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The Journal of Neuroscience, January 30, 2008, 28(5):1224-1235; doi:10.1523/JNEUROSCI.4928-07.2008

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Development/Plasticity/Repair
Metabotropic Glutamate Receptor Type 5-Dependent Long-Term Potentiation of Excitatory Synapses on Fast-Spiking GABAergic Neurons in Mouse Visual Cortex

Abdolrahman Sarihi,¹ Bin Jiang,^1,2 Alireza Komaki,^2,3 Kazuhiro Sohya,^1,2 Yuchio Yanagawa,^2,4 and Tadaharu Tsumoto^1,2

¹Brain Science Institute, RIKEN, Wako 351-0198, Japan, ²Solution-Oriented Research for Science and Technology, Japan Science and Technology Agency, Kawaguchi 442-0012, Japan, ³Department of Physiology, Hamadan University of Medical Sciences, Hamadan, Iran, and ⁴Department of Genetic and Behavioral Neuroscience, Graduate School of Medicine, Gunma University, Maebashi, 371-8511 Japan

Correspondence should be addressed to Dr. Tadaharu Tsumoto, Brain Science Institute, RIKEN, 2-1 Hirosawa, Wako 351-0198, Japan. Email: tsumoto{at}brain.riken.jp

Long-term potentiation (LTP) of excitatory synapses on GABAergic neurons in layer II/III of visual cortical slices was examined in GAD67-GFP knock-in mice by whole-cell recordings of EPSPs evoked by layer IV stimulation. Theta burst stimulation (TBS) paired with postsynaptic depolarization induced LTP in 14 of 19 fast-spiking GABAergic (FS-GABA) neurons, whereas only in 6 of 17 non-FS GABAergic neurons. The mean magnitude of LTP in the former cell group was larger than that in the latter. The paired-pulse stimulation protocol and coefficient of variation analysis indicated that LTP of excitatory synapses on FS-GABA neurons may be postsynaptic in origin. Filling postsynaptic cells with a Ca²⁺-chelator blocked the induction of LTP, suggesting an involvement of postsynaptic Ca²⁺ rise. The developmental analysis of LTP indicated that almost the same magnitude of LTP was induced after postnatal day 17 to the young adulthood, suggesting no age dependence after eye opening. This form of LTP was dependent neither on NMDA receptors nor voltage-gated Ca²⁺ channels (L and T types). An antagonist for type 5 metabotropic glutamate receptors (mGluR5) blocked this form of LTP, whereas an antagonist for mGluR1 was not effective. An agonist for mGluR1/5 induced potentiation of EPSPs of FS-GABA neurons in concentration- and use-dependent manners. This potentiation and TBS-induced LTP occluded each other. Further pharmacological analyses suggested that this form of LTP at FS-GABA neurons is induced through an activation of mGluR5, which triggers Ca²⁺ release from internal stores via activations of phospholipase C and inositol triphosphate.

Key words: LTP; GABAergic neuron; fast-spiking neuron; metabotropic glutamate receptor; visual cortex; transgenic mouse

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Received July 2, 2007; revised Dec. 7, 2007; accepted Dec. 10, 2007.

Correspondence should be addressed to Dr. Tadaharu Tsumoto, Brain Science Institute, RIKEN, 2-1 Hirosawa, Wako 351-0198, Japan. Email: tsumoto{at}brain.riken.jp

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