Skip to main content
SpringerLink
Log in

Synaptic conditions for auto-associative memory storage and pattern completion in Jensen et al.’s model of hippocampal area CA3

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Jensen et al. (Learn Memory 3(2–3):243–256, 1996b) proposed an auto-associative memory model using an integrated short-term memory (STM) and long-term memory (LTM) spiking neural network. Their model requires that distinct pyramidal cells encoding different STM patterns are fired in different high-frequency gamma subcycles within each low-frequency theta oscillation. Auto-associative LTM is formed by modifying the recurrent synaptic efficacy between pyramidal cells. In order to store auto-associative LTM correctly, the recurrent synaptic efficacy must be bounded. The synaptic efficacy must be upper bounded to prevent re-firing of pyramidal cells in subsequent gamma subcycles. If cells encoding one memory item were to re-fire synchronously with other cells encoding another item in subsequent gamma subcycle, LTM stored via modifiable recurrent synapses would be corrupted. The synaptic efficacy must also be lower bounded so that memory pattern completion can be performed correctly. This paper uses the original model by Jensen et al. as the basis to illustrate the following points. Firstly, the importance of coordinated long-term memory (LTM) synaptic modification. Secondly, the use of a generic mathematical formulation (spiking response model) that can theoretically extend the results to other spiking network utilizing threshold-fire spiking neuron model. Thirdly, the interaction of long-term and short-term memory networks that possibly explains the asymmetric distribution of spike density in theta cycle through the merger of STM patterns with interaction of LTM network.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbott, L. F., & Nelson, S. B. (2000). Synaptic plasticity: Taming the beast. Nature Neuroscience, 3, 1178–1183.

    Article  PubMed  CAS  Google Scholar 

  • Alonso, A., Gaztelu, J. M., Bun̋o, W., & García-Austt, E. (1987). Cross-correlation analysis of septohippocampal neurons during theta-rhythm. Brain Research, 413(1), 135–146.

    Article  PubMed  CAS  Google Scholar 

  • Araneda, R., & Andrade, R. (1991). 5-hydroxytryptamine2 and 5-hydroxytryptamine1a receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience, 40(2), 399–412.

    Article  PubMed  CAS  Google Scholar 

  • Bliss, T. V. P., Collingridge, G., & Morris, R. (2007). Synaptic Plasticity in the Hippocampus (chap 10, pp. 343–474). Oxford University Press

  • Bragin, A., Jando, G., Nadasdy, Z., Hetke, J., Wise, K., & Buzsaki, G. (1995). Gamma (40–100 hz) oscillation in the hippocampus of the behaving rat. The Journal of Neuroscience, 15(1), 47–60.

    PubMed  CAS  Google Scholar 

  • Bush, D., Philippides, A., Husbands, P., & O’Shea, M. (2010). Dual coding with stdp in a spiking recurrent neural network model of the hippocampus. PLoS Comput Biol 6(7), e1000,839.

    Article  Google Scholar 

  • Caillard, O., & Debanne, D. (2010). Cell-specific contribution to gamma oscillations. The Journal of Physiology, 588(5), 751–751.

    Article  PubMed  CAS  Google Scholar 

  • Cantero, J. L., Atienza, M., Stickgold, R., Kahana, M. J., Madsen, J. R., & Kocsis, B. (2003). Sleep-dependent θ oscillations in the human hippocampus and neocortex. The Journal of Neuroscience, 23(34), 10,897–10,903.

    PubMed  CAS  Google Scholar 

  • Cutsuridism, V., Cobb, S., Graham, B. P. (2010). Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus, 20(3), 423–446.

    Google Scholar 

  • Cutsuridis, V., & Wennekers, T. (2009). Hippocampus, microcircuits and associative memory. Neural Networks, 22(8), 1120–1128.

    Article  PubMed  Google Scholar 

  • de Almeida, L., Idiart, M., & Lisman, J. E. (2007). Memory retrieval time and memory capacity of the CA3 network: Role of gamma frequency oscillations. Learning & Memory, 14(11), 795–806.

    Article  Google Scholar 

  • Forsythe, I. D., & Westbrook, G. L. (1988). Slow excitatory postsynaptic currents mediated by n-methyl-d-aspartate receptors on cultured mouse central neurones. The Journal of Physiology, 396(1), 515–533.

    PubMed  CAS  Google Scholar 

  • Gerstner, W., & Kistler, W. M. (2002). Spiking neuron models: Single neurons, populations, plasticity. New York: Cambridge University Press.

