Degree centrality and functional connections in presbycusis with and without cognitive impairments

Presbycusis is a major public issue that affecting elderly adults. However, the neural substrates between normal cognition and cognitive deficits in these patients need to be illustrated. 47 patients with presbycusis and 33 well-matched healthy controls were recruited in present study. Each subject...

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Published inBrain imaging and behavior Vol. 16; no. 6; pp. 2725 - 2734
Main Authors Xu, Xiao-Min, Liu, Yin, Feng, Yuan, Xu, Jin-Jing, Gao, Jun, Salvi, Richard, Wu, Yuanqing, Yin, Xindao, Chen, Yu-Chen
Format Journal Article
LanguageEnglish
Published New York Springer US 01.12.2022
Springer Nature B.V
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Abstract Presbycusis is a major public issue that affecting elderly adults. However, the neural substrates between normal cognition and cognitive deficits in these patients need to be illustrated. 47 patients with presbycusis and 33 well-matched healthy controls were recruited in present study. Each subject underwent pure-tone audiometry (PTA), MRI scanning and cognition evaluations, then we found 22 patients with cognitive deficits and 25 patients with common cognition. We analyzed the Degree centrality (DC) characteristics among three groups, and try to recognize key nodes which contribute significantly. Subsequent functional connectivity analysis was applied using the key nodes as seeds. Compared with controls, presbycusis without cognitive impairments showed deceased DC in superior temporal gyrus (STG), inferior frontal gyrus (IFG) and supramarginal gyrus (SMG). Additionally, presbycusis with cognitive impairments showed enhanced DC in fusiform gurus (FFG), cerebellum and para-hippocampal gyrus (PHG), while weakened DC in SMG, middle frontal gyrus (IFG) and inferior Parietal lobule (IPL). Compared with normal cognition, increased DC value of cerebellum and STG, as well as decreased DC value of IPL in presbycusis with cognitive impairments were observed. We noticed that SMG may play an important role. Then the left and right SMG were used as seeds in functional connections analysis. With the seed set at left SMG, presbycusis without cognitive impairments showed decreases connections with cerebellum, temporal pole (TP), superior temporal gyrus (STG) and median cingulate cortex (MCC). Presbycusis with cognitive impairments showed weakened connectivity with cerebellum, IFG, IPL and superior frontal gyrus (SFG). The right SMG showed decrease connections with cerebellum, middle temporal gyrus (MTG), STG and increase connection with middle frontal gyrus (MFG) in presbycusis without cognitive impairments. While the right SMG showed enhanced connections with left TP, caudate, anterior cingulate cortex (ACC), angular, SFG and weakened connectivity with right SFG presbycusis with cognitive impairments. In comparison with normal cognition and impaired cognition, MFG, IFG, PHG, rolandic operculum and cerebellum were involved. These findings enriched our understanding of the neural mechanisms underlying cognitive impairments associated with presbycusis and may serve as a potential imaging biomarker for investigating and predicting cognitive difficulties.
AbstractList Abstract Presbycusis is a major public issue that affecting elderly adults. However, the neural substrates between normal cognition and cognitive deficits in these patients need to be illustrated. 47 patients with presbycusis and 33 well-matched healthy controls were recruited in present study. Each subject underwent pure-tone audiometry (PTA), MRI scanning and cognition evaluations, then we found 22 patients with cognitive deficits and 25 patients with common cognition. We analyzed the Degree centrality (DC) characteristics among three groups, and try to recognize key nodes which contribute significantly. Subsequent functional connectivity analysis was applied using the key nodes as seeds. Compared with controls, presbycusis without cognitive impairments showed deceased DC in superior temporal gyrus (STG), inferior frontal gyrus (IFG) and supramarginal gyrus (SMG). Additionally, presbycusis with cognitive impairments showed enhanced DC in fusiform gurus (FFG), cerebellum and para-hippocampal gyrus (PHG), while weakened DC in SMG, middle frontal gyrus (IFG) and inferior Parietal lobule (IPL). Compared with normal cognition, increased DC value of cerebellum and STG, as well as decreased DC value of IPL in presbycusis with cognitive impairments were observed. We noticed that SMG may play an important role. Then the left and right SMG were used as seeds in functional connections analysis. With the seed set at left SMG, presbycusis without cognitive impairments showed decreases connections with cerebellum, temporal pole (TP), superior temporal gyrus (STG) and median cingulate cortex (MCC). Presbycusis with cognitive impairments showed weakened connectivity with cerebellum, IFG, IPL and superior frontal gyrus (SFG). The right SMG showed decrease connections with cerebellum, middle temporal gyrus (MTG), STG and increase connection with middle frontal gyrus (MFG) in presbycusis without cognitive impairments. While the right SMG showed enhanced connections with left TP, caudate, anterior cingulate cortex (ACC), angular, SFG and weakened connectivity with right SFG presbycusis with cognitive impairments. In comparison with normal cognition and impaired cognition, MFG, IFG, PHG, rolandic operculum and cerebellum were involved. These findings enriched our understanding of the neural mechanisms underlying cognitive impairments associated with presbycusis and may serve as a potential imaging biomarker for investigating and predicting cognitive difficulties.
