Evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamics
Evoked resonant neural activity (ERNA) is induced by subthalamic deep brain stimulation (DBS) and was recently suggested as a marker of lead placement and contact selection in Parkinson's disease. Yet, its underlying mechanisms and how it is modulated by stimulation parameters are unclear. Here...
| Main Authors: | , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-03-01
|
| Series: | Neurobiology of Disease |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0969996123000335 |
| _version_ | 1811165436983640064 |
|---|---|
| author | Christoph Wiest Shenghong He Benoit Duchet Alek Pogosyan Moaad Benjaber Timothy Denison Harutomo Hasegawa Keyoumars Ashkan Fahd Baig Ilaria Bertaina Francesca Morgante Erlick A. Pereira Flavie Torrecillos Huiling Tan |
| author_facet | Christoph Wiest Shenghong He Benoit Duchet Alek Pogosyan Moaad Benjaber Timothy Denison Harutomo Hasegawa Keyoumars Ashkan Fahd Baig Ilaria Bertaina Francesca Morgante Erlick A. Pereira Flavie Torrecillos Huiling Tan |
| author_sort | Christoph Wiest |
| collection | DOAJ |
| description | Evoked resonant neural activity (ERNA) is induced by subthalamic deep brain stimulation (DBS) and was recently suggested as a marker of lead placement and contact selection in Parkinson's disease. Yet, its underlying mechanisms and how it is modulated by stimulation parameters are unclear. Here, we recorded local field potentials from 27 Parkinson's disease patients, while leads were externalised to scrutinise the ERNA. First, we show that ERNA in the time series waveform and spectrogram likely represent the same activity, which was contested before. Second, our results show that the ERNA has fast and slow dynamics during stimulation, consistent with the synaptic failure hypothesis. Third, we show that ERNA parameters are modulated by different DBS frequencies, intensities, medication states and stimulation modes (continuous DBS vs. adaptive DBS). These results suggest the ERNA might prove useful as a predictor of the best DBS frequency and lowest effective intensity in addition to contact selection. Changes with levodopa and DBS mode suggest that the ERNA may indicate the state of the cortico-basal ganglia circuit making it a putative biomarker to track clinical state in adaptive DBS. |
| first_indexed | 2024-04-10T15:37:07Z |
| format | Article |
| id | doaj.art-db0c6fc1a66b4d1897ee67d1ff60d886 |
| institution | Directory Open Access Journal |
| issn | 1095-953X |
| language | English |
| last_indexed | 2024-04-10T15:37:07Z |
| publishDate | 2023-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Disease |
| spelling | doaj.art-db0c6fc1a66b4d1897ee67d1ff60d8862023-02-13T04:06:55ZengElsevierNeurobiology of Disease1095-953X2023-03-01178106019Evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamicsChristoph Wiest0Shenghong He1Benoit Duchet2Alek Pogosyan3Moaad Benjaber4Timothy Denison5Harutomo Hasegawa6Keyoumars Ashkan7Fahd Baig8Ilaria Bertaina9Francesca Morgante10Erlick A. Pereira11Flavie Torrecillos12Huiling Tan13Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UKMedical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UKMedical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UKMedical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UKMedical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UKMedical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UKDepartment of Neurosurgery, King's College Hospital, Denmark Hill, London, UKDepartment of Neurosurgery, King's College Hospital, Denmark Hill, London, UKMedical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK; Neurosciences Research Centre, Molecular and Clinical Sciences Institute, St. George's, University of London, London, UKNeurosciences Research Centre, Molecular and Clinical Sciences Institute, St. George's, University of London, London, UK; Neurology Department, Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Lugano, SwitzerlandNeurosciences Research Centre, Molecular and Clinical Sciences Institute, St. George's, University of London, London, UKNeurosciences Research Centre, Molecular and Clinical Sciences Institute, St. George's, University of London, London, UKMedical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UKMedical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK; Corresponding author.Evoked resonant neural activity (ERNA) is induced by subthalamic deep brain stimulation (DBS) and was recently suggested as a marker of lead placement and contact selection in Parkinson's disease. Yet, its underlying mechanisms and how it is modulated by stimulation parameters are unclear. Here, we recorded local field potentials from 27 Parkinson's disease patients, while leads were externalised to scrutinise the ERNA. First, we show that ERNA in the time series waveform and spectrogram likely represent the same activity, which was contested before. Second, our results show that the ERNA has fast and slow dynamics during stimulation, consistent with the synaptic failure hypothesis. Third, we show that ERNA parameters are modulated by different DBS frequencies, intensities, medication states and stimulation modes (continuous DBS vs. adaptive DBS). These results suggest the ERNA might prove useful as a predictor of the best DBS frequency and lowest effective intensity in addition to contact selection. Changes with levodopa and DBS mode suggest that the ERNA may indicate the state of the cortico-basal ganglia circuit making it a putative biomarker to track clinical state in adaptive DBS.http://www.sciencedirect.com/science/article/pii/S0969996123000335Parkinson's diseaseDeep brain stimulationEvoked resonant neural activityAdaptive DBSLocal field potentialsSubthalamic nucleus |
| spellingShingle | Christoph Wiest Shenghong He Benoit Duchet Alek Pogosyan Moaad Benjaber Timothy Denison Harutomo Hasegawa Keyoumars Ashkan Fahd Baig Ilaria Bertaina Francesca Morgante Erlick A. Pereira Flavie Torrecillos Huiling Tan Evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamics Neurobiology of Disease Parkinson's disease Deep brain stimulation Evoked resonant neural activity Adaptive DBS Local field potentials Subthalamic nucleus |
| title | Evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamics |
| title_full | Evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamics |
| title_fullStr | Evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamics |
| title_full_unstemmed | Evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamics |
| title_short | Evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamics |
| title_sort | evoked resonant neural activity in subthalamic local field potentials reflects basal ganglia network dynamics |
| topic | Parkinson's disease Deep brain stimulation Evoked resonant neural activity Adaptive DBS Local field potentials Subthalamic nucleus |
| url | http://www.sciencedirect.com/science/article/pii/S0969996123000335 |
| work_keys_str_mv | AT christophwiest evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT shenghonghe evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT benoitduchet evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT alekpogosyan evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT moaadbenjaber evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT timothydenison evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT harutomohasegawa evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT keyoumarsashkan evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT fahdbaig evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT ilariabertaina evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT francescamorgante evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT erlickapereira evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT flavietorrecillos evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics AT huilingtan evokedresonantneuralactivityinsubthalamiclocalfieldpotentialsreflectsbasalganglianetworkdynamics |