Skip to main content
Log in

Neural dynamics of the cognitive map in the hippocampus

  • Original Paper
  • Published:
Cognitive Neurodynamics Aims and scope Submit manuscript

Abstract

The rodent hippocampus has been thought to represent the spatial environment as a cognitive map. In the classical theory, the cognitive map has been explained as a consequence of the fact that different spatial regions are assigned to different cell populations in the framework of rate coding. Recently, the relation between place cell firing and local field oscillation theta in terms of theta phase precession was experimentally discovered and suggested as a temporal coding mechanism leading to memory formation of behavioral sequences accompanied with asymmetric Hebbian plasticity. The cognitive map theory is apparently outside of the sequence memory view. Therefore, theoretical analysis is necessary to consider the biological neural dynamics for the sequence encoding of the memory of behavioral sequences, providing the cognitive map formation. In this article, we summarize the theoretical neural dynamics of the real-time sequence encoding by theta phase precession, called theta phase coding, and review a series of theoretical models with the theta phase coding that we previously reported. With respect to memory encoding functions, instantaneous memory formation of one-time experience was first demonstrated, and then the ability of integration of memories of behavioral sequences into a network of the cognitive map was shown. In terms of memory retrieval functions, theta phase coding enables the hippocampus to represent the spatial location in the current behavioral context even with ambiguous sensory input when multiple sequences were coded. Finally, for utilization, retrieved temporal sequences in the hippocampus can be available for action selection, through the process of reverting theta rhythm-dependent activities to information in the behavioral time scale. This theoretical approach allows us to investigate how the behavioral sequences are encoded, updated, retrieved and used in the hippocampus, as the real-time interaction with the external environment. It may indeed be the bridge to the episodic memory function in human hippocampus.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abbott LF, Blum KI (1996) Functional significance of long-term potentiation for sequence learning and prediction. Cerebral Cortex 6:406–416

    Article  PubMed  CAS  Google Scholar 

  • Amari S (1977) Dynamics of pattern formation in lateral-inhibition type neural fields. Biol Cybernet 27(2):77–87

    Article  CAS  Google Scholar 

  • Amit DJ, Tsodyks MV (1992) Effective neurons and attractor neural networks in cortical environment. Network: Comput Neural Syst 3(2):121–137

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18(24):10464–10472

    PubMed  CAS  Google Scholar 

  • Blum KI, Abbott LF (1996) A model of spatial map formation in the hippocampus of the rat. Neural Comput 8(1):85–93

    PubMed  CAS  Google Scholar 

  • Bose A, Recce M (2001) Phase precession and phase-locking of hippocampal pyramidal cells. Hippocampus 11(3):204–215

    Article  PubMed  CAS  Google Scholar 

  • Bostock E, Muller RU, Kubie JL (1991) Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1(2):193–205

    Article  PubMed  CAS  Google Scholar 

  • Bower M, Euston D, Roop R, Gebara N, McNaughton BL (2002) How an ambiguous sequence is learned determines how the hippocampus encodes it. Society for Neuroscience Abstract 28(678.13)

  • Bower MR, Euston DR, McNaughton BL (2005) Sequential-context-dependent hippocampal activity is not necessary to learn sequences with repeated elements. J Neurosci 25(6):1313–1323

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Czurko A, Hirase H, Csicsvari J, Buzsáki G (1999) Sustained activation of hippocampal pyramidal cells by ‹space clamping’ in a running wheel. Eur J Neurosci 11(1):344–352

    Article  PubMed  CAS  Google Scholar 

  • Eichenbaum H, Kuperstein M, Fagan A, Nagode J (1987) Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task. J Neurosci 7(3):716–732

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Eichenbaum H (2001) The hippocampus and declarative memory: cognitive mechanisms and neural codes. Behav Brain Res 127(1–2):199–207

    Article  PubMed  CAS  Google Scholar 

  • Ekstrom AD, Meltzer J, McNaughton BL, Barnes CA (2001) NMDA receptor antagonism blocks experience-dependent expansion of hippocampal “place fields”. Neuron 31(4):631–638

    Article  PubMed  CAS  Google Scholar 

  • Ferbinteanu J, Shapiro ML (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40:1227–1239

    Article  PubMed  CAS  Google Scholar 

  • FitzHugh R (1961) Impulses and physiological states in theoretical models of nerve membrane. Biophys J 1:501–507

    Article  Google Scholar 

  • Fitzsimonds RM, Song HJ, Poo MM (1997) Propagation of activity-dependent synaptic depression in simple neural networks. Nature 388:439–448

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fukai T (1999) Sequence generation in arbitrary temporal patterns from theta-nested gamma oscillations: a model of the basal ganglia-thalamo-cortical loops. Neural Networks 12(7–8):975–987

    Article  PubMed  Google Scholar 

  • Gerstner W, Abbott LF (1997) Learning navigational maps through potentiation and modulation of hippocampal place cells. J Comput Neurosci 4(1):79–94

    Article  PubMed  CAS  Google Scholar 

  • Gorchetchnikov A, Hasselmo ME (2002) A model of hippocampal circuitry mediating goal-driven navigation in a familiar environment. Neurocomputing 44–46:423–427

