Modulation of Theta-Band Local Field Potential Oscillations Across Brain Networks With Central Thalamic Deep Brain Stimulation to Enhance Spatial Working Memory
Deep brain stimulation (DBS) is a well-established technique for the treatment of movement and psychiatric disorders through the modulation of neural oscillatory activity and synaptic plasticity. The central thalamus (CT) has been indicated as a potential target for stimulation to enhance memory. Ho...
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Frontiers Media S.A.
2019-11-01
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Series: | Frontiers in Neuroscience |
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Online Access: | https://www.frontiersin.org/article/10.3389/fnins.2019.01269/full |
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Article |
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DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Ching-Wen Chang Yu-Chun Lo Sheng-Huang Lin Sheng-Huang Lin Shih-Hung Yang Hui-Ching Lin Ting-Chun Lin Ssu-Ju Li Christine Chin-jung Hsieh Christine Chin-jung Hsieh Vina Ro Yueh-Jung Chung Yun-Chi Chang Chi-Wei Lee Chi-Wei Lee Chao-Hung Kuo Chao-Hung Kuo Chao-Hung Kuo Shin-Yuan Chen Shin-Yuan Chen You-Yin Chen You-Yin Chen You-Yin Chen |
spellingShingle |
Ching-Wen Chang Yu-Chun Lo Sheng-Huang Lin Sheng-Huang Lin Shih-Hung Yang Hui-Ching Lin Ting-Chun Lin Ssu-Ju Li Christine Chin-jung Hsieh Christine Chin-jung Hsieh Vina Ro Yueh-Jung Chung Yun-Chi Chang Chi-Wei Lee Chi-Wei Lee Chao-Hung Kuo Chao-Hung Kuo Chao-Hung Kuo Shin-Yuan Chen Shin-Yuan Chen You-Yin Chen You-Yin Chen You-Yin Chen Modulation of Theta-Band Local Field Potential Oscillations Across Brain Networks With Central Thalamic Deep Brain Stimulation to Enhance Spatial Working Memory Frontiers in Neuroscience central thalamus deep brain stimulation spatial working memory synaptic plasticity hippocampal theta oscillation |
author_facet |
Ching-Wen Chang Yu-Chun Lo Sheng-Huang Lin Sheng-Huang Lin Shih-Hung Yang Hui-Ching Lin Ting-Chun Lin Ssu-Ju Li Christine Chin-jung Hsieh Christine Chin-jung Hsieh Vina Ro Yueh-Jung Chung Yun-Chi Chang Chi-Wei Lee Chi-Wei Lee Chao-Hung Kuo Chao-Hung Kuo Chao-Hung Kuo Shin-Yuan Chen Shin-Yuan Chen You-Yin Chen You-Yin Chen You-Yin Chen |
author_sort |
Ching-Wen Chang |
title |
Modulation of Theta-Band Local Field Potential Oscillations Across Brain Networks With Central Thalamic Deep Brain Stimulation to Enhance Spatial Working Memory |
title_short |
Modulation of Theta-Band Local Field Potential Oscillations Across Brain Networks With Central Thalamic Deep Brain Stimulation to Enhance Spatial Working Memory |
title_full |
Modulation of Theta-Band Local Field Potential Oscillations Across Brain Networks With Central Thalamic Deep Brain Stimulation to Enhance Spatial Working Memory |
title_fullStr |
Modulation of Theta-Band Local Field Potential Oscillations Across Brain Networks With Central Thalamic Deep Brain Stimulation to Enhance Spatial Working Memory |
title_full_unstemmed |
Modulation of Theta-Band Local Field Potential Oscillations Across Brain Networks With Central Thalamic Deep Brain Stimulation to Enhance Spatial Working Memory |
title_sort |
modulation of theta-band local field potential oscillations across brain networks with central thalamic deep brain stimulation to enhance spatial working memory |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Neuroscience |
issn |
1662-453X |
publishDate |
2019-11-01 |
description |
Deep brain stimulation (DBS) is a well-established technique for the treatment of movement and psychiatric disorders through the modulation of neural oscillatory activity and synaptic plasticity. The central thalamus (CT) has been indicated as a potential target for stimulation to enhance memory. However, the mechanisms underlying local field potential (LFP) oscillations and memory enhancement by CT-DBS remain unknown. In this study, we used CT-DBS to investigate the mechanisms underlying the changes in oscillatory communication between the CT and hippocampus, both of which are involved in spatial working memory. Local field potentials (LFPs) were recorded from microelectrode array implanted in the CT, dentate gyrus, cornu ammonis (CA) region 1, and CA region 3. Functional connectivity (FC) strength was assessed by LFP–LFP coherence calculations for these brain regions. In addition, a T-maze behavioral task using a rat model was performed to assess the performance of spatial working memory. In DBS group, our results revealed that theta oscillations significantly increased in the CT and hippocampus compared with that in sham controls. As indicated by coherence, the FC between the CT and hippocampus significantly increased in the theta band after CT-DBS. Moreover, Western blotting showed that the protein expressions of the dopamine D1 and α4-nicotinic acetylcholine receptors were enhanced, whereas that of the dopamine D2 receptor decreased in the DBS group. In conclusion, the use of CT-DBS resulted in elevated theta oscillations, increased FC between the CT and hippocampus, and altered synaptic plasticity in the hippocampus, suggesting that CT-DBS is an effective approach for improving spatial working memory. |