Presbycusis is a major public issue that affecting elderly adults. However, the neural substrates between normal cognition and cognitive deficits in these patients need to be illustrated. 47 patients with presbycusis and 33 well-matched healthy controls were recruited in present study. Each subject underwent pure-tone audiometry (PTA), MRI scanning and cognition evaluations, then we found 22 patients with cognitive deficits and 25 patients with common cognition. We analyzed the Degree centrality (DC) characteristics among three groups, and try to recognize key nodes which contribute significantly. Subsequent functional connectivity analysis was applied using the key nodes as seeds. Compared with controls, presbycusis without cognitive impairments showed deceased DC in superior temporal gyrus (STG), inferior frontal gyrus (IFG) and supramarginal gyrus (SMG). Additionally, presbycusis with cognitive impairments showed enhanced DC in fusiform gurus (FFG), cerebellum and para-hippocampal gyrus (PHG), while weakened DC in SMG, middle frontal gyrus (IFG) and inferior Parietal lobule (IPL). Compared with normal cognition, increased DC value of cerebellum and STG, as well as decreased DC value of IPL in presbycusis with cognitive impairments were observed. We noticed that SMG may play an important role. Then the left and right SMG were used as seeds in functional connections analysis. With the seed set at left SMG, presbycusis without cognitive impairments showed decreases connections with cerebellum, temporal pole (TP), superior temporal gyrus (STG) and median cingulate cortex (MCC). Presbycusis with cognitive impairments showed weakened connectivity with cerebellum, IFG, IPL and superior frontal gyrus (SFG). The right SMG showed decrease connections with cerebellum, middle temporal gyrus (MTG), STG and increase connection with middle frontal gyrus (MFG) in presbycusis without cognitive impairments. While the right SMG showed enhanced connections with left TP, caudate, anterior cingulate cortex (ACC), angular, SFG and weakened connectivity with right SFG presbycusis with cognitive impairments. In comparison with normal cognition and impaired cognition, MFG, IFG, PHG, rolandic operculum and cerebellum were involved. These findings enriched our understanding of the neural mechanisms underlying cognitive impairments associated with presbycusis and may serve as a potential imaging biomarker for investigating and predicting cognitive difficulties.Presbycusis is a major public issue that affecting elderly adults. However, the neural substrates between normal cognition and cognitive deficits in these patients need to be illustrated. 47 patients with presbycusis and 33 well-matched healthy controls were recruited in present study. Each subject underwent pure-tone audiometry (PTA), MRI scanning and cognition evaluations, then we found 22 patients with cognitive deficits and 25 patients with common cognition. We analyzed the Degree centrality (DC) characteristics among three groups, and try to recognize key nodes which contribute significantly. Subsequent functional connectivity analysis was applied using the key nodes as seeds. Compared with controls, presbycusis without cognitive impairments showed deceased DC in superior temporal gyrus (STG), inferior frontal gyrus (IFG) and supramarginal gyrus (SMG). Additionally, presbycusis with cognitive impairments showed enhanced DC in fusiform gurus (FFG), cerebellum and para-hippocampal gyrus (PHG), while weakened DC in SMG, middle frontal gyrus (IFG) and inferior Parietal lobule (IPL). Compared with normal cognition, increased DC value of cerebellum and STG, as well as decreased DC value of IPL in presbycusis with cognitive impairments were observed. We noticed that SMG may play an important role. Then the left and right SMG were used as seeds in functional connections analysis. With the seed set at left SMG, presbycusis without cognitive impairments showed decreases connections with cerebellum, temporal pole (TP), superior temporal gyrus (STG) and median cingulate cortex (MCC). Presbycusis with cognitive impairments showed weakened connectivity with cerebellum, IFG, IPL and superior frontal gyrus (SFG). The right SMG showed decrease connections with cerebellum, middle temporal gyrus (MTG), STG and increase connection with middle frontal gyrus (MFG) in presbycusis without cognitive impairments. While the right SMG showed enhanced connections with left TP, caudate, anterior cingulate cortex (ACC), angular, SFG and weakened connectivity with right SFG presbycusis with cognitive impairments. In comparison with normal cognition and impaired cognition, MFG, IFG, PHG, rolandic operculum and cerebellum were involved. These findings enriched our understanding of the neural mechanisms underlying cognitive impairments associated with presbycusis and may serve as a potential imaging biomarker for investigating and predicting cognitive difficulties.
