Skip to main content
Log in

Possible role of cooperative action of NMDA receptor and GABA function in developmental plasticity

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

Abstract

The maturation of cortical circuits is strongly influenced by sensory experience during a restricted critical period. The developmental alteration in the subunit composition of NMDA receptors (NMDARs) has been suggested to be involved in regulating the timing of such plasticity. However, this hypothesis does not explain the evidence that enhancing GABA inhibition triggers a critical period in the visual cortex. Here, to investigate how the NMDAR and GABA functions influence synaptic organization, we examine an spike-timing-dependent plasticity (STDP) model that incorporates the dynamic modulation of LTP, associated with the activity- and subunit-dependent desensitization of NMDARs, as well as the background inhibition by GABA. We show that the competitive interaction between correlated input groups, required for experience-dependent synaptic modifications, may emerge when both the NMDAR subunit expression and GABA inhibition reach a sufficiently mature state. This may suggest that the cooperative action of these two developmental mechanisms can contribute to embedding the spatiotemporal structure of input spikes in synaptic patterns and providing the trigger for experience-dependent cortical plasticity.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahmed, B., Anderson, J. C., Douglas, R. J., Martin, K. A. C., & Whitteridge, D. (1998). Estimates of the net excitatory currents evoked by visual stimulation of identified neurons in cat visual cortex. Cerebral Cortex, 8, 462–476.

    Article  CAS  PubMed  Google Scholar 

  • Angeli, D., Ferrell, J. E., & Sontag, E. D. (2004). Detection of multistability, bifurcations, and hysteresis in a large class of biological positive-feedback systems. Proceedings of the National Academy of Sciences of the United States of America, 101, 1822–1827.

    Article  CAS  PubMed  Google Scholar 

  • Barria, A., & Malinow, R. (2002). Subunit-specific NMDA receptor trafficking to synapses. Neuron, 35, 345–353.

    Article  CAS  PubMed  Google Scholar 

  • Bellone, C., & Nicoll, R. A. (2007). Rapid bidirectional switching of synaptic NMDA receptors. Neuron, 55, 779–785.

    Article  CAS  PubMed  Google Scholar 

  • Bender, V. A., Bender, K. J., Brasier, D. J., & Feldman, D. E. (2006). Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. Journal of Neuroscience, 26, 4166–4177.

    Article  CAS  PubMed  Google Scholar 

  • Bernander, O., Douglas, R. J., Martin, K. A. C., & Koch, C. (1991). Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proceedings of the National Academy of Sciences of the United States of America, 88, 11569–11573.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Caporale, N., & Dan, Y. (2008). Spike timing-dependent plasticity: A Hebbian learning rule. Annual Review of Neuroscience, 31, 25–46.

    Article  CAS  PubMed  Google Scholar 

  • Crair, M. C., & Malenka, R. C. (1995). A critical period for long-term potentiation at thalamocortical synapses. Nature, 375, 325–328.

    Article  CAS  PubMed  Google Scholar 

  • Daw, M. I., Scott, H. L., & Isaac, J. T. R. (2007). Developmental synaptic plasticity at the thalamocortical input to barrel cortex: Mechanisms and roles. Molecular and Cellular Neuroscience, 34, 493–502.

    Article  CAS  PubMed  Google Scholar 

  • Destexhe, A., Rudolph, M., Fellous, J. M., & Sejnowski, T. J. (2001). Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience, 107, 13–24.

    Article  CAS  PubMed  Google Scholar 

  • Dumas, T. C. (2005). Developmental regulation of cognitive abilities: Modified composition of a molecular switch turns on associative learning. Progress in Neurobiology, 76, 189–211.

    Article  CAS  PubMed  Google Scholar 

  • Egger, V., Feldmeyer, D., & Sakmann, B. (1999). Coincidence detection and change of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nature Neuroscience, 2, 1098–1105.

    Article  CAS  PubMed  Google Scholar 

  • Erisir, A., & Harris, J. L. (2003). Decline of the critical period of visual plasticity is concurrent with the reduction of NR2B subunit of the synaptic NMDA receptor in layer 4. Journal of Neuroscience, 23, 5208–5218.

    CAS  PubMed  Google Scholar 

  • Fagiolini, M., & Hensch, T. K. (2000). Inhibitory threshold for critical-period activation in primary visual cortex. Nature, 404, 183–186.