topic |
central thalamus deep brain stimulation spatial working memory synaptic plasticity hippocampal theta oscillation |
url |
https://www.frontiersin.org/article/10.3389/fnins.2019.01269/full |
work_keys_str_mv |
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doaj-d97a71dd1fe44b518103df800671ca562020-11-25T01:58:23ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-11-011310.3389/fnins.2019.01269478206Modulation of Theta-Band Local Field Potential Oscillations Across Brain Networks With Central Thalamic Deep Brain Stimulation to Enhance Spatial Working MemoryChing-Wen Chang0Yu-Chun Lo1Sheng-Huang Lin2Sheng-Huang Lin3Shih-Hung Yang4Hui-Ching Lin5Ting-Chun Lin6Ssu-Ju Li7Christine Chin-jung Hsieh8Christine Chin-jung Hsieh9Vina Ro10Yueh-Jung Chung11Yun-Chi Chang12Chi-Wei Lee13Chi-Wei Lee14Chao-Hung Kuo15Chao-Hung Kuo16Chao-Hung Kuo17Shin-Yuan Chen18Shin-Yuan Chen19You-Yin Chen20You-Yin Chen21You-Yin Chen22Department of Biomedical Engineering, National Yang Ming University, Taipei, TaiwanThe Ph.D. Program for Neural Regenerative Medicine, College of Medical Science and Technology, Taipei Medical University, Taipei, TaiwanDepartment of Neurology, Hualien Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Hualien City, TaiwanDepartment of Neurology, School of Medicine, Tzu Chi University, Hualien City, TaiwanDepartment of Mechanical Engineering, National Cheng Kung University, Tainan, TaiwanDepartment and Institute of Physiology, National Yang Ming University, Taipei, TaiwanDepartment of Biomedical Engineering, National Yang Ming University, Taipei, TaiwanDepartment of Biomedical Engineering, National Yang Ming University, Taipei, TaiwanDepartment of Biomedical Engineering, National Yang Ming University, Taipei, TaiwanTaiwan International Graduate Program in Interdisciplinary Neuroscience, National Yang Ming University, Academia Sinica, Taipei, TaiwanDepartment of Biomedical Engineering, National Yang Ming University, Taipei, TaiwanDepartment and Institute of Physiology, National Yang Ming University, Taipei, TaiwanDepartment and Institute of Physiology, National Yang Ming University, Taipei, TaiwanThe Ph.D. Program for Neural Regenerative Medicine, College of Medical Science and Technology, Taipei Medical University, Taipei, TaiwanDepartment and Institute of Physiology, National Yang Ming University, Taipei, TaiwanDepartment of Biomedical Engineering, National Yang Ming University, Taipei, TaiwanDepartment of Neurosurgery, Taipei Veterans General Hospital, Neurological Institute, Taipei, TaiwanDepartment of Neurological Surgery, University of Washington, Seattle, WA, United States0Department of Neurosurgery, Hualien Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Hualien City, Taiwan1Department of Surgery, School of Medicine, Tzu Chi University, Hualien City, TaiwanDepartment of Biomedical Engineering, National Yang Ming University, Taipei, TaiwanThe Ph.D. Program for Neural Regenerative Medicine, College of Medical Science and Technology, Taipei Medical University, Taipei, TaiwanTaiwan International Graduate Program in Interdisciplinary Neuroscience, National Yang Ming University, Academia Sinica, Taipei, TaiwanDeep brain stimulation (DBS) is a well-established technique for the treatment of movement and psychiatric disorders through the modulation of neural oscillatory activity and synaptic plasticity. The central thalamus (CT) has been indicated as a potential target for stimulation to enhance memory. However, the mechanisms underlying local field potential (LFP) oscillations and memory enhancement by CT-DBS remain unknown. In this study, we used CT-DBS to investigate the mechanisms underlying the changes in oscillatory communication between the CT and hippocampus, both of which are involved in spatial working memory. Local field potentials (LFPs) were recorded from microelectrode array implanted in the CT, dentate gyrus, cornu ammonis (CA) region 1, and CA region 3. Functional connectivity (FC) strength was assessed by LFP–LFP coherence calculations for these brain regions. In addition, a T-maze behavioral task using a rat model was performed to assess the performance of spatial working memory. In DBS group, our results revealed that theta oscillations significantly increased in the CT and hippocampus compared with that in sham controls. As indicated by coherence, the FC between the CT and hippocampus significantly increased in the theta band after CT-DBS. Moreover, Western blotting showed that the protein expressions of the dopamine D1 and α4-nicotinic acetylcholine receptors were enhanced, whereas that of the dopamine D2 receptor decreased in the DBS group. In conclusion, the use of CT-DBS resulted in elevated theta oscillations, increased FC between the CT and hippocampus, and altered synaptic plasticity in the hippocampus, suggesting that CT-DBS is an effective approach for improving spatial working memory.https://www.frontiersin.org/article/10.3389/fnins.2019.01269/fullcentral thalamusdeep brain stimulationspatial working memorysynaptic plasticityhippocampal theta oscillation |