe J (1990) A computational theory of the hippocampal cognitive map. Prog Brain Res 83:301–312

    PubMed  Google Scholar 

  • O’Keefe J (1991) An allocentric spatial model for the hippocampal cognitive map. Hippocampus 1(3):230–235. doi:10.1002/hipo.450010303

    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(7):853–866. doi:10.1002/hipo.20115

    PubMed Central  PubMed  Google Scholar 

  • O’Keefe J, Nadel 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(3):317–330. doi:10.1002/hipo.450030307

    PubMed  Google Scholar 

  • O’Keefe J, Speakman A (1987) Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68(1):1–27

    PubMed  Google Scholar 

  • Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9(5):1465–1472

    CAS  PubMed  Google Scholar 

  • Pearce JM, Roberts AD, Good M (1998) Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature 396(6706):75–77. doi:10.1038/23941

    CAS  PubMed  Google Scholar 

  • Pouget A, Sejnowski TJ (1997) Spatial transformations in the parietal cortex using basis functions. J Cogn Neurosci 9(2):222–237

    CAS  PubMed  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(6):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(5):1945–63

    CAS  PubMed  Google Scholar 

  • Redish AD, Touretzky DS (1997) Cognitive maps beyond the hippocampus. Hippocampus 7(1):15–35. doi:10.1002/(SICI)1098-1063(1997)7:1&lt;15::AID-HIPO3&gt;3.0.CO;2–6

    CAS  PubMed  Google Scholar 

  • Redish AD, McNaughton BL, Barnes CA (2000) Place cell firing shows an inertia-like process. Neurocomputing 32–33:235–241. doi:10.1016/S0925-2312(00)00169-7

    Google Scholar 

  • Remme MW, Lengyel M, Gutkin BS (2009) The role of ongoing dendritic oscillations in single-neuron dynamics. PLoS Comput Biol 5(9):e1000493. doi:10.1371/journal.pcbi.1000493

    PubMed Central  PubMed  Google Scholar 

  • Robinson DA (1989) Integrating with neurons. Annu Rev Neurosci 12:33–45. doi:10.1146/annurev.ne.12.030189.000341

    CAS  PubMed  Google Scholar 

  • Samsonovich A, McNaughton BL (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17(15):5900–5920

    CAS  PubMed  Google Scholar 

  • Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser M-B, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science (New York, NY) 312(5774):758–62. doi:10.1126/science.1125572

    CAS  Google Scholar 

  • Schmidt-Hieber C, Häusser M (2013) Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat Neurosci 16(3):325–31. doi:10.1038/nn.3340

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Sharp PE (1997) Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: comparison with hippocampal place cells. Behav Brain Res 85(1):71–92

    CAS  PubMed  Google Scholar 

  • Sharp PE, Kubie JL, Muller RU (1990) Firing properties of hippocampal neurons in a visually symmetrical environment: contributions of multiple sensory cues and mnemonic processes. J Neurosci 10(9):3093–3105

    CAS  PubMed  Google Scholar 

  • Skaggs WE, 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 

  • Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6(2):149–72. doi:10.1002/(SICI)1098-1063(1996)6:2&lt;149::AID-HIPO6&gt;3.0.CO;2-K

    CAS  PubMed  Google Scholar 

  • Solstad T, Moser EI, Einevoll GT (2006) From grid cells to place cells: a mathematical model. Hippocampus 16(12):1026–1031. doi:10.1002/hipo.20244

    PubMed  Google Scholar 

  • Stensola H, Stensola T, Solstad T (2012) The entorhinal grid map is discretized. Nature 492(7427):72–8. doi:10.1038/nature11649

    CAS  PubMed  Google Scholar 

  • Steward O (1976) Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167(3):285–314. doi:10.1002/cne.901670303

    CAS  PubMed  Google Scholar 

  • Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207. doi:10.1146/annurev.neuro.29.051605.112854

    CAS  PubMed  Google Scholar 

  • Terrazas A, Krause M, Lipa P, Gothard KM, Barnes CA, McNaughton BL (2005) Self-motion and the hippocampal spatial metric. J Neurosci 25(35):8085–96. doi:10.1523/JNEUROSCI.0693-05.2005

    CAS  PubMed  Google Scholar 

  • Touretzky DS, Redish AD (1996) Theory of rodent navigation based on interacting representations of space. Hippocampus 6(3):247–70. doi:10.1002/(SICI)1098-1063(1996)6:3&lt;247::AID-HIPO4&gt;3.0.CO;2-K

    CAS  PubMed  Google Scholar 

  • Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL (1996) Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6(3):271–80. doi:10.1002/(SICI)1098-1063(1996)6:1<9::AID-HIPO3>3.0.CO;2-M

    CAS  PubMed  Google Scholar 

  • Vann SD, Aggleton JP (2004) The mammillary bodies: two memory systems in one? Nat Rev Neurosci 5(1):35–44. doi:10.1038/nrn1299

    CAS  PubMed  Google Scholar 

  • Wallenstein GV, Hasselmo ME (1997) GABAergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect. J Neurophysiol 78(1):393–408

    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(45):16157–76. doi:10.1523/JNEUROSCI.0712-11.2011

    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(12):1283–300. doi:10.1002/hipo.20519

    PubMed  Google Scholar 

  • Widloski J, Fiete I (2014) Adult neurogenesis in the dentate gyrus. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, Heidelberg

    Google Scholar 

  • Wiener SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. J Neurosci 13(9):3802–3817

    CAS  PubMed  Google Scholar 

  • Wills TJ, Lever C, Cacucci F, Burgess N, O’Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science (New York, NY) 308(5723):873–6. doi:10.1126/science.1108905

    CAS  Google Scholar 

  • Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261(5124):1055–1058

    CAS  PubMed  Google Scholar 

  • Winter SS, Taube JS (2014) Head direction cells: from generation to integration. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, Heidelberg

    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(3):623–633

    CAS  PubMed  Google Scholar 

  • Yartsev M, Witter M, Ulanovsky N (2011) Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479(7371):103–107. doi:10.1038/nature10583

    CAS  PubMed  Google Scholar 

  • Yoganarasimha D, Rao G, Knierim JJ (2011) Lateral entorhinal neurons are not spatially selective in cue-rich environments. Hippocampus 21(12):1363–1374. doi:10.1002/hipo.20839

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16(6):2112–2126

    CAS  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(41):13850–60. doi:10.1523/JNEUROSCI.0547-10.2010

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zinyuk L, Kubik S, Kaminsky Y, Fenton AA, Bures J (2000) Understanding hippocampal activity by using purposeful behavior: place navigation induces place cell discharge in both task-relevant and task-irrelevant spatial reference frames. Proc Natl Acad Sci U S A 97(7):3771–6. doi:10.1073/pnas.050576397

    CAS  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

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Authors and Affiliations

  1. Canadian Centre for Behavioural Neuroscience, Lethbridge, AB, Canada

    Zaneta Navratilova & Bruce L. McNaughton

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  1. Zaneta Navratilova
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  2. Bruce L. McNaughton
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Correspondence to Zaneta Navratilova .

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  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

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Navratilova, Z., McNaughton, B.L. (2014). Models of Path Integration in the Hippocampal Complex. 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_8

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