    Article  CAS  PubMed  Google Scholar 

  • Fagiolini, M., Katagiri, H., Miyamoto, H., Mori, H., Grant, S. G. N., Mishina, M., et al. (2003). Separable features of visual cortical plasticity revealed by N-methyl-d-aspartate receptor 2A signaling. Proceedings of the National Academy of Sciences of the United States of America, 100, 2854–2859.

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Feldman, D. E., Nicoll, R. A., Malenka, R. C., & Isaac, J. T. R. (1998). Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron, 21, 347–357.

    Article  CAS  PubMed  Google Scholar 

  • Flint, A. C., Maisch, U. S., Weishaupt, J. H., Kriegstein, A. R., & Monyer, H. (1997). NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. Journal of Neuroscience, 17, 2469–2476.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gerstner, W., Kempter, R., van Hemmen, J. L., & Wagner, H. (1996). A neuronal learning rule for sub-millisecond temporal coding. Nature, 383, 76–78.

    Article  CAS  PubMed  Google Scholar 

  • Gerstner, W., & Kistler, W. M. (2002). Spiking neuron models. Cambridge: Cambridge University.

    Google Scholar 

  • Gordon, J. A., & Stryker, M. P. (1996). Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. Journal of Neuroscience, 16, 3274–3286.

    CAS  PubMed  Google Scholar 

  • Gütig, R., Aharonov, R., Rotter, S., & Sompolinsky, H. (2003). Learning input correlations though nonlinear temporally asymmetric Hebbian plasticity. Journal of Neuroscience, 23, 3697–3714.

    PubMed  Google Scholar 

  • Hanover, J. L., Huang, Z. J., Tonegawa, S., & Stryker, M. P. (1999). Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. Journal of Neuroscience, 19, RC40.

  • Helmchen, F., Imoto, K., & Sakmann, B. (1996). Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. Biophysical Journal, 70, 1069–1081.

    Article  CAS  PubMed  Google Scholar 

  • Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nature Reviews Neuroscience, 6, 877–888.

    Article  CAS  PubMed  Google Scholar 

  • Hensch, T. K., Fagiolini, M., Mataga, N., Stryker, M. P., Baekkeskov, S., & Kash, S. F. (1998). Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science, 282, 1504–1508.

    Article  CAS  PubMed  Google Scholar 

  • Hessler, N. A., Shirke, A. M., & Malinow, R. (1993). The probability of transmitter release at a mammalian central synapse. Nature, 366, 569–572.

    Article  CAS  PubMed  Google Scholar 

  • Huang, Z. J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M. F., et al. (1999). BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell, 98, 739–755.

    Article  CAS  PubMed  Google Scholar 

  • Ito, I., Futai, K., Katagiri, H., Watanabe, M., Sakimura, K., Mishina, M., et al. (1997). Synapse-selective impairment of NMDA receptor functions in mice lacking NMDA receptor epsilon 1 or epsilon 2 subunit. Journal of Physiology (London), 500(2), 401–408.

    CAS  Google Scholar 

  • Iwai, Y., Fagiolini, M., Obata, K., & Hensch, T. K. (2003). Rapid critical period induction by tonic inhibition in visual cortex. Journal of Neuroscience, 23, 6695–6702.

    CAS  PubMed  Google Scholar 

  • Jahr, C. E., & Stevens, C. F. (1990). Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. Journal of Neuroscience, 10, 3178–3182.

    CAS  PubMed  Google Scholar 

  • Kempter, R., Gerstner, W., & van Hemmen, J. L. (1999). Hebbian learning and spiking neurons. Physical Review E, 59, 4498–4514.

    Article  CAS  Google Scholar 

  • Kempter, R., Gerstner, W., & van Hemmen, J. L. (2001). Intrinsic stabilization of output rates by spike-based Hebbian learning. Neural Computation, 13, 2709–2741.

    Article  CAS  PubMed  Google Scholar 

  • Kepecs, A., van Rossum, M. C. W., Song, S., & Tegner, J. (2002). Spike-timing-dependent plasticity: Common themes and divergent vistas. Biological Cybernetics, 87, 446–458.

    Article  PubMed  Google Scholar 

  • Kirkwood, A., & Bear, M. F. (1994). Hebbian synapses in visual cortex. Journal of Neuroscience, 14, 1634–1645.

    CAS  PubMed  Google Scholar 

  • Koch, C. (1999). Biophysics of computation. New York: Oxford University.

