Beta bursts in the parkinsonian cortico-basal ganglia network form spatially discrete ensembles
Defining spatial synchronisation of pathological beta oscillations is important, given that many theories linking them to parkinsonian symptoms propose a reduction in the dimensionality of the coding space within and/or across cortico-basal ganglia structures. Such spatial synchronisation could aris...
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Elsevier
2024-10-01
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| Series: | Neurobiology of Disease |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0969996124002523 |
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| author | Isaac Grennan Nicolas Mallet Peter J. Magill Hayriye Cagnan Andrew Sharott |
| author_facet | Isaac Grennan Nicolas Mallet Peter J. Magill Hayriye Cagnan Andrew Sharott |
| author_sort | Isaac Grennan |
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| description | Defining spatial synchronisation of pathological beta oscillations is important, given that many theories linking them to parkinsonian symptoms propose a reduction in the dimensionality of the coding space within and/or across cortico-basal ganglia structures. Such spatial synchronisation could arise from a single process, with widespread entrainment of neurons to the same oscillation. Alternatively, the partially segregated structure of cortico-basal ganglia loops could provide a substrate for multiple ensembles that are independently synchronized at beta frequencies. Addressing this question requires an analytical approach that identifies groups of signals with a statistical tendency for beta synchronisation, which is unachievable using standard pairwise measures. Here, we utilized such an approach on multichannel recordings of background unit activity (BUA) in the external globus pallidus (GP) and subthalamic nucleus (STN) in parkinsonian rats. We employed an adapted version of a principle and independent component analysis-based method commonly used to define assemblies of single neurons (i.e., neurons that are synchronized over short timescales). This analysis enabled us to define whether changes in the power of beta oscillations in local ensembles of neurons (i.e., the BUA recorded from single contacts) consistently covaried over time, forming a “beta ensemble”. Multiple beta ensembles were often present in single recordings and could span brain structures. Membership of a beta ensemble predicted significantly higher levels of short latency (<5 ms) synchrony in the raw BUA signal and phase synchronisation with cortical beta oscillations, suggesting that they comprised clusters of neurons that are functionally connected at multiple levels, despite sometimes being non-contiguous in space. Overall, these findings suggest that beta oscillations do not comprise of a single synchronisation process, but rather multiple independent activities that can bind both spatially contiguous and non-contiguous pools of neurons within and across structures. As previously proposed, such ensembles provide a substrate for beta oscillations to constrain the coding space of cortico-basal ganglia circuits. |
| format | Article |
| id | doaj-art-3493040dbaec47f6af013ec8f8b6a635 |
| institution | OA Journals |
| issn | 1095-953X |
| language | English |
| publishDate | 2024-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Disease |
| spelling | doaj-art-3493040dbaec47f6af013ec8f8b6a6352025-08-20T01:48:03ZengElsevierNeurobiology of Disease1095-953X2024-10-0120110665210.1016/j.nbd.2024.106652Beta bursts in the parkinsonian cortico-basal ganglia network form spatially discrete ensemblesIsaac Grennan0Nicolas Mallet1Peter J. Magill2Hayriye Cagnan3Andrew Sharott4Medical Research Council Brain Network Dynamics Unit, Nuffield Deptartment of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH, United KingdomUniversite de Bordeaux, Institut des Maladies Neurodégénératives, 33076 Bordeaux, France; CNRS UMR 5293, Institut des Maladies Neurodégénératives, 33076 Bordeaux, FranceMedical Research Council Brain Network Dynamics Unit, Nuffield Deptartment of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH, United KingdomMedical Research Council Brain Network Dynamics Unit, Nuffield Deptartment of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH, United KingdomMedical Research Council Brain Network Dynamics Unit, Nuffield Deptartment of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH, United Kingdom; Corresponding author.Defining spatial synchronisation of pathological beta oscillations is important, given that many theories linking them to parkinsonian symptoms propose a reduction in the dimensionality of the coding space within and/or across cortico-basal ganglia structures. Such spatial synchronisation could arise from a single process, with widespread entrainment of neurons to the same oscillation. Alternatively, the partially segregated structure of cortico-basal ganglia loops could provide a substrate for multiple ensembles that are independently synchronized at beta frequencies. Addressing this question requires an analytical approach that identifies groups of signals with a statistical tendency for beta synchronisation, which is unachievable using standard pairwise measures. Here, we utilized such an approach on multichannel recordings of background unit activity (BUA) in the external globus pallidus (GP) and subthalamic nucleus (STN) in parkinsonian rats. We employed an adapted version of a principle and independent component analysis-based method commonly used to define assemblies of single neurons (i.e., neurons that are synchronized over short timescales). This analysis enabled us to define whether changes in the power of beta oscillations in local ensembles of neurons (i.e., the BUA recorded from single contacts) consistently covaried over time, forming a “beta ensemble”. Multiple beta ensembles were often present in single recordings and could span brain structures. Membership of a beta ensemble predicted significantly higher levels of short latency (<5 ms) synchrony in the raw BUA signal and phase synchronisation with cortical beta oscillations, suggesting that they comprised clusters of neurons that are functionally connected at multiple levels, despite sometimes being non-contiguous in space. Overall, these findings suggest that beta oscillations do not comprise of a single synchronisation process, but rather multiple independent activities that can bind both spatially contiguous and non-contiguous pools of neurons within and across structures. As previously proposed, such ensembles provide a substrate for beta oscillations to constrain the coding space of cortico-basal ganglia circuits.http://www.sciencedirect.com/science/article/pii/S0969996124002523Parkinson's diseasebeta oscillationsPathophysiologyDeep brain stimulationSynchrony |
| spellingShingle | Isaac Grennan Nicolas Mallet Peter J. Magill Hayriye Cagnan Andrew Sharott Beta bursts in the parkinsonian cortico-basal ganglia network form spatially discrete ensembles Neurobiology of Disease Parkinson's disease beta oscillations Pathophysiology Deep brain stimulation Synchrony |
| title | Beta bursts in the parkinsonian cortico-basal ganglia network form spatially discrete ensembles |
| title_full | Beta bursts in the parkinsonian cortico-basal ganglia network form spatially discrete ensembles |
| title_fullStr | Beta bursts in the parkinsonian cortico-basal ganglia network form spatially discrete ensembles |
| title_full_unstemmed | Beta bursts in the parkinsonian cortico-basal ganglia network form spatially discrete ensembles |
| title_short | Beta bursts in the parkinsonian cortico-basal ganglia network form spatially discrete ensembles |
| title_sort | beta bursts in the parkinsonian cortico basal ganglia network form spatially discrete ensembles |
| topic | Parkinson's disease beta oscillations Pathophysiology Deep brain stimulation Synchrony |
| url | http://www.sciencedirect.com/science/article/pii/S0969996124002523 |
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