Effect of repeated transcranial magnetic stimulation on excitability of glutaminergic neurons and gamma-aminobutyric neurons in mouse hippocampus_Journal of Biomedical Engineering

Authors：

WANG Jiale ^1,2 ,  DING Chong ^1,2 , FU Rui ^1,2 , ZHANG Ze ^1,2 , ZHAO Junqiao ^1,2 , ZHU Haijun ³

1. School of Health Sciences & Biomedical Engineering, Hebei University of Technology, Tianjin 300130, P. R. China;
2. Hebei Key Laboratory of Bioelectromagnetics and Neural Engineering, Hebei University of Technology, Tianjin 300130, P. R. China;
3. Key Laboralory of Digital Medical Engincering of Hebei Province, School of Electronic Information Engineering, Hebei Universily, Baoding, Hebei 071002, P. R. China;

Corresponding author：

DING Chong, Email: dingchong@hebut.edu.cn

Keywords：

Repetitive transcranial magnetic stimulation; Glutaminergic neurons; Gamma-aminobutyric neurons; Learning and memory; Fiber photometry; Brain patch clamp

DOI：

10.7507/1001-5515.202405025

Video：

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Repeated transcranial magnetic stimulation (rTMS) is one of the commonly used brain stimulation techniques. In order to investigate the effects of rTMS on the excitability of different types of neurons, this study is conducted to investigate the effects of rTMS on the cognitive function of mice and the excitability of hippocampal glutaminergic neurons and gamma-aminobutyric neurons from the perspective of electrophysiology. In this study, mice were randomly divided into glutaminergic control group, glutaminergic magnetic stimulation group, gamma-aminobutyric acid energy control group, and gamma-aminobutyric acid magnetic stimulation group. The four groups of mice were injected with adeno-associated virus to label two types of neurons and were implanted optical fiber. The stimulation groups received 14 days of stimulation and the control groups received 14 days of pseudo-stimulation. The fluorescence intensity of calcium ions in mice was recorded by optical fiber system. Behavioral experiments were conducted to explore the changes of cognitive function in mice. The patch-clamp system was used to detect the changes of neuronal action potential characteristics. The results showed that rTMS significantly improved the cognitive function of mice, increased the amplitude of calcium fluorescence of glutamergic neurons and gamma-aminobutyric neurons in the hippocampus, and enhanced the action potential related indexes of glutamergic neurons and gamma-aminobutyric neurons. The results suggest that rTMS can improve the cognitive ability of mice by enhancing the excitability of hippocampal glutaminergic neurons and gamma-aminobutyric neurons.

