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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Main Authors: Ching-Wen Chang, Yu-Chun Lo, Sheng-Huang Lin, Shih-Hung Yang, Hui-Ching Lin, Ting-Chun Lin, Ssu-Ju Li, Christine Chin-jung Hsieh, Vina Ro, Yueh-Jung Chung, Yun-Chi Chang, Chi-Wei Lee, Chao-Hung Kuo, Shin-Yuan Chen, You-Yin Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2019.01269/full
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language English
format Article
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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
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spelling 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