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Deciphering functional roles of synaptic plasticity and intrinsic neural firing in developing mouse visual cortex layer IV microcircuit

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Abstract

Between the onset of the critical period of mouse primary visual cortex and eye opening at postnatal day 14 is a complex process and that is vital for the cognitive function of vision. The onset of the critical period of mouse primary visual cortex involves changes of the intrinsic firing property of each neuron and short term plasticity of synapses. In order to investigate the functional role of each factor in regulating the circuit firing activity during the critical period plasticity, we adopted the Markram’s model for short term plasticity and Wilson’s model for intrinsic neuron firing activity, and construct a microcircuit for mouse visual cortex layer IV based on the connection probabilities from experimental results. Our results indicate that, during CP development, the most critical factors that regulate the firing pattern of microcircuit is the short term plasticity of the synapse from PC to PV and SST interneurons, which upregulates the PV interneuron firing and produces new balance between excitation and inhibition; the intrinsic firing activity of PC and PV during development downregulates the firing frequency of the circuits. In addition, we have investigated the function of feedforward excitatory thalamic-cortical projection to PC and PV interneuron during CP, and found that neural firing activity largely depends on the TC input and the results are similar to the local circuit with minor differences. We conclude that the short term plasticity development during critical period plays a crucial role in regulating the circuit behavior.

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References

  • Beierlein, M. (2003). Two dynamically distinct inhibitory networks in layer 4 of the neocortex. Journal of Neurophysiology, 90(5), 2987.

    Article  Google Scholar 

  • Cardin, J. A., Carlen, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L. H., & Moore, C. I. (2009). Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature, 459(7247), 663–667.

    Article  CAS  Google Scholar 

  • Cisneros-Franco, J. M., & de Villers-Sidani, É. (2019). Reactivation of critical period plasticity in adult auditory cortex through chemogenetic silencing of parvalbumin-positive interneurons. Proceedings of the National Academy of Sciences, 116(52), 26329–26331. https://doi.org/10.1073/pnas.1913227117.

    Article  CAS  Google Scholar 

  • Cruikshank, S. J., Urabe, H., Nurmikko, A. V., & Connors, B. W. (2010). Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron, 65(2), 230–245.

    Article  CAS  Google Scholar 

  • Davis, M. F., Figueroa Velez, D. X., Guevarra, R. P., Yang, M. C., Habeeb, M., Carathedathu, M. C., & Gandhi, S. P. (2015). Inhibitory neuron transplantation into adult visual cortex creates a new critical period that rescues impaired vision. Neuron, 86(4), 1055–1066.

    Article  CAS  Google Scholar 

  • Espinosa, J. S., & Stryker, M. P. (2012). Development and plasticity of the primary visual cortex. Neuron, 75(2), 230–249.

    Article  CAS  Google Scholar 

  • Fagiolini, M., Fritschy, J. M., Low, K., Mohler, H., Rudolph, U., & Hensch, T. K. (2004). Specific GABAA circuits for visual cortical plasticity. Science, 303(5664), 1681–1683.

    Article  CAS  Google Scholar 

  • Gonchar, Y., Wang, Q., & Burkhalter, A. (2007). Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Frontiers in Neuroanatomy, 1, 3.

    Google Scholar 

  • Gu, Y., Huang, S., Chang, M. C., Worley, P., Kirkwood, A., & Quinlan, E. M. (2013). Obligatory role for the immediate early gene NARP in critical period plasticity. Neuron, 79(2), 335–346.

    Article  CAS  Google Scholar 

  • Gutierrez, C., Cox, C. L., Rinzel, J., & Sherman, S. M. (2001). Dynamics of low-threshold spike activation in relay neurons of the cat lateral geniculate nucleus. The Journal of Neuroscience, 21(3), 1022–1032.

    Article  CAS  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(22), RC40.

    Article  CAS  Google Scholar 

  • Hensch, T. K., & Fagiolini, M. (2005). Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Progress in Brain Research, 147, 115–124.

    Article  CAS  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(5393), 1504–1508.

    Article  CAS  Google Scholar 

  • Huang, Z. J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M. F., Maffei, L., & Tonegawa, S. (1999). BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell, 98(6), 739–755.

