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Effects of high-frequency transcranial magnetic stimulation on theta-gamma oscillations and coupling in the prefrontal cortex of rats during working memory task

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Abstract

High-frequency rTMS has been widely used to improve working memory (WM) impairment; however, the underlying neurophysiological mechanisms are unclear. We evaluated the effect of high-frequency rTMS on behaviors relevant to WM as well as coupling between theta and gamma oscillations in the prefrontal cortex (PFC) of rats. Accordingly, Wistar rats received high-frequency rTMS daily for 14 days (5 Hz, 10 Hz, and 15 Hz stimulation; 600 pulses; n = 6 per group), whereas the control group received sham stimulation. Electrophysiological signals were recorded simultaneously to obtain the local field potential (LFP) from the PFC, while the rats performed T-maze tasks for the evaluation of WM. Phase-amplitude coupling (PAC) was utilized to determine the effect of high-frequency rTMS on the theta-gamma coupling of LFPs. We observed that rats in the rTMS groups needed a smaller number of training days to complete the WM task as compared to the control group. High-frequency rTMS reinforced the coupling connection strength in the PFC of rats. Notably, the effect of rTMS at 15 Hz was the most effective among the three frequencies, i.e., 5 Hz, 10 Hz, and 15 Hz. The results suggested that rTMS can improve WM impairment in rats by modulating the coupling of theta and gamma rhythms. Hence, the current study provides a scientific basis for the optimization of TMS models, which would be relevant for clinical application.

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Funding

This work was supported by the National Natural Science Foundation of China (Grant numbers 51737003, 51677053, and 51707054), the Natural Foundation of Hebei Province, China (Grant numbers E2021202222); the S&T Program of Hebei, China (Grant numbers 18963001D, 215676146H, 225676163GH); the Natural Science Foundation of Tianjin, China (Grant numbers 20JCQNJC00710, 21JCZXJC00090); and the State Key Laboratory of Reliability and Intelligence of Electrical Equipment of Hebei University of Technology (Grant number No.EERI_OY2021009).

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Authors and Affiliations

  1. State Key Laboratory of Reliability and Intelligence of Electrical Equipment, Hebei University of Technology, Tianjin, 300130, China

    Miaomiao Guo, Tian Wang, Tianheng Zhang, Haodi Zhai & Guizhi Xu

  2. School of Health Sciences & Biomedical Engineering, Hebei University of Technology, Tianjin, 300130, China

    Miaomiao Guo, Tian Wang, Tianheng Zhang, Haodi Zhai & Guizhi Xu

  3. Tianjin Key Laboratory of Bioelectromagnetic Technology and Intelligent Health, Hebei University of Technology, Tianjin, 300130, China

    Miaomiao Guo, Tian Wang, Tianheng Zhang, Haodi Zhai & Guizhi Xu

  4. Hebei Key Laboratory of Bioelectromagnetics and Neuroengineering, Hebei University of Technology, Tianjin, 300130, China

    Miaomiao Guo, Tian Wang, Tianheng Zhang, Haodi Zhai & Guizhi Xu

  5. School of Mechanical and Electrical Engineering, Shijiazhuang University, Shijiazhuang, 050035, Hebei, China

    Tianheng Zhang

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  1. Miaomiao Guo
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  2. Tian Wang
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Contributions

MG: developed the study concept, designed the study, and revised the manuscript. TW: data analysis and drafted and revised the manuscript. TZ: implementation of some experiments. HZ: data analysis. GX: developed the study concept. All authors approved the final version of the manuscript for submission.

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Correspondence to Miaomiao Guo.

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All the authors confirm that all animal experiments complied with the ARRIVE guidelines and were carried out in accordance with the UK Animals (Scientific Procedures) Act, 1986 and associated guidelines, EU Directive 2010/63/EU for animal experiments, or the National Research Council’s Guide for the Care and Use of Laboratory Animals.

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Guo, M., Wang, T., Zhang, T. et al. Effects of high-frequency transcranial magnetic stimulation on theta-gamma oscillations and coupling in the prefrontal cortex of rats during working memory task. Med Biol Eng Comput 61, 3209–3223 (2023). https://doi.org/10.1007/s11517-023-02940-w

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  • DOI: https://doi.org/10.1007/s11517-023-02940-w

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