    Google Scholar 

  • Köhr, G. (2006). NMDA receptor function: subunit composition versus spatial distribution. Cell and Tissue Research, 326, 439–446.

    Article  PubMed  Google Scholar 

  • Krupp, J. J., Vissel, B., Heinemann, S. F., & Westbrook, G. L. (1996). Calcium-dependent inactivation of recombinant N-methyl-d-aspartate receptors is NR2 subunit specific. Molecular Pharmacology, 50, 1680–1688.

    CAS  PubMed  Google Scholar 

  • Kubota, S., & Kitajima, T. (2008). A model for synaptic development regulated by NMDA receptor subunit expression. Journal of Computational Neuroscience, 24, 1–20.

    Article  PubMed  Google Scholar 

  • Kubota, S., Rubin, J., & Kitajima, T. (2009). Modulation of LTP/LTD balance in STDP by an activity-dependent feedback mechanism. Neural Networks, 22, 527–535.

    Article  PubMed  Google Scholar 

  • Kumar, S. S., & Huguenard, J. R. (2003). Pathway-specific differences in subunit composition of synaptic NMDA receptors on pyramidal neurons in neocortex. Journal of Neuroscience, 23, 10074–10083.

    CAS  PubMed  Google Scholar 

  • Legendre, P., Rosenmund, C., & Westbrook, G. L. (1993). Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. Journal of Neuroscience, 13, 674–684.

    CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Medina, I., Leinekugel, X., & Ben-Ari, Y. (1999). Calcium-dependent inactivation of the monosynaptic NMDA EPSCs in rat hippocampal neurons in culture. European Journal of Neuroscience, 11, 2422–2430.

    Article  CAS  PubMed  Google Scholar 

  • Meffin, H., Besson, J., Burkitt, A. N., & Grayden, D. B. (2006). Learning the structure of correlated synaptic subgroups using stable and competitive spike-timing-dependent plasticity. Physical Review E, 73, 041911.

    Article  CAS  Google Scholar 

  • Mierau, S. B., Meredith, R. M., Upton, A. L., & Paulsen, O. (2004). Dissociation of experience-dependent and -independent changes in excitatory synaptic transmission during development of barrel cortex. Proceedings of the National Academy of Sciences of the United States of America, 101, 15518–15523.

    Article  CAS  PubMed  Google Scholar 

  • Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., & Seeburg, P. H. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron, 12, 529–540.

    Article  CAS  PubMed  Google Scholar 

  • Morrison, A., Diesmann, M., & Gerstner, W. (2008). Phenomenological models of synaptic plasticity based on spike timing. Biological Cybernetics, 98, 459–478.

    Article  PubMed  Google Scholar 

  • Nevian, T., & Sakmann, B. (2006). Spine Ca2+ signaling in spike-timing-dependent plasticity. Journal of Neuroscience, 26, 11001–11013.

    Article  CAS  PubMed  Google Scholar 

  • Quinlan, E. M., Olstein, D. H., & Bear, M. F. (1999a). Bidirectional, experience-dependent regulation of N-methyl-d-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proceedings of the National Academy of Sciences of the United States of America, 96, 12876–12880.

    Article  CAS  PubMed  Google Scholar 

  • Quinlan, E. M., Philpot, B. D., Huganir, R. L., & Bear, M. F. (1999b). Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nature Neuroscience, 2, 352–357.

    Article  CAS  PubMed  Google Scholar 

  • Ramoa, A. S., Paradiso, M. A., & Freeman, R. D. (1988). Blockade of intracortical inhibition in kitten striate cortex: Effects on receptive field properties and associated loss of ocular dominance plasticity. Experimental Brain Research, 73, 285–296.

    Article  CAS  Google Scholar 

  • Rauschecker, J. P., & Singer, W. (1979). Changes in the circuitry of the kitten visual cortex are gated by postsynaptic activity. Nature, 280, 58–60.

    Article  CAS  PubMed  Google Scholar 

  • Rittenhouse, C. D., Shouval, H. Z., Paradiso, M. A., & Bear, M. F. (1999). Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature, 397, 347–350.

    Article  CAS  PubMed  Google Scholar 

  • Rittenhouse, C. D., Siegler, B. A., Voelker, C. A., Shouval, H. Z., Paradiso, M. A., & Bear, M. F. (2006). Stimulus for rapid ocular dominance plasticity in visual cortex. Journal of Neurophysiology, 95, 2947–2950.

