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Dyskinesia is Closely Associated with Synchronization of Theta Oscillatory Activity Between the Substantia Nigra Pars Reticulata and Motor Cortex in the Off L-dopa State in Rats

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Abstract

Excessive theta (θ) frequency oscillation and synchronization in the basal ganglia (BG) has been reported in elderly parkinsonian patients and animal models of levodopa (L-dopa)-induced dyskinesia (LID), particularly the θ oscillation recorded during periods when L-dopa is withdrawn (the off L-dopa state). To gain insight into processes underlying this activity, we explored the relationship between primary motor cortex (M1) oscillatory activity and BG output in LID. We recorded local field potentials in the substantia nigra pars reticulata (SNr) and M1 of awake, inattentive resting rats before and after L-dopa priming in Sham control, Parkinson disease model, and LID model groups. We found that chronic L-dopa increased θ synchronization and information flow between the SNr and M1 in off L-dopa state LID rats, with a SNr-to-M1 flow directionality. Compared with the on state, θ oscillational activity (θ synchronization and information flow) during the off state were more closely associated with abnormal involuntary movements. Our findings indicate that θ oscillation in M1 may be consequent to abnormal synchronous discharges in the BG and support the notion that M1 θ oscillation may participate in the induction of dyskinesia.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (81771210) and the Natural Science Foundation of Guangdong Province, China (2015A030313288).

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  1. Jiazhi Chen and Qiang Wang contributed equally to this work.

Authors and Affiliations

  1. The National Key Clinic Specialty, The Engineering Technology Research Center of the Ministry of Education of China, Guangdong Provincial Key Laboratory on Brain Function Repair and Regeneration, Department of Neurosurgery, Zhujiang Hospital, Southern Medical University, Guangzhou, 510282, China

    Jiazhi Chen, Qiang Wang, Nanxiang Li, Shujie Huang, Min Li, Junbin Cai, Huantao Wen, Siyuan Lv & Wangming Zhang

  2. Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, China

    Yuzheng Wang, Ning Wang, Jinyan Wang & Fei Luo

  3. Movement Disorders and Neuromodulation Unit, Department for Neurology, Charité - University Medicine Berlin, 10117, Berlin, Germany

    Qiang Wang

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  1. Jiazhi Chen
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Chen, J., Wang, Q., Li, N. et al. Dyskinesia is Closely Associated with Synchronization of Theta Oscillatory Activity Between the Substantia Nigra Pars Reticulata and Motor Cortex in the Off L-dopa State in Rats. Neurosci. Bull. 37, 323–338 (2021). https://doi.org/10.1007/s12264-020-00606-3

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