    Article  Google Scholar 

  • Gothard KM, Skaggs WE, Moore KM, McNaughton BL (1996) Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J␣Neurosci 16(2):823–835

    PubMed  CAS  Google Scholar 

  • Hafting T, Fyhn MH, Molden S, Moser MB, Moser EI (2005) Topographic organization of a spatial map in the entorhinal cortex. Society for Neuroscience Abstract 31(198.3)

  • Hafting T, Fyhn MH, Moser MB, Moser EI (2006) Phase precession and phase locking in entorhinal grid cells. Society for Neuroscience Abstract 32(68.8)

  • Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurko A, Buzsáki G (2002) Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417(6890):738–741

    Article  PubMed  CAS  Google Scholar 

  • Hasselmo ME, Schnell E (1994) Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14(6):3898–3914

    PubMed  CAS  Google Scholar 

  • Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3(9):351–359

    Article  PubMed  Google Scholar 

  • Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (2002a) Neuromodulation, theta rhythm and rat spatial navigation. Neural Networks 15(4–6):689–707

    Article  Google Scholar 

  • Hasselmo ME, Cannon RC, Koene RA (2002b) A simulation of parahippocampal and hippocampal structures guiding spatial navigation of a virtual rat in a virtual environment: a functional framework for theta theory. In: Witter MP, Wouterlood FG (eds) The parahippocampal region: organization and role in cognitive function. Oxford University Press, Oxford

    Google Scholar 

  • Hasselmo ME, Bodelon C, Wyble BP (2002c) A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14(4):793–817

    Article  Google Scholar 

  • Hoppensteadt FC (1986) An introduction to the mathematics of neurons. Cambridge University Press, New York

    Google Scholar 

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

    CAS  Google Scholar 

  • Káli S, Dayan P (2000) The involvement of recurrent connections in area CA3 in establishing the properties of place fields: a model. J Neurosci 20(19):7463–7477

    PubMed  Google Scholar 

  • Kamondi A, Acsády L, Wang XJ, Buzsáki G (1998) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8(3):244–261

    Article  PubMed  CAS  Google Scholar 

  • Koene RA, Gorchetchnikov A, Cannon RC, Hasselmo ME (2003) Modeling goal-directed spatial navigation in the rat based on physiological data from the hippocampal formation. Neural Network 16(5–6):577–584

    Article  Google Scholar 

  • Larson J, Lynch G (1989) Theta pattern stimulation and the induction of LTP: the sequence in which synapses are stimulated determines the degree to which they potentiate. Brain Res 489(1):49–58

    Article  PubMed  CAS  Google Scholar 

  • Lenck-Santini PP, Save E, Poucet B (2001) Place-cell firing does not depend on the direction of turn in a Y-maze alternation task. Eur J Neurosci 13(5):1055–1058

    Article  PubMed  CAS  Google Scholar 

  • Lengyel M, Szatmáry Z, Érdi P (2003) Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13(6):700–714

    Article  PubMed  Google Scholar 

  • Levy WB, Steward O (1983) Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8(4):791–797

    Article  PubMed  CAS  Google Scholar 

  • Levy WB (1996) A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 6(6):579–590

    Article  PubMed  CAS  Google Scholar 

  • Lisman JE, Idiart MA (1995) Storage of 7 2 short-term memories in oscillatory subcycles. Science 267:1512–1515

    Article  PubMed  CAS  Google Scholar 

  • Magee JC (2001) Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons. J Neurophysiol 86(1):528–532

    PubMed  CAS  Google Scholar 

  • Magee JC (2003) A prominent role for intrinsic neuronal properties in temporal coding. Trends Neurosci 26(1):14–16

    Article  PubMed  CAS  Google Scholar 

  • Marr D (1971) Simple memory: a theory for archicortex. Phil Trans Roy Soc London Ser B; Biol Sci 262(841):23–81

    CAS  Google Scholar 

  • Mehta MR, Barnes CA, McNaughton BL (1997) Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci 94(16):8918–8921

    Article  PubMed  CAS  Google Scholar 

  • Mehta MR, Lee AK, Wilson MA (2002) Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417(6890):741–746

    Article  PubMed  CAS  Google Scholar 

  • Melamed O, Gerstner W, Maass W, Tsodyks M, Markram H (2004) Coding and learning of behavioral sequences. Trends Neurosci 27(1):11–14

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • McNaughton BL (1989) Neuronal mechanisms for spatial computation and information storage. In: Nadel L, Cooper L, Culicover P, Harnish RM (eds) Neural connections, mental computation. MIT Press, Cambridge, MA, pp 285–350

    Google Scholar 

  • McNaughton BL, Nadel L (1989) Hebbian–Marr networks and the neurobiological representation of action in space. In: Gluck MA, Rumelhart DE (eds) Neuroscience and connectionist theory. Lawrence Erlbaum Associates, Hillsdale, pp␣1–63

    Google Scholar 

  • McNaughton BL (1996) Cognitive cartography. Nature 381:368–369

    Article  PubMed  CAS  Google Scholar 

  • McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‹cognitive map’. Nat Rev Neurosci 7(8):663–678

