Cargando…

Topologically Disrupted Gray Matter Networks in Drug-Naïve Essential Tremor Patients With Poor Sleep Quality

BACKGROUND: Sleep disturbances are widespread among patients with essential tremor (ET) and may have adverse effects on patients' quality of life. However, the pathophysiology underlying poor quality of sleep (QoS) in patients with ET remains unclear. Our study aimed to identify gray matter (GM...

Descripción completa

Detalles Bibliográficos
Autores principales: Peng, Jiaxin, Yang, Jing, Li, Nannan, Lei, Du, Li, Junying, Duan, Liren, Chen, Chaolan, Zeng, Yan, Xi, Jing, Jiang, Yi, Gong, Qiyong, Peng, Rong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9086904/
https://www.ncbi.nlm.nih.gov/pubmed/35557617
http://dx.doi.org/10.3389/fneur.2022.834277
_version_ 1784704107649433600
author Peng, Jiaxin
Yang, Jing
Li, Nannan
Lei, Du
Li, Junying
Duan, Liren
Chen, Chaolan
Zeng, Yan
Xi, Jing
Jiang, Yi
Gong, Qiyong
Peng, Rong
author_facet Peng, Jiaxin
Yang, Jing
Li, Nannan
Lei, Du
Li, Junying
Duan, Liren
Chen, Chaolan
Zeng, Yan
Xi, Jing
Jiang, Yi
Gong, Qiyong
Peng, Rong
author_sort Peng, Jiaxin
collection PubMed
description BACKGROUND: Sleep disturbances are widespread among patients with essential tremor (ET) and may have adverse effects on patients' quality of life. However, the pathophysiology underlying poor quality of sleep (QoS) in patients with ET remains unclear. Our study aimed to identify gray matter (GM) network alterations in the topological properties of structural MRI related to QoS in patients with ET. METHOD: We enrolled 45 ET patients with poor QoS (SleET), 59 ET patients with normal QoS (NorET), and 66 healthy controls (HC), and they all underwent a three-dimensional T1-weighted MRI scan. We used a graph-theoretical approach to investigate the topological organization of GM morphological networks, and individual morphological brain networks were constructed according to the interregional similarity of GM volume distributions. Furthermore, we performed network-based statistics, and partial correlation analyses between topographic features and clinical characteristics were conducted. RESULTS: Global network organization was disrupted in patients with ET. Compared with the NorET group, the SleET group exhibited disrupted topological GM network organization with a shift toward randomization. Moreover, they showed altered nodal centralities in mainly the frontal, temporal, parietal, and cerebellar lobes. Morphological connection alterations within the default mode network (DMN), salience, and basal ganglia networks were observed in the SleET group and were generally more extensive than those in the NorET and HC groups. Alterations within the cerebello-thalamo-(cortical) network were only detected in the SleET group. The nodal degree of the left thalamus was negatively correlated with the Fahn-Tolosa-Marin Tremor Rating Scale score (r = −0.354, p =0.027). CONCLUSION: Our findings suggest that potential complex interactions underlie tremor and sleep disruptions in patients with ET. Disruptions within the DMN and the cerebello-thalamo-(cortical) network may have a broader impact on sleep quality in patients with ET. Our results offer valuable insight into the neural mechanisms underlying poor QoS in patients with ET.
format Online
Article
Text
id pubmed-9086904
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-90869042022-05-11 Topologically Disrupted Gray Matter Networks in Drug-Naïve Essential Tremor Patients With Poor Sleep Quality Peng, Jiaxin Yang, Jing Li, Nannan Lei, Du Li, Junying Duan, Liren Chen, Chaolan Zeng, Yan Xi, Jing Jiang, Yi Gong, Qiyong Peng, Rong Front Neurol Neurology BACKGROUND: Sleep disturbances are widespread among patients with essential tremor (ET) and may have adverse effects on patients' quality of life. However, the pathophysiology underlying poor quality of sleep (QoS) in patients with ET remains unclear. Our study aimed to identify gray matter (GM) network alterations in the topological properties of structural MRI related to QoS in patients with ET. METHOD: We enrolled 45 ET patients with poor QoS (SleET), 59 ET patients with normal QoS (NorET), and 66 healthy controls (HC), and they all underwent a three-dimensional T1-weighted MRI scan. We used a graph-theoretical approach to investigate the topological organization of GM morphological networks, and individual morphological brain networks were constructed according to the interregional similarity of GM volume distributions. Furthermore, we performed network-based statistics, and partial correlation analyses between topographic features and clinical characteristics were conducted. RESULTS: Global network organization was disrupted in patients with ET. Compared with the NorET group, the SleET group exhibited disrupted topological GM network organization with a shift toward randomization. Moreover, they showed altered nodal centralities in mainly the frontal, temporal, parietal, and cerebellar lobes. Morphological connection alterations within the default mode network (DMN), salience, and basal ganglia networks were observed in the SleET group and were generally more extensive than those in the NorET and HC groups. Alterations within the cerebello-thalamo-(cortical) network were only detected in the SleET group. The nodal degree of the left thalamus was negatively correlated with the Fahn-Tolosa-Marin Tremor Rating Scale score (r = −0.354, p =0.027). CONCLUSION: Our findings suggest that potential complex interactions underlie tremor and sleep disruptions in patients with ET. Disruptions within the DMN and the cerebello-thalamo-(cortical) network may have a broader impact on sleep quality in patients with ET. Our results offer valuable insight into the neural mechanisms underlying poor QoS in patients with ET. Frontiers Media S.A. 2022-04-26 /pmc/articles/PMC9086904/ /pubmed/35557617 http://dx.doi.org/10.3389/fneur.2022.834277 Text en Copyright © 2022 Peng, Yang, Li, Lei, Li, Duan, Chen, Zeng, Xi, Jiang, Gong and Peng. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Peng, Jiaxin
Yang, Jing
Li, Nannan
Lei, Du
Li, Junying
Duan, Liren
Chen, Chaolan
Zeng, Yan
Xi, Jing
Jiang, Yi
Gong, Qiyong
Peng, Rong
Topologically Disrupted Gray Matter Networks in Drug-Naïve Essential Tremor Patients With Poor Sleep Quality
title Topologically Disrupted Gray Matter Networks in Drug-Naïve Essential Tremor Patients With Poor Sleep Quality
title_full Topologically Disrupted Gray Matter Networks in Drug-Naïve Essential Tremor Patients With Poor Sleep Quality
title_fullStr Topologically Disrupted Gray Matter Networks in Drug-Naïve Essential Tremor Patients With Poor Sleep Quality
title_full_unstemmed Topologically Disrupted Gray Matter Networks in Drug-Naïve Essential Tremor Patients With Poor Sleep Quality
title_short Topologically Disrupted Gray Matter Networks in Drug-Naïve Essential Tremor Patients With Poor Sleep Quality
title_sort topologically disrupted gray matter networks in drug-naïve essential tremor patients with poor sleep quality
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9086904/
https://www.ncbi.nlm.nih.gov/pubmed/35557617
http://dx.doi.org/10.3389/fneur.2022.834277
work_keys_str_mv AT pengjiaxin topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT yangjing topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT linannan topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT leidu topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT lijunying topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT duanliren topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT chenchaolan topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT zengyan topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT xijing topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT jiangyi topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT gongqiyong topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality
AT pengrong topologicallydisruptedgraymatternetworksindrugnaiveessentialtremorpatientswithpoorsleepquality