    Article  PubMed  Google Scholar 

  • Roberts, E. B., & Ramoa, A. S. (1999). Enhanced NR2A subunit expression and decreased NMDA receptor decay time at the onset of ocular dominance plasticity in the ferret. Journal of Neurophysiology, 81, 2587–2591.

    CAS  PubMed  Google Scholar 

  • Rosenmund, C., Feltz, A., & Westbrook, G. L. (1995). Calcium-dependent inactivation of synaptic NMDA receptors in hippocampal neurons. Journal of Neurophysiology, 73, 427–430.

    CAS  PubMed  Google Scholar 

  • Rubin, J., Lee, D. D., & Sompolinsky, H. (2001). Equilibrium properties of temporally asymmetric Hebbian plasticity. Physical Review Letters, 86, 364–367.

    Article  CAS  PubMed  Google Scholar 

  • Shadlen, M. N., & Newsome, W. T. (1994). Noise, neural codes and cortical organization. Current Opinion in Neurobiology, 4, 569–579.

    Article  CAS  PubMed  Google Scholar 

  • Shatz, C. J. (1990). Impulse activity and the patterning of connections during CNS development. Neuron, 5, 745–756.

    Article  CAS  PubMed  Google Scholar 

  • Shpiro, A., Curtu, R., Rinzel, J., & Rubin, N. (2007). Dynamical characteristics common to neuronal competition models. Journal of Neurophysiology, 97, 462–473.

    Article  PubMed  Google Scholar 

  • Song, S., & Abbott, L. F. (2001). Cortical development and remapping through spike timing-dependent plasticity. Neuron, 32, 339–350.

    Article  CAS  PubMed  Google Scholar 

  • Song, S., Miller, K. D., & Abbott, L. F. (2000). Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nature Neuroscience, 3, 919–926.

    Article  CAS  PubMed  Google Scholar 

  • Stephenson, F. A. (2001). Subunit characterization of NMDA receptors. Current Drug Targets, 2, 233–239.

    Article  CAS  PubMed  Google Scholar 

  • Svoboda, K., Denk, W., Kleinfeld, D., & Tank, D. W. (1997). in vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature, 385, 161–165.

    Article  CAS  PubMed  Google Scholar 

  • Tanabe, S., & Pakdaman, K. (2001). Noise-enhanced neuronal reliability. Physical Review E, 64, 041904.

    Article  CAS  Google Scholar 

  • Tegnér, J., & Kepecs, Á. (2002). Why neuronal dynamics should control synaptic learning rules. Advances in Neural Information Processing Systems, 14, 285–292.

    Google Scholar 

  • Wang, X. J. (1998). Calcium coding and adaptive temporal computation in cortical pyramidal neurons. Journal of Neurophysiology, 79, 1549–1566.

    CAS  PubMed  Google Scholar 

  • Wiesel, T. N. (1982). Postnatal development of the visual cortex and the influence of environment. Nature, 299, 583–591.

    Article  CAS  PubMed  Google Scholar 

  • Wolfart, J., Debay, D., Masson, G. L., Destexhe, A., & Bal, T. (2005). Synaptic background activity controls spike transfer from thalamus to cortex. Nature Neuroscience, 8, 1760–1767.

    Article  CAS  PubMed  Google Scholar 

  • Yeung, L. C., Shouval, H. Z., Blais, B. S., & Cooper, L. N. (2004). Synaptic homeostasis and input selectivity follow from a calcium-dependent plasticity model. Proceedings of the National Academy of Sciences of the United States of America, 101, 14943–14948.

    Article  CAS  PubMed  Google Scholar 

  • Zador, A., Koch, C., & Brown, T. H. (1990). Biophysical model of a Hebbian synapse. Proceedings of the National Academy of Sciences of the United States of America, 87, 6718–6722.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

This study is partially supported by Grant-in-Aid for Scientific Research (KAKENHI (19700281), Young Scientists (B)) from the Japanese government. S.K. is partially supported by the Program to Accelerate the Internationalization of University Education from the Japanese government and the International Research Training Program from Yamagata University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shigeru Kubota.

Additional information

Action Editor: Wulfram Gerstner

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kubota, S., Kitajima, T. Possible role of cooperative action of NMDA receptor and GABA function in developmental plasticity. J Comput Neurosci 28, 347–359 (2010). https://doi.org/10.1007/s10827-010-0212-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-010-0212-0

Keywords

Navigation