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Muller RU, Kubie JL, Saypoff R (1991) The hippocampus as a cognitive graph (abridged version). Hippocampus 1(3):243–246

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, Sun LD, Kato A, Carr CA, Johnston D, Wilson MA, Tonegawa S (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297:211–218

    Article  PubMed  CAS  Google Scholar 

  • Nakazawa K, Sun LD, Quirk MC, Rondi-Reig L, Wilson MA, Tonegawa S (2003) Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38(2):305–315

    Article  PubMed  CAS  Google Scholar 

  • Nagumo JS, Arimato S, Yoshizawa S (1962) An active spike transmission line simulating a nerve axon. Proc IRE 50:2061–2070

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Piaget J (1928) Judgement and reasoning in the child. Harcourt, Brace and World, New York, 1928

  • Redish AD, Touretzky DS (1998) The role of the hippocampus in solving the Morris water maze. Neural Comput 10(1):73–111

    Article  PubMed  CAS  Google Scholar 

  • Redish AD (1999) Beyond the cognitive map., The MIT Press, Cambridge

    Google Scholar 

  • Rolls ET (1989) The representation and storage of information in neuronal networks in the primate cerebral cortex and hippocampus. In: Durbin R, Miall C, Mitchison G (eds) The computing neuron. Addison-Wesley, Workingham, UK, pp 125–159

    Google Scholar 

  • Rolls ET, Stringer SM, Trappenberg TP (2002) A unified model of spatial and episodic memory. Proc Roy Soc B: Biol Sci 269(1496):1087–1093

    Article  Google Scholar 

  • Rosenzweig AD, Ekstrom AD, Redish AD, McNaughton BL, Barnes CA (2000) Phase precession as an experience-independent process: hippocampal pyramidal cell phase precession in a novel environment and under NMDA-receptor blockade. Society for Neuroscience Abstract 26(982)

  • Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69(3):143–179

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Sato N, Yamaguchi Y (2003) Memory encoding by theta phase precession in the hippocampal network. Neural Comput 15(10):2379–2397

    Article  PubMed  Google Scholar 

  • Sato N, Yamaguchi Y (2005) Online formation of a hierarchical cognitive map for object-place association by theta phase coding. Hippocampus 15(7):963–978

    Article  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):149–172

    Article  PubMed  CAS  Google Scholar 

  • Sohal VS, Hasselmo ME (1998) GABA(B) modulation improves sequence disambiguation in computational models of hippocampal region CA3. Hippocampus 8(2):171–193

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Trullier O, Meyer JA (2000) Animat navigation using a cognitive graph. Biol Cybernet 83(3):271–285

    Article  CAS  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):271–280

    Article  PubMed  CAS  Google Scholar 

  • Tulving E (1972) Episodic and semantic memory. In: Tulving E, Donaldson W (eds) Organization of memory. Academic Press, New York

    Google Scholar 

  • Wagatsuma H, Yamaguchi Y (1999) A neural network model self-organizing a cognitive map using theta phase precession. Proceedings of SMC’99, Tokyo, Japan, III, pp 199–204

  • Wagatsuma H, Yamaguchi Y (2000) Self-organization of the cognitive map in a neural network model using theta phase precession. Society for Neuroscience Abstract 26(1589)

  • Wagatsuma H, Yamaguchi Y (2004) Cognitive map formation through sequence encoding by theta phase precession. Neural Comput 16:2665–2697

    Article  PubMed  Google Scholar 

  • Wagatsuma H, Yamaguchi Y (2005) Disambiguation of multiple sequence learning by theta phase coding. Brain Neural Networks 12:17–31 (in Japanese)

    Google Scholar 

  • Wagatsuma H (2005) A theory of the cognitive map formation in the hippocampus by using theta phase coding, Doctoral thesis, Tokyo Denki University

  • Wagatsuma H, Yamaguchi Y (2006) Disambiguation in spatial navigation with theta phase coding. Neurocomputing 69:1228–1232

    Article  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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Wu Z, Yamaguchi Y (2004) Input-dependent learning rule for the memory of spatiotemporal sequences in hippocampal network with theta phase precession. Biol Cybernet 90(2):113–124

    Article  Google Scholar 

  • Yamaguchi Y, McNaughton BL (1998) Nonlinear dynamics generating theta phase precession in hippocampal closed circuit and generation of episodic memory. Proceedings of ICONIP98, Kitakyushu, Japan, vol 2, pp 781–784

  • Yamaguchi Y (2003) A theory of hippocampal memory based on theta phase precession. Biol Cybernet 89(1):1–9

    Google Scholar 

  • Yamaguchi Y, Aota Y, Sato N, Wagatsuma H, Wu Z (2004) Synchronization of neural oscillations as a possible mechanism underlying episodic memory: a study of theta rhythm in the hippocampus. J Integrative Neurosci 3(2):143–157

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroaki Wagatsuma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wagatsuma, H., Yamaguchi, Y. Neural dynamics of the cognitive map in the hippocampus. Cogn Neurodyn 1, 119–141 (2007). https://doi.org/10.1007/s11571-006-9013-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-006-9013-6

Keywords

Navigation