Long-term depression of synaptic transmission in the adult mouse insular cortex in vitro

Authors

  • Ming-Gang Liu,

    1. Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, Korea
    2. Department of Physiology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
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    • M.G.L. and K.K. contributed equally to this work.
  • Kohei Koga,

    1. Department of Physiology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
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    • M.G.L. and K.K. contributed equally to this work.
  • Yan-Yan Guo,

    1. Department of Pharmacology, School of Pharmacy, Fourth Military Medical University, Xi'an, China
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  • SukJae Joshua Kang,

    1. Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, Korea
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  • Graham L. Collingridge,

    1. Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, Korea
    2. Centre for Synaptic Plasticity, School of Physiology and Pharmacology, Bristol, UK
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  • Bong-Kiun Kaang,

    1. Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, Korea
    2. Department of Biological Sciences, College of Natural Sciences, National Creative Research Initiative Center for Memory, Seoul National University, Seoul, Korea
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  • Ming-Gao Zhao,

    1. Department of Pharmacology, School of Pharmacy, Fourth Military Medical University, Xi'an, China
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  • Min Zhuo

    Corresponding author
    1. Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, Korea
    2. Department of Physiology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
    3. Center for Neuron and Disease, Frontier Institutes of Life Science and of Science and Technology, Xi'an Jiaotong University, Xi'an, China
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Abstract

The insular cortex (IC) is known to play important roles in higher brain functions such as memory and pain. Activity-dependent long-term depression (LTD) is a major form of synaptic plasticity related to memory and chronic pain. Previous studies of LTD have mainly focused on the hippocampus, and no study in the IC has been reported. In this study, using a 64-channel recording system, we show for the first time that repetitive low-frequency stimulation (LFS) can elicit frequency-dependent LTD of glutamate receptor-mediated excitatory synaptic transmission in both superficial and deep layers of the IC of adult mice. The induction of LTD in the IC required activation of the N-methyl-d-aspartate (NMDA) receptor, metabotropic glutamate receptor (mGluR)5, and L-type voltage-gated calcium channel. Protein phosphatase 1/2A and endocannabinoid signaling are also critical for the induction of LTD. In contrast, inhibiting protein kinase C, protein kinase A, protein kinase Mζ or calcium/calmodulin-dependent protein kinase II did not affect LFS-evoked LTD in the IC. Bath application of the group I mGluR agonist (RS)-3,5-dihydroxyphenylglycine produced another form of LTD in the IC, which was NMDA receptor-independent and could not be occluded by LFS-induced LTD. Our studies have characterised the basic mechanisms of LTD in the IC at the network level, and suggest that two different forms of LTD may co-exist in the same population of IC synapses.

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