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Depolarization-induced suppression of inhibition mediated by endocannabinoids at synapses from fast-spiking interneurons to medium spiny neurons in the striatum

Authors

  • Madoka Narushima,

    1. Department of Cellular Neuroscience, Osaka University, Graduate School of Medicine, Yamada-oka, Suita 565–0871, Japan
    2. Department of Cellular Neurophysiology, Graduate School of Medical Science, Kanazawa University, Takara-machi, Kanazawa 920–8640, Japan,
    3. CREST, Japan Science and Technology Agency, Tokyo 102–8666, Japan
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  • Motokazu Uchigashima,

    1. Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060–8638, Japan
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  • Kouichi Hashimoto,

    1. Department of Cellular Neuroscience, Osaka University, Graduate School of Medicine, Yamada-oka, Suita 565–0871, Japan
    2. CREST, Japan Science and Technology Agency, Tokyo 102–8666, Japan
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  • Masahiko Watanabe,

    1. Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060–8638, Japan
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  • Masanobu Kano

    1. Department of Cellular Neuroscience, Osaka University, Graduate School of Medicine, Yamada-oka, Suita 565–0871, Japan
    2. Department of Cellular Neurophysiology, Graduate School of Medical Science, Kanazawa University, Takara-machi, Kanazawa 920–8640, Japan,
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Dr Masanobu Kano, 1Department of Cellular Neuroscience, as above.
E-mail: mkano@cns.med.osaka-u.ac.jp

Abstract

Endogenous cannabinoids (endocannabinoids) act as retrograde inhibitory messengers in various regions of the brain. We have recently reported that endocannabinoids mediate short-term retrograde suppression of excitatory synaptic transmission from the neocortex to medium spiny (MS) neurons, the major projection neurons from the striatum. However, it remains unclear whether endocannabinoids modulate inhibitory transmission in the striatum. Here we show that depolarization of MS neurons induces transient suppression of inhibition that is mediated by retrograde endocannabinoid signalling. By paired recording from a fast-spiking (FS) interneuron and an MS neuron, we demonstrated that FS–MS inhibitory synapses undergo endocannabinoid-mediated retrograde suppression. We verified that GABAergic inhibitory terminals immunopositive for parvalbumin (PV), a marker for FS interneurons, expressed CB1 receptors. These PV–CB1 double-positive terminals surrounded dopamine D1 receptor-positive and D2 receptor-positive MS neurons; these constitute direct and indirect pathways, respectively. These results suggest that endocannabinoid-mediated retrograde suppression of inhibition influences information flow along both direct and indirect pathways, depending on the activity of MS neurons.

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