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.
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.
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.
Barria, A., & Malinow, R. (2002). Subunit-specific NMDA receptor trafficking to synapses. Neuron, 35, 345–353.
Bellone, C., & Nicoll, R. A. (2007). Rapid bidirectional switching of synaptic NMDA receptors. Neuron, 55, 779–785.
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.
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.
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.
Caporale, N., & Dan, Y. (2008). Spike timing-dependent plasticity: A Hebbian learning rule. Annual Review of Neuroscience, 31, 25–46.
Crair, M. C., & Malenka, R. C. (1995). A critical period for long-term potentiation at thalamocortical synapses. Nature, 375, 325–328.
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.
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.
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.
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.
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.
Fagiolini, M., & Hensch, T. K. (2000). Inhibitory threshold for critical-period activation in primary visual cortex. Nature, 404, 183–186.
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.
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.
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.
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.
Froemke, R. C., & Dan, Y. (2002). Spike-timing-dependent synaptic modification induced by natural spike trains. Nature, 416, 433–438.
Gerstner, W., Kempter, R., van Hemmen, J. L., & Wagner, H. (1996). A neuronal learning rule for sub-millisecond temporal coding. Nature, 383, 76–78.
Gerstner, W., & Kistler, W. M. (2002). Spiking neuron models. Cambridge: Cambridge University.
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.
Gütig, R., Aharonov, R., Rotter, S., & Sompolinsky, H. (2003). Learning input correlations though nonlinear temporally asymmetric Hebbian plasticity. Journal of Neuroscience, 23, 3697–3714.
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.
Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nature Reviews Neuroscience, 6, 877–888.
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.
Hessler, N. A., Shirke, A. M., & Malinow, R. (1993). The probability of transmitter release at a mammalian central synapse. Nature, 366, 569–572.
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.
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.
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.
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.
Kempter, R., Gerstner, W., & van Hemmen, J. L. (1999). Hebbian learning and spiking neurons. Physical Review E, 59, 4498–4514.
Kempter, R., Gerstner, W., & van Hemmen, J. L. (2001). Intrinsic stabilization of output rates by spike-based Hebbian learning. Neural Computation, 13, 2709–2741.
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.
Kirkwood, A., & Bear, M. F. (1994). Hebbian synapses in visual cortex. Journal of Neuroscience, 14, 1634–1645.
Koch, C. (1999). Biophysics of computation. New York: Oxford University.
Köhr, G. (2006). NMDA receptor function: subunit composition versus spatial distribution. Cell and Tissue Research, 326, 439–446.
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.
Kubota, S., & Kitajima, T. (2008). A model for synaptic development regulated by NMDA receptor subunit expression. Journal of Computational Neuroscience, 24, 1–20.
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.
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.
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.
Markram, H., Lubke, J., Frotscher, M., & Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213–215.
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.
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.
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.
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.
Morrison, A., Diesmann, M., & Gerstner, W. (2008). Phenomenological models of synaptic plasticity based on spike timing. Biological Cybernetics, 98, 459–478.
Nevian, T., & Sakmann, B. (2006). Spine Ca2+ signaling in spike-timing-dependent plasticity. Journal of Neuroscience, 26, 11001–11013.
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.
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.
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.
Rauschecker, J. P., & Singer, W. (1979). Changes in the circuitry of the kitten visual cortex are gated by postsynaptic activity. Nature, 280, 58–60.
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.
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.
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.
Rosenmund, C., Feltz, A., & Westbrook, G. L. (1995). Calcium-dependent inactivation of synaptic NMDA receptors in hippocampal neurons. Journal of Neurophysiology, 73, 427–430.
Rubin, J., Lee, D. D., & Sompolinsky, H. (2001). Equilibrium properties of temporally asymmetric Hebbian plasticity. Physical Review Letters, 86, 364–367.
Shadlen, M. N., & Newsome, W. T. (1994). Noise, neural codes and cortical organization. Current Opinion in Neurobiology, 4, 569–579.
Shatz, C. J. (1990). Impulse activity and the patterning of connections during CNS development. Neuron, 5, 745–756.
Shpiro, A., Curtu, R., Rinzel, J., & Rubin, N. (2007). Dynamical characteristics common to neuronal competition models. Journal of Neurophysiology, 97, 462–473.
Song, S., & Abbott, L. F. (2001). Cortical development and remapping through spike timing-dependent plasticity. Neuron, 32, 339–350.
Song, S., Miller, K. D., & Abbott, L. F. (2000). Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nature Neuroscience, 3, 919–926.
Stephenson, F. A. (2001). Subunit characterization of NMDA receptors. Current Drug Targets, 2, 233–239.
Svoboda, K., Denk, W., Kleinfeld, D., & Tank, D. W. (1997). in vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature, 385, 161–165.
Tanabe, S., & Pakdaman, K. (2001). Noise-enhanced neuronal reliability. Physical Review E, 64, 041904.
Tegnér, J., & Kepecs, Á. (2002). Why neuronal dynamics should control synaptic learning rules. Advances in Neural Information Processing Systems, 14, 285–292.
Wang, X. J. (1998). Calcium coding and adaptive temporal computation in cortical pyramidal neurons. Journal of Neurophysiology, 79, 1549–1566.
Wiesel, T. N. (1982). Postnatal development of the visual cortex and the influence of environment. Nature, 299, 583–591.
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.
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.
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.
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
Corresponding author
Additional information
Action Editor: Wulfram Gerstner
Rights 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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10827-010-0212-0