    Book  Google Scholar 

  • Hájos, N., & Paulsen, O. (2009). Network mechanisms of gamma oscillations in the CA3 region of the hippocampus. Neural Networks, 22(8), 1113–1119.

    Article  PubMed  Google Scholar 

  • Hasselmo, M. E., Bodelon, C., & Wyble, B. P. (2002). A proposed function for hippocampal theta rhythm: Separate phases of encoding and retrieval enhance reversal of prior learning. Neural Computation, 14(4), 793–817.

    Article  PubMed  Google Scholar 

  • Hughes, J. R. (2008). Gamma, fast, and ultrafast waves of the brain: Their relationships with epilepsy and behavior. Epilepsy & Behavior, 13(1), 25–31.

    Article  Google Scholar 

  • Hunter, R., Cobb, S., & Graham, B. (2008). Improving associative memory in a network of spiking neurons. In Artificial neural networks - ICANN 2008 (vol. 5164, pp. 636–645). Springer Berlin/Heidelberg

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

    Article  CAS  Google Scholar 

  • Jensen, O., & Lisman, J. E. (1996b). Novel lists of 7 + / − 2 known items can be reliably stored in an oscillatory short-term memory network: Interaction with long-term memory. Learning & Memory, 3, (2–3), 257–263.

    Article  CAS  Google Scholar 

  • Jensen, O., & Lisman, J. E. (1996c). Theta/gamma networks with slow nmda channels learn sequences and encode episodic memory: Role of NMDA channels in recall. Learning & Memory, 3(2–3), 264–278

    Article  CAS  Google Scholar 

  • Jensen, M. S., Azouz, R., & Yaari, Y. (1996a). Spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. The Journal of Physiology, 492(Pt 1), 199–210.

    PubMed  CAS  Google Scholar 

  • Jensen, O., Idiart, M. A., & Lisman, J. E. (1996b). Physiologically realistic formation of autoassociative memory in networks with theta/gamma oscillations: Role of fast NMDA channels. Learning & Memory, 3(2–3), 243–256.

    Article  CAS  Google Scholar 

  • Koene, R. A., & Hasselmo M. E. (2007). First-in-first-out item replacement in a model of short-term memory based on persistent spiking. Cerebral Cortex, 17(8), 1766–1781.

    Article  PubMed  Google Scholar 

  • Kunec, S., Hasselmo, M. E., & Kopell, N. (2005). Encoding and retrieval in the CA3 region of the hippocampus: A model of theta-phase separation. Journal of Neurophysiology, 94(1), 70–82.

    Article  PubMed  Google Scholar 

  • Lisman, J., & Idiart, M. (1995). Storage of 7 +/- 2 short-term memories in oscillatory subcycles. Science, 267(5203), 1512–1515.

    Article  PubMed  CAS  Google Scholar 

  • Maass, W., & Bishop, C. M. (Eds.), (1998). Pulsed neural networks. Cambridge, MA, USA: MIT Press.

    Google Scholar 

  • Mann, E. O., Radcliffe, C. A., & Paulsen, O. (2005). Hippocampal gamma-frequency oscillations: From interneurones to pyramidal cells, and back. The Journal of Physiology, 562(1), 55–63.

    Article  PubMed  CAS  Google Scholar 

  • Marr, D. (1971). Simple memory: A theory for archicortex. Philosophical Transactions of the Royal Society of London B, Biological Sciences, 262(841), 23–81.

    Article  CAS  Google Scholar 

  • Miles, R. (1990). Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. The Journal of Physiology, 428(1), 61–77.

    PubMed  CAS  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(2), 267–280.

    Article  PubMed  CAS  Google Scholar 

  • Neves, G., Cooke, S. F., Bliss, T. V. P. (2008). Synaptic plasticity, memory and the hippocampus: A neural network approach to causality. Nature Reviews Neuroscience, 9(1), 65–75.

    Article  PubMed  CAS  Google Scholar 

  • Ozawa, S., Kamiya, H., & Tsuzuki, K. (1998). Glutamate receptors in the mammalian central nervous system. Progress in Neurobiology, 54(5), 581–618.

    Article  PubMed  CAS  Google Scholar 

  • Park, J. Y., Remy, S., Varela, J., Cooper, D. C., Chung, S., Kang, H. W., et al. (2010). A post-burst afterdepolarization is mediated by group I metabotropic glutamate receptor-dependent upregulation of Cav2.3 R-type calcium channels in CA1 pyramidal neurons. PLoS Biology, 8(11), e1000,534.