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2.	Klomjai W, Katz R, Lackmy-Vallée A. Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Ann Phys Rehabil Med, 2015, 58(4): 208-213.
3.	Arias-Carrion O, Machado S, Paes F, et al. Is rTMS an effective therapeutic strategy that can be used to treat Parkinson's disease?. CNS Neurol Disord Drug Targets, 2011, 10(6): 693-702.
4.	Konstantinou G, Hui J, Ortiz A, et al. Repetitive transcranial magnetic stimulation (rTMS) in bipolar disorder: A systematic review. Bipolar Disord, 2022, 24(1): 10-26.
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6.	Tambini A, Nee D E, D’Esposito M. Hippocampal-targeted theta-burst stimulation enhances associative memory formation. J Cogn Neurosci, 2018, 30(10): 1452-1472.
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8.	Chameh H M, Janahmadi M, Semnanian S, et al. Effect of low frequency repetitive transcranial magnetic stimulation on kindling-induced changes in electrophysiological properties of rat CA1 pyramidal neurons. Brain Res, 2015, 1606: 34-43.
9.	朱海军, 丁冲, 李洋, 等. 重复经颅磁刺激显著改善小鼠老化过程中认知损伤及提高神经元兴奋性. 生物医学工程学杂志, 2020, 37(3): 380-388.
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12.	Innocenti G M. Defining neuroplasticity. Handb Clin Neurol, 2022, 184: 3-18.
13.	Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci, 2008, 9(3): 206-221.
14.	Perrenoud Q, Leclerc C, Geoffroy H, et al. Molecular and electrophysiological features of GABAergic neurons in the dentate gyrus reveal limited homology with cortical interneurons. PLoS One, 2022, 17(7): e0270981.
15.	Lee S H, Sheng M. Development of neuron-neuron synapses. Curr Opin Neurobiol, 2000, 10(1): 125-131.
16.	Achim K, Salminen M, Partanen J. Mechanisms regulating GABAergic neuron development. Cell Mol Life Sci, 2014, 71(8): 1395-1415.
17.	Li Y C, Wang Q, Li M G, et al. A paraventricular hypothalamic nucleus input to ventral of lateral septal nucleus controls chronic visceral pain. Pain, 2023, 164(3): 625-637.
18.	Chen L, Mckenna J T, Leonard M Z, et al. GAD67-GFP knock-in mice have normal sleep-wake patterns and sleep homeostasis. Neuroreport, 2010, 21(3): 216-220.
19.	Kaech S, Banker G. Culturing hippocampal neurons. Nat Protoc, 2006, 1(5): 2406-2415.
20.	Zhao Z, Gu H. Transitions between classes of neuronal excitability and bifurcations induced by autapse. Sci Rep, 2017, 7(1): 6760.
21.	Tan T, Xie J, Tong Z, et al. Repetitive transcranial magnetic stimulation increases excitability of hippocampal CA1 pyramidal neurons. Brain Res, 2013, 1520: 23-35.
22.	Jannati A, Oberman L M, Rotenberg A, et al. Assessing the mechanisms of brain plasticity by transcranial magnetic stimulation. Neuropsychopharmacology, 2023, 48(1): 191-208.
23.	Prestigio C, Ferrante D, Valente P, et al. Spike-related electrophysiological identification of cultured hippocampal excitatory and inhibitory neurons. Mol Neurobiol, 2019, 56(9): 6276-6292.
24.	Leger M, Quiedeville A, Bouet V, et al. Object recognition test in mice. Nat Protoc, 2013, 8(12): 2531-2537.
25.	Vorhees C V, Williams M T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc, 2006, 1(2): 848-858.
26.	侯文涛, 付蕊, 朱明强, 等. 重复经颅磁刺激对后肢去负荷小鼠神经元兴奋性及离子通道影响的研究. 生物医学工程学杂志, 2023, 40(1): 8-19.
27.	Zhu H, Yin X, Yang H, et al. Repetitive transcranial magnetic stimulation enhances the neuronal excitability of mice by regulating dynamic characteristics of Granule cells’ Ion channels. Cogn Neurodyn, 2023, 17(2): 431-443.

