Spatio-temporal dynamics of cortical drive to human subthalamic nucleus neurons in Parkinson's disease
Pathological synchronisation of beta frequency (12–35Hz) oscillations between the subthalamic nucleus (STN) and cerebral cortex is thought to contribute to motor impairment in Parkinson's disease (PD). For this cortico-subthalamic oscillatory drive to be mechanistically important, it must influ...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2018-04-01
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| Series: | Neurobiology of Disease |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0969996118300019 |
| _version_ | 1818573223158087680 |
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| author | Andrew Sharott Alessandro Gulberti Wolfgang Hamel Johannes A. Köppen Alexander Münchau Carsten Buhmann Monika Pötter-Nerger Manfred Westphal Christian Gerloff Christian K.E. Moll Andreas K. Engel |
| author_facet | Andrew Sharott Alessandro Gulberti Wolfgang Hamel Johannes A. Köppen Alexander Münchau Carsten Buhmann Monika Pötter-Nerger Manfred Westphal Christian Gerloff Christian K.E. Moll Andreas K. Engel |
| author_sort | Andrew Sharott |
| collection | DOAJ |
| description | Pathological synchronisation of beta frequency (12–35Hz) oscillations between the subthalamic nucleus (STN) and cerebral cortex is thought to contribute to motor impairment in Parkinson's disease (PD). For this cortico-subthalamic oscillatory drive to be mechanistically important, it must influence the firing of STN neurons and, consequently, their downstream targets. Here, we examined the dynamics of synchronisation between STN LFPs and units with multiple cortical areas, measured using frontal ECoG, midline EEG and lateral EEG, during rest and movement. STN neurons lagged cortical signals recorded over midline (over premotor cortices) and frontal (over prefrontal cortices) with stable time delays, consistent with strong corticosubthalamic drive, and many neurons maintained these dynamics during movement. In contrast, most STN neurons desynchronised from lateral EEG signals (over primary motor cortices) during movement and those that did not had altered phase relations to the cortical signals. The strength of synchronisation between STN units and midline EEG in the high beta range (25–35Hz) correlated positively with the severity of akinetic-rigid motor symptoms across patients. Together, these results suggest that sustained synchronisation of STN neurons to premotor-cortical beta oscillations play an important role in disrupting the normal coding of movement in PD. |
| first_indexed | 2024-12-15T00:08:19Z |
| format | Article |
| id | doaj.art-6f91e57af8464e81beeed30f6c460b04 |
| institution | Directory Open Access Journal |
| issn | 1095-953X |
| language | English |
| last_indexed | 2024-12-15T00:08:19Z |
| publishDate | 2018-04-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Disease |
| spelling | doaj.art-6f91e57af8464e81beeed30f6c460b042022-12-21T22:42:40ZengElsevierNeurobiology of Disease1095-953X2018-04-011124962Spatio-temporal dynamics of cortical drive to human subthalamic nucleus neurons in Parkinson's diseaseAndrew Sharott0Alessandro Gulberti1Wolfgang Hamel2Johannes A. Köppen3Alexander Münchau4Carsten Buhmann5Monika Pötter-Nerger6Manfred Westphal7Christian Gerloff8Christian K.E. Moll9Andreas K. Engel10MRC Brain Network Dynamics Unit, Dept. of Pharmacology, University of Oxford, Oxford OX1 3TH, United Kingdom; Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Correspondence to: A. Sharott, MRC Brain Network Dynamics Unit, Dept. of Pharmacology, University of Oxford, Oxford OX13TH, United Kingdom.Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurosurgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurosurgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Paediatric and Adult Movement Disorders and Neuropsychiatry, Institute of Neurogenetics, University of Lübeck, Lübeck, Germany; Department of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurosurgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Correspondence to: C.K.E. Moll, Department of Neurophysiology and Pathophysiology, Basal Ganglia Physiology Group, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyPathological synchronisation of beta frequency (12–35Hz) oscillations between the subthalamic nucleus (STN) and cerebral cortex is thought to contribute to motor impairment in Parkinson's disease (PD). For this cortico-subthalamic oscillatory drive to be mechanistically important, it must influence the firing of STN neurons and, consequently, their downstream targets. Here, we examined the dynamics of synchronisation between STN LFPs and units with multiple cortical areas, measured using frontal ECoG, midline EEG and lateral EEG, during rest and movement. STN neurons lagged cortical signals recorded over midline (over premotor cortices) and frontal (over prefrontal cortices) with stable time delays, consistent with strong corticosubthalamic drive, and many neurons maintained these dynamics during movement. In contrast, most STN neurons desynchronised from lateral EEG signals (over primary motor cortices) during movement and those that did not had altered phase relations to the cortical signals. The strength of synchronisation between STN units and midline EEG in the high beta range (25–35Hz) correlated positively with the severity of akinetic-rigid motor symptoms across patients. Together, these results suggest that sustained synchronisation of STN neurons to premotor-cortical beta oscillations play an important role in disrupting the normal coding of movement in PD.http://www.sciencedirect.com/science/article/pii/S0969996118300019Parkinson's diseaseSubthalamic nucleusBeta oscillationsMotor cortexNeuronal synchronisation |
| spellingShingle | Andrew Sharott Alessandro Gulberti Wolfgang Hamel Johannes A. Köppen Alexander Münchau Carsten Buhmann Monika Pötter-Nerger Manfred Westphal Christian Gerloff Christian K.E. Moll Andreas K. Engel Spatio-temporal dynamics of cortical drive to human subthalamic nucleus neurons in Parkinson's disease Neurobiology of Disease Parkinson's disease Subthalamic nucleus Beta oscillations Motor cortex Neuronal synchronisation |
| title | Spatio-temporal dynamics of cortical drive to human subthalamic nucleus neurons in Parkinson's disease |
| title_full | Spatio-temporal dynamics of cortical drive to human subthalamic nucleus neurons in Parkinson's disease |
| title_fullStr | Spatio-temporal dynamics of cortical drive to human subthalamic nucleus neurons in Parkinson's disease |
| title_full_unstemmed | Spatio-temporal dynamics of cortical drive to human subthalamic nucleus neurons in Parkinson's disease |
| title_short | Spatio-temporal dynamics of cortical drive to human subthalamic nucleus neurons in Parkinson's disease |
| title_sort | spatio temporal dynamics of cortical drive to human subthalamic nucleus neurons in parkinson s disease |
| topic | Parkinson's disease Subthalamic nucleus Beta oscillations Motor cortex Neuronal synchronisation |
| url | http://www.sciencedirect.com/science/article/pii/S0969996118300019 |
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