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Research Articles, Behavioral/Cognitive

Multisession Anodal Transcranial Direct Current Stimulation Enhances Adult Hippocampal Neurogenesis and Context Discrimination in Mice

Ting-Hsuan Yu, Yi-Jen Wu, Miao-Er Chien and Kuei-Sen Hsu
Journal of Neuroscience 25 January 2023, 43 (4) 635-646; DOI: https://doi.org/10.1523/JNEUROSCI.1476-22.2022
Ting-Hsuan Yu
1Institute of Basic Medical Sciences, College of Medicine, National Cheng Kung University, Tainan 70101, Taiwan
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Yi-Jen Wu
2Department of Neurology, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan 70457, Taiwan
3Institute of Clinical Medicine, College of Medicine, National Cheng Kung University, Tainan 70457, Taiwan
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Miao-Er Chien
2Department of Neurology, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan 70457, Taiwan
3Institute of Clinical Medicine, College of Medicine, National Cheng Kung University, Tainan 70457, Taiwan
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Kuei-Sen Hsu
1Institute of Basic Medical Sciences, College of Medicine, National Cheng Kung University, Tainan 70101, Taiwan
4Department of Pharmacology, College of Medicine, National Cheng Kung University, Tainan 70101, Taiwan
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Abstract

Transcranial direct current stimulation (tDCS) is a promising noninvasive neuromodulatory treatment option for multiple neurologic and psychiatric disorders, but its mechanism of action is still poorly understood. Adult hippocampal neurogenesis (AHN) continues throughout life and is crucial for preserving several aspects of hippocampal-dependent cognitive functions. Nevertheless, the contribution of AHN in the neuromodulatory effects of tDCS remains unexplored. Here, we sought to investigate whether multisession anodal tDCS may modulate AHN and its associated cognitive functions. Multisession anodal tDCS were applied on the skull over the hippocampus of adult male mice for 20 min at 0.25 mA once daily for 10 d totally. We found that multisession anodal tDCS enhances AHN by increasing the proliferation, differentiation and survival of neural stem/progenitor cells (NSPCs). In addition, tDCS treatment increased cell cycle reentry and reduced cell cycle exit of NSPCs. The tDCS-treated mice exhibited a reduced GABAergic inhibitory tone in the dentate gyrus compared with sham-treated mice. The effect of tDCS on the proliferation of NSPCs was blocked by pharmacological restoration of GABAB receptor-mediated inhibition. Functionally, multisession anodal tDCS enhances performance on a contextual fear discrimination task, and this enhancement was prevented by blocking AHN using the DNA alkylating agent temozolomide (TMZ). Our results emphasize an important role for AHN in mediating the beneficial effects of tDCS on cognitive functions that substantially broadens the mechanistic understanding of tDCS beyond its well-described in hippocampal synaptic plasticity.

SIGNIFICANCE STATEMENT Transcranial direct current stimulation (tDCS) has been shown to effectively enhance cognitive functions in healthy and pathologic conditions. However, the mechanisms underlying its effects are largely unknown and need to be better understood to enable its optimal clinical use. This study shows that multisession anodal tDCS enhances adult hippocampal neurogenesis (AHN) and therefore contributes to enhance context discrimination in mice. Our results also show that the effect of tDCS on AHN is associated with reduced GABAergic inhibition in the dentate gyrus. Our study uncovers a novel mechanism of anodal tDCS to elicit cognitive-enhancing effects and may have the potential to improve cognitive decline associated with normal aging and neurodegenerative disorders.

  • adult neurogenesis
  • context discrimination
  • GABAergic inhibition
  • hippocampus
  • neural stem/progenitor cells
  • transcranial direct current stimulation

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The Journal of Neuroscience: 43 (4)
Journal of Neuroscience
Vol. 43, Issue 4
25 Jan 2023
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Multisession Anodal Transcranial Direct Current Stimulation Enhances Adult Hippocampal Neurogenesis and Context Discrimination in Mice
Ting-Hsuan Yu, Yi-Jen Wu, Miao-Er Chien, Kuei-Sen Hsu
Journal of Neuroscience 25 January 2023, 43 (4) 635-646; DOI: 10.1523/JNEUROSCI.1476-22.2022

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Multisession Anodal Transcranial Direct Current Stimulation Enhances Adult Hippocampal Neurogenesis and Context Discrimination in Mice
Ting-Hsuan Yu, Yi-Jen Wu, Miao-Er Chien, Kuei-Sen Hsu
Journal of Neuroscience 25 January 2023, 43 (4) 635-646; DOI: 10.1523/JNEUROSCI.1476-22.2022
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Keywords

  • adult neurogenesis
  • context discrimination
  • GABAergic inhibition
  • hippocampus
  • neural stem/progenitor cells
  • transcranial direct current stimulation

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