1. Zong X, Gu J, Geng D, et al. Repetitive transcranial magnetic stimulation (rTMS) for multiple neurological conditions in rodent animal models: A systematic review. Neurochem Int, 2022, 157: 105356.
2. Klomjai W, Katz R, Lackmy-Vallée A. Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Ann Phys Rehabil Med, 2015, 58(4): 208-213.
3. Arias-Carrion O, Machado S, Paes F, et al. Is rTMS an effective therapeutic strategy that can be used to treat Parkinson's disease?. CNS Neurol Disord Drug Targets, 2011, 10(6): 693-702.
4. Konstantinou G, Hui J, Ortiz A, et al. Repetitive transcranial magnetic stimulation (rTMS) in bipolar disorder: A systematic review. Bipolar Disord, 2022, 24(1): 10-26.
5. Koch G, Spampinato D. Alzheimer disease and neuroplasticity. Handb Clin Neurol, 2022, 184: 473-479.
6. Tambini A, Nee D E, D’Esposito M. Hippocampal-targeted theta-burst stimulation enhances associative memory formation. J Cogn Neurosci, 2018, 30(10): 1452-1472.
7. Maeda F, Keenan J P, Tormos J M, et al. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol, 2000, 111(5): 800-805.
8. Chameh H M, Janahmadi M, Semnanian S, et al. Effect of low frequency repetitive transcranial magnetic stimulation on kindling-induced changes in electrophysiological properties of rat CA1 pyramidal neurons. Brain Res, 2015, 1606: 34-43.
9. 朱海军, 丁冲, 李洋, 等. 重复经颅磁刺激显著改善小鼠老化过程中认知损伤及提高神经元兴奋性. 生物医学工程学杂志, 2020, 37(3): 380-388.
10. Knierim J J. The hippocampus. Curr Biol, 2015, 25(23): R1116-R1121.
11. Hermiller M S, Vanhaerents S, Raij T, et al. Frequency-specific noninvasive modulation of memory retrieval and its relationship with hippocampal network connectivity. Hippocampus, 2019, 29(7): 595-609.
12. Innocenti G M. Defining neuroplasticity. Handb Clin Neurol, 2022, 184: 3-18.
13. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci, 2008, 9(3): 206-221.
14. Perrenoud Q, Leclerc C, Geoffroy H, et al. Molecular and electrophysiological features of GABAergic neurons in the dentate gyrus reveal limited homology with cortical interneurons. PLoS One, 2022, 17(7): e0270981.
15. Lee S H, Sheng M. Development of neuron-neuron synapses. Curr Opin Neurobiol, 2000, 10(1): 125-131.
16. Achim K, Salminen M, Partanen J. Mechanisms regulating GABAergic neuron development. Cell Mol Life Sci, 2014, 71(8): 1395-1415.
17. Li Y C, Wang Q, Li M G, et al. A paraventricular hypothalamic nucleus input to ventral of lateral septal nucleus controls chronic visceral pain. Pain, 2023, 164(3): 625-637.
18. Chen L, Mckenna J T, Leonard M Z, et al. GAD67-GFP knock-in mice have normal sleep-wake patterns and sleep homeostasis. Neuroreport, 2010, 21(3): 216-220.
19. Kaech S, Banker G. Culturing hippocampal neurons. Nat Protoc, 2006, 1(5): 2406-2415.
20. Zhao Z, Gu H. Transitions between classes of neuronal excitability and bifurcations induced by autapse. Sci Rep, 2017, 7(1): 6760.
21. Tan T, Xie J, Tong Z, et al. Repetitive transcranial magnetic stimulation increases excitability of hippocampal CA1 pyramidal neurons. Brain Res, 2013, 1520: 23-35.
22. Jannati A, Oberman L M, Rotenberg A, et al. Assessing the mechanisms of brain plasticity by transcranial magnetic stimulation. Neuropsychopharmacology, 2023, 48(1): 191-208.
23. Prestigio C, Ferrante D, Valente P, et al. Spike-related electrophysiological identification of cultured hippocampal excitatory and inhibitory neurons. Mol Neurobiol, 2019, 56(9): 6276-6292.
24. Leger M, Quiedeville A, Bouet V, et al. Object recognition test in mice. Nat Protoc, 2013, 8(12): 2531-2537.
25. Vorhees C V, Williams M T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc, 2006, 1(2): 848-858.
26. 侯文涛, 付蕊, 朱明强, 等. 重复经颅磁刺激对后肢去负荷小鼠神经元兴奋性及离子通道影响的研究. 生物医学工程学杂志, 2023, 40(1): 8-19.
27. Zhu H, Yin X, Yang H, et al. Repetitive transcranial magnetic stimulation enhances the neuronal excitability of mice by regulating dynamic characteristics of Granule cells’ Ion channels. Cogn Neurodyn, 2023, 17(2): 431-443.

Journal of Biomedical Engineering

Latest ArticlesEffect of repeated transcranial magnetic stimulation on excitability of glutaminergic neurons and gamma-aminobutyric neurons in mouse hippocampus

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