Skip to main content

Advertisement

Log in

A Context-Sensitive Mechanism in Hippocampal CA1 Networks

  • Original Article
  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

This paper presents a possible context-sensitive mechanism in a neural network and at single neuron levels based on the experiments of hippocampal CA1 and their theoretical models. First, the spatiotemporal learning rule (STLR, non-Hebbian) and the Hebbian rule (HEBB) are experimentally shown to coexist in dendrite–soma interactions in single hippocampal pyramidal cells of CA1. Second, the functional differences between STLR and HEBB are theoretically shown in pattern separation and pattern completion. Third, the interaction between STLR and HEBB in neural levels is proposed to play an important role in forming a selective context determined by value information, which is related to expected reward and behavioral estimation.

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

  • Aihara, T., Tsukada, M., Crair, M. C., & Sinomoto, S. (1997). Stimulus-dependent induction of long-term potentiation in CA1 area of the hippocampus: experiment and model. Hippocampus, 7, 416–426.

    Article  Google Scholar 

  • Aihara, T., Kobayashi, Y., Matsuda, H., Sasaki, H., & Tsukada, M. (1998). Optical imaging of LTP and LTD induced simultaneously by temporal stimulus in hippocampal CA1 area. Soc. Neurosci. Abstr., 24, 1070.

    Google Scholar 

  • Aihara, T., Tsukada, M., & Matsuda, H. (2000). Two dynamic processes for the induction of long-term in hippocampal CA1 neurons. Biol. Cybern., 82, 189–195.

    Article  MATH  Google Scholar 

  • Bi, G., & Poo, M. (1998). Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic type. J. Neurosci., 18, 10464–10472.

    Google Scholar 

  • Bland, B. H., Jackson, J., Derrie-Gillespie, D., Azad, T., Rickhi, A., & Abriam, J. (2006). Amplitude, frequency, and phase analysis of hippocampal theta during sensorimotor processing in a jump avoidance task. Hippocampus, 16, 673–681.

    Article  Google Scholar 

  • Bliss, T. P., & Lømo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of perforant path. J. Physiol., 232, 331–356.

    Google Scholar 

  • Boettiger, C. A., & Doupe, A. J. (2001). Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron, 31, 809–818.

    Article  Google Scholar 

  • Buzsaki, G., Leung, L., & Vanderwolf, C. H. (1983). Cellular bases of hippocampal EEG in the behaving rat. Brain Res. Rev., 6, 169–171.

    Article  Google Scholar 

  • Csicsvari, J., Jamieson, B., Wise, K. D., & Buzsaki, G. (2003). Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron, 37, 311–322.

    Article  Google Scholar 

  • Debanne, D., & Thompson, S. M. (1998). Associative long-term depression in the hippocampus in vitro. Hippocampus, 6, 9–16.

    Article  Google Scholar 

  • Feldman, D. E. (2000). Timing based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron, 27, 45–56.

    Article  Google Scholar 

  • Fregnac, Y., & Shulz, D. (1994). Models of synaptic plasticity and cellular analogs of learning in the developing and adult vertebrate visual cortex. In Casagrande, V., & Shinkman, P. (Eds.), Advances in neural and behavioral development (pp. 149–235). Norwood: Ablex.

    Google Scholar 

  • Froemke, R. C., & Dan, Y. (2002). Spike-timing-dependent synaptic modification induced by natural spike trains. Nature, 416, 433–438.

    Article  Google Scholar 

  • Fukushima, Y., Tsukada, M., Tsuda, I., Yamaguti, Y., & Kuroda, S. (2007). Spatial clustering property and its self-similarity in membrane potentials of hippocampal CA1 pyramidal neurons for a spatiotemporal input sequence. Cogn. Neurodyn., 1, 305–316.

    Article  Google Scholar 

  • Golding, N. L., Staff, N. P., & Spruston, N. (2002). Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature, 418, 326–331.

    Article  Google Scholar 

  • Hasselmo, M. (1999). Neuromodulation: Acetylcholine and memory consolidation. Trends Cogn. Sci., 3, 351–359.

    Article  Google Scholar 

  • Hasselmo, M. (2006). The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol., 16, 710–715.

    Article  Google Scholar 

  • Hebb, D. O. (1949). The organization of behavior. New York: Wiley.

    Google Scholar 

  • Ihalainen, J. A., Riekkinen, P. J., & Feenstra, M. G. (1999). Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis. Neurosci. Lett., 277, 71–74.

    Article  Google Scholar 

  • Kay, J., & Phillips, W. A. (1997). Activation functions, computational goals and learning rules for local processors with contextual guidance. Neural Comput., 9, 895–910.

    Article  Google Scholar 

  • Li, S., Cullen, W. K., Anwyl, R., & Rowan, M. J. (2003). Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat. Neurosci., 6, 526–531.

    Google Scholar 

  • Lisman, J. E. (1989). A mechanism for Hebb and the anti-Hebb processes underlying learning and memory. Proc. Natl. Acad. Sci. USA, 86, 9574–9578.