    Article  CAS  Google Scholar 

  • Jang, H. J., Chung, H., Rowland, J. M., Richards, B. A., Kohl, M. M., & Kwag, J. (2020). Distinct roles of parvalbumin and somatostatin interneurons in gating the synchronization of spike times in the neocortex. Science Advances, 6(47), eaay5333.

    Article  CAS  Google Scholar 

  • Levelt, C. N., & Hubener, M. (2012). Critical-period plasticity in the visual cortex. Annual Review of Neuroscience, 35, 309–330.

    Article  CAS  Google Scholar 

  • Kelsom, C., & Lu, W. (2013). Development and specification of GABAergic cortical interneurons. Cell & Bioscience, 3, 19.

    Article  CAS  Google Scholar 

  • Khibnik, L. A., Cho, K. K., & Bear, M. F. (2010). Relative contribution of feedforward excitatory connections to expression of ocular dominance plasticity in layer 4 of visual cortex. Neuron, 66(4), 493–500.

    Article  CAS  Google Scholar 

  • Ko, H., Cossell, L., Baragli, C., Antolik, J., Clopath, C., Hofer, S. B., & Mrsic-Flogel, T. D. (2013). The emergence of functional microcircuits in visual cortex. Nature, 496(7443), 96–100.

    Article  CAS  Google Scholar 

  • Kuhlman, S. J., Lu, J., Lazarus, M. S., & Huang, Z. J. (2010). Maturation of GABAergic inhibition promotes strengthening of temporally coherent inputs among convergent pathways. PLoS Computational Biology, 6(6), e1000797.

    Article  Google Scholar 

  • Kuhlman, S. J., Tring, E., & Trachtenberg, J. T. (2011). Fast-spiking interneurons have an initial orientation bias that is lost with vision. Nature Neuroscience, 14(9), 1121–1123.

    Article  CAS  Google Scholar 

  • Liu, B. H., Wu, G. K., Arbuckle, R., Tao, H. W., & Zhang, L. I. (2007). Defining cortical frequency tuning with recurrent excitatory circuitry. Nature Neuroscience, 10(12), 1594–1600.

    Article  CAS  Google Scholar 

  • Markram, H., Yun, W., & Tsodyks, M. (1998). Differential signaling via the same axon of neocortical pyramidal neurons. Proceedings of the National Academy of Sciences of the United States of America, 95(9), 5323–5328.

    Article  CAS  Google Scholar 

  • Miao, Q., Yao, L., Rasch, M., Ye, Q., Li, X., & Zhang, X. (2016). Selective maturation of temporal dynamics of intracortical excitatory transmission at the critical period onset. Cell Reports, 16(6), 1677–1689.

    Article  CAS  Google Scholar 

  • Markram, H., Lübke, J., Frotscher, M., & Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic aps and epsps. Science, 275(5297), 213–215.

    Article  CAS  Google Scholar 

  • Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nature Reviews Neuroscience, 5(10), 793–807.

    Article  CAS  Google Scholar 

  • Miao, Q. (2014). Circuit Mechanisms underlying the early developmental regulation of visual cortical plasticity, PhD thesis.

  • Oswald, A. M., & Reyes, A. D. (2011). Development of inhibitory timescales in auditory cortex. Cerebral Cortex, 21(6), 1351–1361.

    Article  Google Scholar 

  • Pan, N. C., Fang, A., Shen, C., Sun, L., Wu, Q., & Wang, X. (2019). Early excitatory activity-dependent maturation of somatostatin interneurons in cortical layer 2/3 of mice. Cerebral Cortex, 29(10), 4107–4118.

    Google Scholar 

  • Ramoa, A. S., & Sur, M. (1996). Short-term synaptic plasticity in the visual cortex during development. Cerebral Cortex, 6(4), 640–646.

    Article  CAS  Google Scholar 

  • Rozov, A., & Burnashev, N. (1999). Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression. Nature, 401(6753), 594–598.

    Article  CAS  Google Scholar 

  • Sakurai, I., Kubota, S., & Niwano, M. (2014). The onset and closure of critical period plasticity regulated by feedforward inhibition. Neurocomputing, 143, 261–268.

