Resting state activity and connectivity of the nucleus basalis of Meynert and globus pallidus in Lewy body dementia and Parkinson's disease dementia

Parkinson's disease dementia (PDD) and dementia with Lewy bodies (DLB) are two related diseases which can be difficult to distinguish. There is no objective biomarker which can reliably differentiate between them. The synergistic combination of electrophysiological and neuroimaging approaches i...

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Main Authors: James Gratwicke, Ashwini Oswal, Harith Akram, Marjan Jahanshahi, Marwan Hariz, Ludvic Zrinzo, Tom Foltynie, Vladimir Litvak
Format: Article
Language:English
Published: Elsevier 2020-11-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811920306704
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spelling doaj-81c6b3270069463abecf3f984452146d2020-12-13T04:18:01ZengElsevierNeuroImage1095-95722020-11-01221117184Resting state activity and connectivity of the nucleus basalis of Meynert and globus pallidus in Lewy body dementia and Parkinson's disease dementiaJames Gratwicke0Ashwini Oswal1Harith Akram2Marjan Jahanshahi3Marwan Hariz4Ludvic Zrinzo5Tom Foltynie6Vladimir Litvak7Department of Clinical and Movement Neurosciences, UCL Institute of Neurology and The National Hospital for Neurology and Neurosurgery, Queen Square, London, UKNuffield Department of Clinical Neurosciences, John Radcliffe Hospital, Oxford, UK; Wellcome Centre for Human Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London, UKDepartment of Clinical and Movement Neurosciences, UCL Institute of Neurology and The National Hospital for Neurology and Neurosurgery, Queen Square, London, UK; Wellcome Centre for Human Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London, UKDepartment of Clinical and Movement Neurosciences, UCL Institute of Neurology and The National Hospital for Neurology and Neurosurgery, Queen Square, London, UKDepartment of Clinical and Movement Neurosciences, UCL Institute of Neurology and The National Hospital for Neurology and Neurosurgery, Queen Square, London, UKDepartment of Clinical and Movement Neurosciences, UCL Institute of Neurology and The National Hospital for Neurology and Neurosurgery, Queen Square, London, UKDepartment of Clinical and Movement Neurosciences, UCL Institute of Neurology and The National Hospital for Neurology and Neurosurgery, Queen Square, London, UKWellcome Centre for Human Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London, UK; Corresponding author.Parkinson's disease dementia (PDD) and dementia with Lewy bodies (DLB) are two related diseases which can be difficult to distinguish. There is no objective biomarker which can reliably differentiate between them. The synergistic combination of electrophysiological and neuroimaging approaches is a powerful method for interrogation of functional brain networks in vivo. We recorded bilateral local field potentials (LFPs) from the nucleus basalis of Meynert (NBM) and the internal globus pallidus (GPi) with simultaneous cortical magnetoencephalography (MEG) in six PDD and five DLB patients undergoing surgery for deep brain stimulation (DBS) to look for differences in underlying resting-state network pathophysiology. In both patient groups we observed spectral peaks in the theta (2–8 Hz) band in both the NBM and the GPi. Furthermore, both the NBM and the GPi exhibited similar spatial and spectral patterns of coupling with the cortex in the two disease states. Specifically, we report two distinct coherent networks between the NBM/GPi and cortical regions: (1) a theta band (2–8 Hz) network linking the NBM/GPi to temporal cortical regions, and (2) a beta band (13–22 Hz) network coupling the NBM/GPi to sensorimotor areas. We also found differences between the two disease groups: oscillatory power in the low beta (13–22Hz) band was significantly higher in the globus pallidus in PDD patients compared to DLB, and coherence in the high beta (22–35Hz) band between the globus pallidus and lateral sensorimotor cortex was significantly higher in DLB patients compared to PDD. Overall, our findings reveal coherent networks of the NBM/GPi region that are common to both DLB and PDD. Although the neurophysiological differences between the two conditions in this study are confounded by systematic differences in DBS lead trajectories and motor symptom severity, they lend support to the hypothesis that DLB and PDD, though closely related, are distinguishable from a neurophysiological perspective.http://www.sciencedirect.com/science/article/pii/S1053811920306704HumanBasal gangliaNetworkPallidumBasal forebrain