    Article  Google Scholar 

  • Lisman, J. E., & Grace, A. A. (2005). The hippocampal-VTA loop: Controlling the entry of information into long-term memory. Neuron, 46, 703–713.

    Article  Google Scholar 

  • Magee, J. C., & Johnston, D. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science, 275, 209–213.

    Article  Google Scholar 

  • Markram, H., Lubke, J., Frotscher, M., & Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213–215.

    Article  Google Scholar 

  • Nakazawa, K., Quirk, M. C., Chitwood, R. A., Watanabe, M., Yeckel, M. F., Sun, L. D., Kato, A., Carr, C. A., Johnston, D., Wilson, M. A., & Tonegawa, S. (2002). Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science, 297, 211–218.

    Article  Google Scholar 

  • Reynolds, J. N., & Wickens, J. R. (2002). Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw., 15, 507–521.

    Article  Google Scholar 

  • Sainsbury, R. S., Heynen, A., & Montoya, C. P. (1987). Behavioral correlates of hippocampal type 2 theta in the rat. Physiol. Behav., 39, 513–519.

    Article  Google Scholar 

  • Scheiderer, C. L., Smith, C. C., McCutchen, E., McCoy, P. A., Thacker, E. E., Kolasa, K., Dobrunz, L. E., & McMahon, L. L. (2008). Coactivation of M(1) muscarinic and alpha1 adrenergic receptors stimulates extracellular signal-regulated protein kinase and induces long-term depression at CA3-CA1 synapses in rat hippocampus. J. Neurosci., 28, 5350–5358.

    Article  Google Scholar 

  • Shinoe, T., Matsui, M., Taketo, M., & Manabe, T. (2005). Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J. Neurosci., 25, 11194–11200.

    Article  Google Scholar 

  • Sjöström, P. J., Turrigiano, G. G., & Nelson, S. B. (2001). Rate timing and cooperativity jointly determine cortical synaptic plasticity. Neuron, 32, 1149–1164.

    Article  Google Scholar 

  • Sourdet, V., & Debanne, D. (1999). The role of dendritic. Filtering in associative long-term synaptic. Plasticity Learn. Mem., 6, 422–447.

    Article  Google Scholar 

  • Stegeren, A. H. (2008). The role of the noradrenergic system in emotional memory. Acta Psychol. (Amst.), 127, 532–541.

    Article  Google Scholar 

  • Takahashi, M., Lauwereyns, J., Sakurai, Y., & Tsukada, M. (2009). A code for spatial alternation during fixation in rat hippocampal CA1 neurons. J. Neurophysiol., 102, 556–567.

    Article  Google Scholar 

  • Thomas, M. J., Watabe, A. M., Moody, T. D., Makhinson, M., & O’Dell, T. J. (1998). Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation. J. Neurosci., 18, 7118–7126.

    Google Scholar 

  • Tsubokawa, H., & Ross, W. M. (1997). Muscarinic modulation of spike back-propagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J. Neurosci., 17, 5782–5791.

    Google Scholar 

  • Tsuda, I. (1996). A new type of self-organization associated with chaotic dynamics in neural networks. Int. J. Neural Syst., 7, 451–459.

    Article  Google Scholar 

  • Tsuda, I. (2001). Toward an interpretation of dynamic neural activity in terms of chaotic dynamical systems. Behav. Brain Sci., 24, 793–847.

    Article  Google Scholar 

  • Tsukada, M., Aihara, T., Mizuno, M., Kato, H., & Ito, K. (1994). Temporal pattern sensitivity of long-term potentiation in hippocampal CA1 neurons. Biol. Cybern., 70, 495–503.

    Article  Google Scholar 

  • Tsukada, M., Aihara, T., Saito, H., & Kato, H. (1996). Hippocampal LTP depends on spatial and temporal correlation of inputs. Neural Netw., 9, 1357–1365.

    Article  MATH  Google Scholar 

  • Tsukada, M., & Pan, X. (2005). The spatiotemporal learning rule and its efficiency in separating spatiotemporal patterns. Biol. Cybern., 92, 139–146.

    Article  MathSciNet  MATH  Google Scholar 

  • Tsukada, M., Yamazaki, Y., & Kojima, H. (2007). Interaction between the Spatio-Temporal Learning Rule (STLR) and Hebb type (HEBB) in single pyramidal cells in the hippocampal CA1 Area. Cogn. Neurodyn., 1, 1157–1167.

    Article  Google Scholar 

  • Watabe, A. M., Zaki, P. A., & O’Dell, T. J. (2000). Coactivation of beta-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and synergistically activates mitogen-activated protein kinase in the hippocampal CA1 region. J. Neurosci., 20, 5924–5931.

    Google Scholar 

  • Zhang, L. I., Tao, H. W., Holt, C. E., Harris, W. A., & Poo, M. (1998). A critical window for cooperation and competition among developing retinotectal synapses. Nature, 395, 37–44.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Minoru Tsukada.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsukada, M., Fukushima, Y. A Context-Sensitive Mechanism in Hippocampal CA1 Networks. Bull Math Biol 73, 417–435 (2011). https://doi.org/10.1007/s11538-010-9566-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11538-010-9566-8

Keywords

Navigation