Spectral characteristics of subthalamic nucleus local field potentials in Parkinson's disease: Phenotype and movement matter
Parkinson's disease (PD) is clinically heterogeneous across patients and may be classified in three motor phenotypes: tremor dominant (TD), postural instability and gait disorder (PIGD), and undetermined. Despite the significant clinical characterization of motor phenotypes, little is known abo...
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Published in: | The European journal of neuroscience Vol. 53; no. 8; pp. 2804 - 2818 |
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Abstract | Parkinson's disease (PD) is clinically heterogeneous across patients and may be classified in three motor phenotypes: tremor dominant (TD), postural instability and gait disorder (PIGD), and undetermined. Despite the significant clinical characterization of motor phenotypes, little is known about how electrophysiological data, particularly subthalamic nucleus local field potentials (STN‐LFP), differ between TD and PIGD patients. This is relevant since increased STN‐LFP bandpower at α–β range (8–35 Hz) is considered a potential PD biomarker and, therefore, a critical setpoint to drive adaptive deep brain stimulation. Acknowledging STN‐LFP differences between phenotypes, mainly in rest and movement states, would better fit DBS to clinical and motor demands. We studied this issue through spectral analyses on 35 STN‐LFP in TD and PIGD patients during rest and movement. We demonstrated that higher β2 activity (22–35 Hz) was observed in PIGD only during rest. Additionally, bandpower differences between rest and movement occurred at the α–β range, but with different patterns as per phenotypes: movement‐induced desynchronization concerned lower frequencies in TD (10–20 Hz) and higher frequencies in PIGD patients (21–28 Hz). Finally, when supervised learning algorithms were employed aiming to discriminate PD phenotypes based on STN‐LFP bandpower features, movement information had improved the classification accuracy, achieving peak performances when TD and PIGD movement‐induced desynchronization ranges were considered. These results suggest that STN‐LFP β‐band encodes phenotype‐movement dependent information in PD patients.
Spectral characterization of local field potentials (LFPs) from the Subthalamic Nucleus (STN) during the intra‐operative procedure was performed in rest and movement conditions for tremor dominant (TD) and postural instability and gait disorder (PIGD) Parkinson's disease patients. A higher β2 activity (22–35 Hz) was observed for PIGD patients in rest, while a phenotype‐dependent movement‐induced desynchronization was observed in lower frequencies (10‐20 Hz) for TD, and in higher frequencies (21–28 Hz) for PIGD. Besides, multifactorial statistical analysis, machine learning‐based algorithms using bandpower features in the mentioned frequency ranges achieved better phenotype discriminatory performance, suggesting that STN‐LFP encodes phenotype‐movement dependent information in Parkinson’s disease. |
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AbstractList | Parkinson's disease (PD) is clinically heterogeneous across patients and may be classified in three motor phenotypes: tremor dominant (TD), postural instability and gait disorder (PIGD), and undetermined. Despite the significant clinical characterization of motor phenotypes, little is known about how electrophysiological data, particularly subthalamic nucleus local field potentials (STN‐LFP), differ between TD and PIGD patients. This is relevant since increased STN‐LFP bandpower at α–β range (8–35 Hz) is considered a potential PD biomarker and, therefore, a critical setpoint to drive adaptive deep brain stimulation. Acknowledging STN‐LFP differences between phenotypes, mainly in rest and movement states, would better fit DBS to clinical and motor demands. We studied this issue through spectral analyses on 35 STN‐LFP in TD and PIGD patients during rest and movement. We demonstrated that higher β2 activity (22–35 Hz) was observed in PIGD only during rest. Additionally, bandpower differences between rest and movement occurred at the α–β range, but with different patterns as per phenotypes: movement‐induced desynchronization concerned lower frequencies in TD (10–20 Hz) and higher frequencies in PIGD patients (21–28 Hz). Finally, when supervised learning algorithms were employed aiming to discriminate PD phenotypes based on STN‐LFP bandpower features, movement information had improved the classification accuracy, achieving peak performances when TD and PIGD movement‐induced desynchronization ranges were