collection DOAJ
language English
format Article
sources DOAJ
author James Gratwicke
Ashwini Oswal
Harith Akram
Marjan Jahanshahi
Marwan Hariz
Ludvic Zrinzo
Tom Foltynie
Vladimir Litvak
spellingShingle James Gratwicke
Ashwini Oswal
Harith Akram
Marjan Jahanshahi
Marwan Hariz
Ludvic Zrinzo
Tom Foltynie
Vladimir Litvak
Resting state activity and connectivity of the nucleus basalis of Meynert and globus pallidus in Lewy body dementia and Parkinson's disease dementia
NeuroImage
Human
Basal ganglia
Network
Pallidum
Basal forebrain
author_facet James Gratwicke
Ashwini Oswal
Harith Akram
Marjan Jahanshahi
Marwan Hariz
Ludvic Zrinzo
Tom Foltynie
Vladimir Litvak
author_sort James Gratwicke
title Resting state activity and connectivity of the nucleus basalis of Meynert and globus pallidus in Lewy body dementia and Parkinson's disease dementia
title_short Resting state activity and connectivity of the nucleus basalis of Meynert and globus pallidus in Lewy body dementia and Parkinson's disease dementia
title_full Resting state activity and connectivity of the nucleus basalis of Meynert and globus pallidus in Lewy body dementia and Parkinson's disease dementia
title_fullStr Resting state activity and connectivity of the nucleus basalis of Meynert and globus pallidus in Lewy body dementia and Parkinson's disease dementia
title_full_unstemmed Resting state activity and connectivity of the nucleus basalis of Meynert and globus pallidus in Lewy body dementia and Parkinson's disease dementia
title_sort resting state activity and connectivity of the nucleus basalis of meynert and globus pallidus in lewy body dementia and parkinson's disease dementia
publisher Elsevier
series NeuroImage
issn 1095-9572
publishDate 2020-11-01
description Parkinson's disease dementia (PDD) and dementia with Lewy bodies (DLB) are two related diseases which can be difficult to distinguish. There is no objective biomarker which can reliably differentiate between them. The synergistic combination of electrophysiological and neuroimaging approaches is a powerful method for interrogation of functional brain networks in vivo. We recorded bilateral local field potentials (LFPs) from the nucleus basalis of Meynert (NBM) and the internal globus pallidus (GPi) with simultaneous cortical magnetoencephalography (MEG) in six PDD and five DLB patients undergoing surgery for deep brain stimulation (DBS) to look for differences in underlying resting-state network pathophysiology. In both patient groups we observed spectral peaks in the theta (2–8 Hz) band in both the NBM and the GPi. Furthermore, both the NBM and the GPi exhibited similar spatial and spectral patterns of coupling with the cortex in the two disease states. Specifically, we report two distinct coherent networks between the NBM/GPi and cortical regions: (1) a theta band (2–8 Hz) network linking the NBM/GPi to temporal cortical regions, and (2) a beta band (13–22 Hz) network coupling the NBM/GPi to sensorimotor areas. We also found differences between the two disease groups: oscillatory power in the low beta (13–22Hz) band was significantly higher in the globus pallidus in PDD patients compared to DLB, and coherence in the high beta (22–35Hz) band between the globus pallidus and lateral sensorimotor cortex was significantly higher in DLB patients compared to PDD. Overall, our findings reveal coherent networks of the NBM/GPi region that are common to both DLB and PDD. Although the neurophysiological differences between the two conditions in this study are confounded by systematic differences in DBS lead trajectories and motor symptom severity, they lend support to the hypothesis that DLB and PDD, though closely related, are distinguishable from a neurophysiological perspective.
topic Human
Basal ganglia
Network
Pallidum
Basal forebrain
url http://www.sciencedirect.com/science/article/pii/S1053811920306704
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