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Bidirectional plasticity in fast-spiking GABA circuits by visual experience

Abstract

Experience-dependent plasticity in the brain requires balanced excitation–inhibition1. How individual circuit elements contribute to plasticity outcome in complex neocortical networks remains unknown. Here we report an intracellular analysis of ocular dominance plasticity—the loss of acuity and cortical responsiveness for an eye deprived of vision in early life2,3. Unlike the typical progressive loss of pyramidal-cell bias, direct recording from fast-spiking cells in vivo reveals a counterintuitive initial shift towards the occluded eye followed by a late preference for the open eye, consistent with a spike-timing-dependent plasticity rule for these inhibitory neurons. Intracellular pharmacology confirms a dynamic switch of GABA (γ-aminobutyric acid) impact to pyramidal cells following deprivation in juvenile mice only. Together these results suggest that the bidirectional recruitment of an initially binocular GABA circuit may contribute to experience-dependent plasticity in the developing visual cortex.

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Figure 1: Distinct plasticity profiles in pyramidal and fast-spiking visual cortical neurons.
Figure 2: Bidirectional plasticity in fast-spiking cells in vivo follows an STDP rule.
Figure 3: Intracellular GABA-receptor blockade in pyramidal neurons of visual cortex.
Figure 4: Dynamic GABA impact in single pyramidal cells with age and experience.

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Acknowledgements

We thank A. Scheuber for slice experiments, and T. Hosoya and S. Yanagihara for MATLAB programming advice. This work was supported in part by a Grant-in-aid for Scientific Research on Priority Areas (‘Integrative Brain Research’) from the Japanese Ministry of Education, Culture, Sports, Science & Technology (T.F., S.K. and T.K.H.).

Author Contributions T.K.H. and Y.Y.-S. designed the experiments; S.K., H.C. and T.F. formulated the computational models; Y.Y.-S. performed the intracellular recording in vivo; S.K. ran the simulations; and T.K.H., Y.Y.-S., S.K. and T.F. wrote the paper.

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Correspondence to Takao K. Hensch.

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Yazaki-Sugiyama, Y., Kang, S., Câteau, H. et al. Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 462, 218–221 (2009). https://doi.org/10.1038/nature08485

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