considered. These results suggest that STN‐LFP β‐band encodes phenotype‐movement dependent information in PD patients. Parkinson's disease (PD) is clinically heterogeneous across patients and may be classified in three motor phenotypes: tremor dominant (TD), postural instability and gait disorder (PIGD), and undetermined. Despite the significant clinical characterization of motor phenotypes, little is known about how electrophysiological data, particularly subthalamic nucleus local field potentials (STN‐LFP), differ between TD and PIGD patients. This is relevant since increased STN‐LFP bandpower at α–β range (8–35 Hz) is considered a potential PD biomarker and, therefore, a critical setpoint to drive adaptive deep brain stimulation. Acknowledging STN‐LFP differences between phenotypes, mainly in rest and movement states, would better fit DBS to clinical and motor demands. We studied this issue through spectral analyses on 35 STN‐LFP in TD and PIGD patients during rest and movement. We demonstrated that higher β 2 activity (22–35 Hz) was observed in PIGD only during rest. Additionally, bandpower differences between rest and movement occurred at the α–β range, but with different patterns as per phenotypes: movement‐induced desynchronization concerned lower frequencies in TD (10–20 Hz) and higher frequencies in PIGD patients (21–28 Hz). Finally, when supervised learning algorithms were employed aiming to discriminate PD phenotypes based on STN‐LFP bandpower features, movement information had improved the classification accuracy, achieving peak performances when TD and PIGD movement‐induced desynchronization ranges were considered. These results suggest that STN‐LFP β‐band encodes phenotype‐movement dependent information in PD patients. Parkinson's disease (PD) is clinically heterogeneous across patients and may be classified in three motor phenotypes: tremor dominant (TD), postural instability and gait disorder (PIGD), and undetermined. Despite the significant clinical characterization of motor phenotypes, little is known about how electrophysiological data, particularly subthalamic nucleus local field potentials (STN‐LFP), differ between TD and PIGD patients. This is relevant since increased STN‐LFP bandpower at α–β range (8–35 Hz) is considered a potential PD biomarker and, therefore, a critical setpoint to drive adaptive deep brain stimulation. Acknowledging STN‐LFP differences between phenotypes, mainly in rest and movement states, would better fit DBS to clinical and motor demands. We studied this issue through spectral analyses on 35 STN‐LFP in TD and PIGD patients during rest and movement. We demonstrated that higher β2 activity (22–35 Hz) was observed in PIGD only during rest. Additionally, bandpower differences between rest and movement occurred at the α–β range, but with different patterns as per phenotypes: movement‐induced desynchronization concerned lower frequencies in TD (10–20 Hz) and higher frequencies in PIGD patients (21–28 Hz). Finally, when supervised learning algorithms were employed aiming to discriminate PD phenotypes based on STN‐LFP bandpower features, movement information had improved the classification accuracy, achieving peak performances when TD and PIGD movement‐induced desynchronization ranges were considered. These results suggest that STN‐LFP β‐band encodes phenotype‐movement dependent information in PD patients. Spectral characterization of local field potentials (LFPs) from the Subthalamic Nucleus (STN) during the intra‐operative procedure was performed in rest and movement conditions for tremor dominant (TD) and postural instability and gait disorder (PIGD) Parkinson's disease patients. A higher β2 activity (22–35 Hz) was observed for PIGD patients in rest, while a phenotype‐dependent movement‐induced desynchronization was observed in lower frequencies (10‐20 Hz) for TD, and in higher frequencies (21–28 Hz) for PIGD. Besides, multifactorial statistical analysis, machine learning‐based algorithms using bandpower features in the mentioned frequency ranges achieved better phenotype discriminatory performance, suggesting that STN‐LFP encodes phenotype‐movement dependent information in Parkinson’s disease. Parkinson's disease (PD) is clinically heterogeneous across patients and may be classified in three motor phenotypes: tremor dominant (TD), postural instability and gait disorder (PIGD), and undetermined. Despite the significant clinical characterization of motor phenotypes, little is known about how electrophysiological data, particularly subthalamic nucleus local field potentials (STN-LFP), differ between TD and PIGD patients. This is relevant since increased