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Functional Autapses Form in Striatal Parvalbumin Interneurons but not Medium Spiny Projection Neurons

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Abstract

Autapses selectively form in specific cell types in many brain regions. Previous studies have also found putative autapses in principal spiny projection neurons (SPNs) in the striatum. However, it remains unclear whether these neurons indeed form physiologically functional autapses. We applied whole-cell recording in striatal slices and identified autaptic cells by the occurrence of prolonged asynchronous release (AR) of neurotransmitters after bursts of high-frequency action potentials (APs). Surprisingly, we found no autaptic AR in SPNs, even in the presence of Sr2+. However, robust autaptic AR was recorded in parvalbumin (PV)-expressing neurons. The autaptic responses were mediated by GABAA receptors and their strength was dependent on AP frequency and number. Further computer simulations suggest that autapses regulate spiking activity in PV cells by providing self-inhibition and thus shape network oscillations. Together, our results indicate that PV neurons, but not SPNs, form functional autapses, which may play important roles in striatal functions.

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Data Availability

All relevant data and computation codes are available from the corresponding authors upon request.

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Acknowledgements

We are grateful to Drs. Suixin Deng and Junlong Li for their help in data analysis. This work was supported by the National Natural Science Foundation of China (32130044, 31630029, 32171094, and 32100930) and the National Key Research and Development Program of China (2021ZD0202500).

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Author notes

  1. Zhenfeng Shu

    Present address: Section of Infection and Immunity, Herman Ostrow School of Dentistry, University of Southern California, Los Angeles, CA, 90089, USA

Authors and Affiliations

  1. School of Systems Science and State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, 100875, China

    Xuan Wang, Luozheng Li & Da-Hui Wang

  2. Department of Neurosurgery, Jinshan Hospital, State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, Institute for Translational Brain Research, Fudan University, Shanghai, 200032, China

    Zhenfeng Shu, Quansheng He, Xiaowen Zhang, Xiaoxue Zhang, Liang Li, Yujie Xiao, Bo Peng, Feifan Guo & Yousheng Shu

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Wang, X., Shu, Z., He, Q. et al. Functional Autapses Form in Striatal Parvalbumin Interneurons but not Medium Spiny Projection Neurons. Neurosci. Bull. 39, 576–588 (2023). https://doi.org/10.1007/s12264-022-00991-x

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