    Article  Google Scholar 

  • Sale, A., Berardi, N., Spolidoro, M., Baroncelli, L., & Maffei, L. (2010). GABAergic inhibition in visual cortical plasticity. Frontiers in Cellular Neuroscience, 4, 10.

    Google Scholar 

  • Sohal, V. S., Zhang, F., Yizhar, O., & Deiseeroth, K. (2009). Parvalbulmin neurons and gamma rhythms enhance cortical circuit performance. Nature, 459(7247), 698–702.

    Article  CAS  Google Scholar 

  • Traub, R. D., Kopell, N., Bibbig, A., Buhl, E. H., LeBeau, F. E., & Whittington, M. A. (2001). Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. The Journal of Neuroscience, 21(23), 9478–9486.

    Article  CAS  Google Scholar 

  • Tsodyks, M. V., & Markram, H. (1997). The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proceedings of the National Academy of Sciences, 94(2), 719–723.

    Article  CAS  Google Scholar 

  • Tuncdemir, S. N., Wamsley, B., Stam, F. J., Osakada, F., Goulding, M., Callaway, E. M., Rudy, B., & Fishell, C. (2016). Early somatostatin interneuron connectivity mediates the maturation of deep layer cortical circuits. Neuron, 89, 521–535.

    Article  CAS  Google Scholar 

  • Trappenberg, T. P. (2010). Fundamentals of computational neuroscience. Oxford University Press, 2nd edition. 

  • Tremblay, R., Lee, S., & Rudy, B. (2016). GABAergic interneurons in the neocortex: from cellular properties to circuits. Neuron, 91, 260–292. https://doi.org/10.1016/j.neuron.2016.06.033.

    Article  CAS  Google Scholar 

  • Tsodyks, M., Pawelzik, K., & Markram, H. (1998). Neural networks with dynamic synapses. Neural Computation, 10(4), 821–835.

    Article  CAS  Google Scholar 

  • Virginia, G. M., Kelly, J. G., & Hawken, M. J. (2019). Major feedforward thalamic input into layer 4C of primary visual cortex in primate. Cerebral Cortex, 29(1), 134–149. https://doi.org/10.1093/cercor/bhx311

    Article  Google Scholar 

  • Wang, X. J., Rinzel, J., & Rogawski, M. A. (1991). A model of the t-type calcium current and the low-threshold spike in thalamic neurons. Journal of Neurophysiology, 66(3), 839–850.

    Article  CAS  Google Scholar 

  • Wilson, H. R. (1999). Simplified dynamics of human and mammalian neocortical neurons. Journal of Theoretical Biology, 200(4), 375–388.

    Article  CAS  Google Scholar 

  • Zucker, R. S., & Regehr, W. G. (2002). Short-term synaptic plasticity. Annual Review of Physiology, 64, 355–405.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Dr. Yao (Li, Yao) for helpful discussions. This research is supported by National Key R&D Program of China (No. 2019 YFA0709503), Beijing high-level discipline construction project–cognitive neuroscience, and China National Science Foundation (No. 31601145).

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  1. School of Systems Science, Beijing Normal University, Beijing, China

    Sanwu Liu & Yinyun Li

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Highlights

Critical Period (CP) development is a specific period during early development after eye opening for mouse at postnatal day P14-P20 until the critical period onset (P20-21). The plasticity in mouse primary visual cortex layer IV during CP development involves changes of the intrinsic neuronal firing property and synaptic short term plasticity. We have investigated the functional roles of each factor in regulating the firing pattern of the microcircuits of visual cortex IV during the critical period. For local circuits, the short term plasticity changes of PC output synapses during CP increases PC and PV firing activity intensively, while the intrinsic neuronal firing properties of PC and PV interneuron down regulates the circuit’s firing activity. The local circuit switches from PC and SST firing patterns before CP to PC and PV firing patterns after CP onset. For global circuits with thalamus cell injection, neural firing activity is basically similar to the local circuit with minor differences, indicating that the short term plasticity development during critical period plays a crucial role in regulating the circuit behavior.

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Liu, S., Li, Y. Deciphering functional roles of synaptic plasticity and intrinsic neural firing in developing mouse visual cortex layer IV microcircuit. J Comput Neurosci 51, 23–42 (2023). https://doi.org/10.1007/s10827-022-00823-x

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