STN-LFP bandpower at α-β range (8-35 Hz) is considered a potential PD biomarker and, therefore, a critical setpoint to drive adaptive deep brain stimulation. Acknowledging STN-LFP differences between phenotypes, mainly in rest and movement states, would better fit DBS to clinical and motor demands. We studied this issue through spectral analyses on 35 STN-LFP in TD and PIGD patients during rest and movement. We demonstrated that higher β activity (22-35 Hz) was observed in PIGD only during rest. Additionally, bandpower differences between rest and movement occurred at the α-β range, but with different patterns as per phenotypes: movement-induced desynchronization concerned lower frequencies in TD (10-20 Hz) and higher frequencies in PIGD patients (21-28 Hz). Finally, when supervised learning algorithms were employed aiming to discriminate PD phenotypes based on STN-LFP bandpower features, movement information had improved the classification accuracy, achieving peak performances when TD and PIGD movement-induced desynchronization ranges were considered. These results suggest that STN-LFP β-band encodes phenotype-movement dependent information in PD patients. |
Author | Rocha, Maria Sheila Soriano, Diogo Coutinho Terzian Filho, Paulo Roberto Takahata, André Kazuo Figueiredo, Eberval Gadelha Yoneyama, Takashi Godinho, Fabio Almeida, Tiago Paggi Bianqueti, Bruno Leonardo Varjão, Eduardo Smith, Yoland Luccas, Julia Baldi Fim Neto, Arnaldo |
Author_xml | – sequence: 1 givenname: Fabio orcidid: 0000-0002-7100-4303 surname: Godinho fullname: Godinho, Fabio email: godinho.f1@gmail.com.br organization: University of São Paulo Medical School – sequence: 2 givenname: Arnaldo surname: Fim Neto fullname: Fim Neto, Arnaldo organization: University of Campinas – sequence: 3 givenname: Bruno Leonardo surname: Bianqueti fullname: Bianqueti, Bruno Leonardo organization: Brazilian Institute of Neuroscience and Neurotechnology – sequence: 4 givenname: Julia Baldi surname: Luccas fullname: Luccas, Julia Baldi organization: Brazilian Institute of Neuroscience and Neurotechnology – sequence: 5 givenname: Eduardo surname: Varjão fullname: Varjão, Eduardo organization: Santa Marcelina Hospital – sequence: 6 givenname: Paulo Roberto surname: Terzian Filho fullname: Terzian Filho, Paulo Roberto organization: Santa Marcelina Hospital – sequence: 7 givenname: Eberval Gadelha surname: Figueiredo fullname: Figueiredo, Eberval Gadelha organization: Medicine School – sequence: 8 givenname: Tiago Paggi surname: Almeida fullname: Almeida, Tiago Paggi organization: University of Leicester – sequence: 9 givenname: Takashi surname: Yoneyama fullname: Yoneyama, Takashi organization: Technological Institute of Aeronautics – sequence: 10 givenname: André Kazuo surname: Takahata fullname: Takahata, André Kazuo organization: Brazilian Institute of Neuroscience and Neurotechnology – sequence: 11 givenname: Maria Sheila surname: Rocha fullname: Rocha, Maria Sheila organization: Santa Marcelina Hospital – sequence: 12 givenname: Diogo Coutinho surname: Soriano fullname: Soriano, Diogo Coutinho organization: Brazilian Institute of Neuroscience and Neurotechnology – sequence: 13 givenname: Yoland surname: Smith fullname: Smith, Yoland |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33393163$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_clinph_2022_05_013 crossref_primary_10_1007_s00415_022_11388_1 crossref_primary_10_1002_mds_29393 crossref_primary_10_1016_j_expneurol_2022_114150 crossref_primary_10_1113_JP284768 crossref_primary_10_3389_fnins_2021_733203 crossref_primary_10_1016_j_neurom_2023_01_006 crossref_primary_10_3389_fneur_2021_723476 crossref_primary_10_1016_j_wneu_2022_04_084 crossref_primary_10_3233_JPD_225053 crossref_primary_10_3389_fnhum_2022_958521 crossref_primary_10_1007_s11055_024_01594_x crossref_primary_10_31857_S0044467723060059 crossref_primary_10_1038_s41531_022_00443_3 |
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Snippet | Parkinson's disease (PD) is clinically heterogeneous across patients and may be classified in three motor phenotypes: tremor dominant (TD), postural... |
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SubjectTerms | biomarkers brain waves Deep brain stimulation Electrical stimuli Gait Learning algorithms Movement disorders Neurodegenerative diseases neurology neurosurgery Parkinson's disease Phenotypes physiology Solitary tract nucleus Subthalamic nucleus Synchronization Tremor |
Title | Spectral characteristics of subthalamic nucleus local field potentials in Parkinson's disease: Phenotype and movement matter |
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