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Compartmental organization of synaptic inputs to parvalbumin-expressing GABAergic neurons in mouse primary somatosensory cortex

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Abstract

Parvalbumin (PV)-positive fast-spiking cells in the neocortex are known to generate gamma oscillations by mutual chemical and electrical connections. Recent findings suggest that this rhythm might be responsible for higher-order brain functions, and related to psychiatric disorders. To elucidate the precise structural rules of the connections of PV neurons, we first produced genetic tools. Using a lentiviral expression system, we developed neuron-specific promoters and a new reporter protein that labels the somatodendritic membrane of neurons. We applied the reporter protein to the generation of transgenic mice, and succeeded in visualizing the dendrites and cell bodies of PV neurons efficiently. Then we analyzed excitatory and inhibitory inputs to PV neurons in the primary somatosensory cortex using the mice. Corticocortical glutamatergic inputs were more frequently found on the distal dendrites than on the soma, whereas thalamocortical inputs did not differ between the proximal and distal portions. Corticocortical inhibitory inputs were more densely distributed on the soma than on the dendrites. We further investigated which types of neocortical GABAergic neurons preferred the PV soma over their dendrites. We revealed that the somatic and dendritic compartments principally received GABAergic inputs from vasoactive intestinal polypeptide (VIP)-positive and PV neurons, respectively. This compartmental organization suggests that PV neurons communicate with each other mainly via the dendrites, and that their activity is effectively controlled by the somatic inputs of VIP neurons. These findings provide new insights into the neuronal circuits involving PV neurons, and contribute to a better understanding of brain functions and mental disorders.

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Acknowledgments

The author greatly thanks Prof. Takeshi Kaneko and the lab members at the Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University for their valuable discussions and collaborations. This work was supported in part by a Grant-in-Aid for Scientific Research on Innovative Areas “Neural Diversity and Neocortical Organization” (25123709) from The Ministry of Education, Culture, Sports, Science and Technology (MEXT) and a Grant-in-Aid for Scientific Research (C) (24500408) from the Japan Society for the Promotion of Science (JSPS). The author received the Incitement Award of the Japanese Association of Anatomists in Japan for the fiscal year 2013, and gave a presentation of the present review at the 119th Annual Meeting in Shimono, Japan on March 28, 2014.

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The author has no conflicts of interest to declare.

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  1. Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto, 606-8501, Japan

    Hiroyuki Hioki

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Hioki, H. Compartmental organization of synaptic inputs to parvalbumin-expressing GABAergic neurons in mouse primary somatosensory cortex. Anat Sci Int 90, 7–21 (2015). https://doi.org/10.1007/s12565-014-0264-8

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