    Article  Google Scholar 

  • Rajji, T., Chapman, D., Eichenbaum, H., & Greene, R. (2006). The role of CA3 hippocampal NMDA receptors in paired associate learning. The Journal of Neuroscience, 26(3), 908–915.

    Article  PubMed  CAS  Google Scholar 

  • Rolls, E. T. (2008). Computational models of hippocampal functions. In J. H. Byrne (Ed.), Learning and memory: A comprehensive reference (pp. 641–665). Oxford: Academic Press.

    Chapter  Google Scholar 

  • Rolls E. T. (2010). A computational theory of episodic memory formation in the hippocampus. Behavioural Brain Research, 215(2), 180–196.

    Article  PubMed  Google Scholar 

  • Rutishauser, U., Ross, I. B., Mamelak, A. N., & Schuman, E. M. (2010). Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464(7290), 903–907.

    Article  PubMed  CAS  Google Scholar 

  • Samura, T., Hattori, M., & Ishizaki, S. (2007). Autoassociative and heteroassociative hippocampal CA3 model based on location dependencies derived from anatomical and physiological findings. International Congress Series 1301, 140–143.

    Article  Google Scholar 

  • Sik, A., Penttonen, M., Ylinen, A., & Buzsaki, G. (1995). Hippocampal CA1 interneurons: an in vivo intracellular labeling study. The Journal of Neuroscience, 15(10), 6651–6665.

    PubMed  CAS  Google Scholar 

  • Skaggs, W. E., McNaughton, B. L., Wilson M. A., & Barnes C. A. (1996). Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus, 6(2), 149–172.

    Article  PubMed  CAS  Google Scholar 

  • Sommer, F. T., & Wennekers, T. (2001). Associative memory in networks of spiking neurons. Neural Networks, 14(6–7), 825–834

    Article  PubMed  CAS  Google Scholar 

  • Stern, P., Edwards, F. A., & Sakmann, B. (1992). Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. The Journal of Physiology, 449(1), 247–278.

    PubMed  CAS  Google Scholar 

  • Storm, J. F. (1989). An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. The Journal of Physiology, 409(1), 171–190.

    PubMed  CAS  Google Scholar 

  • Tan, C. H., Cheu, E. Y., Hu, J., Yu, Q., & Tang, H. (2011). Associative memory model of hippocampus CA3 using spike response neurons. In International conference on neural information processing (pp. 493–500).

  • Vanderwolf, C. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalography and Clinical Neurophysiology, 26(4), 407–418.

    Article  PubMed  CAS  Google Scholar 

  • Wagatsuma, H., & Yamaguchi, Y. (2004). Cognitive map formation through sequence encoding by theta phase precession. Neural Computation, 16(12), 2665–2697.

    Article  PubMed  Google Scholar 

  • Wagatsuma, H., & Yamaguchi, Y. (2007). Neural dynamics of the cognitive map in the hippocampus. Cognitive Neurodynamics, 1(2), 119–141.

    Article  PubMed  Google Scholar 

  • Yamaguchi, Y., Aota, Y., McNaughton, B. L., & Lipa, P. (2002). Bimodality of theta phase precession in hippocampal place cells in freely running rats. Journal of Neurophysiology, 87(6), 2629–2642.

    PubMed  Google Scholar 

  • Yamaguchi, Y., Sato, N., Wagatsuma, H., Wu, Z., Molter, C., & Aota, Y. (2007). A unified view of theta-phase coding in the entorhinal-hippocampal system. Current Opinion in Neurobiology, 17(2), 197–204.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Agency for Science, Technology and Research (A*STAR), Singapore under SERC Grant 092 157 0130.

Author information

Authors and Affiliations

  1. Institute for Infocomm Research, Agency for Science Technology and Research (A*STAR), Singapore, Singapore

    Eng Yeow Cheu, Jiali Yu, Chin Hiong Tan & Huajin Tang

Authors
  1. Eng Yeow Cheu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiali Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chin Hiong Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huajin Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Action Editor: Alessandro Treves

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cheu, E.Y., Yu, J., Tan, C.H. et al. Synaptic conditions for auto-associative memory storage and pattern completion in Jensen et al.’s model of hippocampal area CA3. J Comput Neurosci 33, 435–447 (2012). https://doi.org/10.1007/s10827-012-0394-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-012-0394-8

Keywords

Search

Navigation