Presbycusis is a major public issue that affecting elderly adults. However, the neural substrates between normal cognition and cognitive deficits in these patients need to be illustrated. 47 patients with presbycusis and 33 well-matched healthy controls were recruited in present study. Each subject underwent pure-tone audiometry (PTA), MRI scanning and cognition evaluations, then we found 22 patients with cognitive deficits and 25 patients with common cognition. We analyzed the Degree centrality (DC) characteristics among three groups, and try to recognize key nodes which contribute significantly. Subsequent functional connectivity analysis was applied using the key nodes as seeds. Compared with controls, presbycusis without cognitive impairments showed deceased DC in superior temporal gyrus (STG), inferior frontal gyrus (IFG) and supramarginal gyrus (SMG). Additionally, presbycusis with cognitive impairments showed enhanced DC in fusiform gurus (FFG), cerebellum and para-hippocampal gyrus (PHG), while weakened DC in SMG, middle frontal gyrus (IFG) and inferior Parietal lobule (IPL). Compared with normal cognition, increased DC value of cerebellum and STG, as well as decreased DC value of IPL in presbycusis with cognitive impairments were observed. We noticed that SMG may play an important role. Then the left and right SMG were used as seeds in functional connections analysis. With the seed set at left SMG, presbycusis without cognitive impairments showed decreases connections with cerebellum, temporal pole (TP), superior temporal gyrus (STG) and median cingulate cortex (MCC). Presbycusis with cognitive impairments showed weakened connectivity with cerebellum, IFG, IPL and superior frontal gyrus (SFG). The right SMG showed decrease connections with cerebellum, middle temporal gyrus (MTG), STG and increase connection with middle frontal gyrus (MFG) in presbycusis without cognitive impairments. While the right SMG showed enhanced connections with left TP, caudate, anterior cingulate cortex (ACC), angular, SFG and weakened connectivity with right SFG presbycusis with cognitive impairments. In comparison with normal cognition and impaired cognition, MFG, IFG, PHG, rolandic operculum and cerebellum were involved. These findings enriched our understanding of the neural mechanisms underlying cognitive impairments associated with presbycusis and may serve as a potential imaging biomarker for investigating and predicting cognitive difficulties.
Author Wu, Yuanqing
Salvi, Richard
Xu, Xiao-Min
Liu, Yin
Xu, Jin-Jing
Yin, Xindao
Chen, Yu-Chen
Feng, Yuan
Gao, Jun
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Supramarginal gyrus
Degree centrality
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Presbycusis
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PublicationDate 20221200
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20221201
PublicationDateYYYYMMDD 2022-12-01
PublicationDate_xml – month: 12
  year: 2022
  text: 20221200
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PublicationTitle Brain imaging and behavior
PublicationTitleAbbrev Brain Imaging and Behavior
PublicationYear 2022
Publisher Springer US
Springer Nature B.V
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– name: Springer Nature B.V
References PauquetJThielCMMathysCRosemannSRelationship between Memory Load and Listening Demands in Age-Related Hearing ImpairmentNeural Plasticity20212021884045210.1155/2021/8840452341886768195652
JaegerJDigit symbol substitution test: The case for sensitivity over specificity in neuropsychological testingJournal of Clinical Psychopharmacology201838551351910.1097/JCP.0000000000000941301245836291255
WeiYZhangWLiYLiuXZhaBHuSWangYWangXYuXYangJQiuBAcupuncture treatment decreased temporal variability of dynamic functional connectivity in chronic tinnitusFrontiers in Neuroscience20211573799310.3389/fnins.2021.73799335153654
HuaKWangTLiCLiSMaXLiCLiMFuSYinYWuYLiuMYuKFangJWangPJiangGAbnormal degree centrality in chronic users of codeine-containing cough syrups: A resting-state functional magnetic resonance imaging studyNeuroimage Clin20181977578110.1016/j.nicl.2018.06.003299887656031869
RenFMaWLiMSunHXinQZongWChenWWangGGaoFZhaoBGray matter atrophy is associated with cognitive impairment in patients with Presbycusis: A comprehensive morphometric studyFrontiers in Neuroscience20181274410.3389/fnins.2018.00744304053336205975
SchaalNKWilliamsonVJKellyMMuggletonNGPollokBKrauseVBanissyMJA causal involvement of the left supramarginal gyrus during the retention of musical pitchesCortex20156431031710.1016/j.cortex.2014.11.01125577719
XingCChenYCTongZXuWXuJJYinXWuYCaiYAberrant brain functional hubs and causal connectivity in presbycusisBrain Imaging and Behavior202115145346310.1007/s11682-020-00386-432979169
JafariZKolbBEMohajeraniMHAge-related hearing loss and tinnitus, dementia risk, and auditory amplification outcomesAgeing Research Reviews20195610096310.1016/j.arr.2019.10096331557539
LinFRMetterEJO'BrienRJResnickSMZondermanABFerrucciLHearing loss and incident dementiaArchives of Neurology201168221422010.1001/archneurol.2010.362213209883277836
TomasiDShokri-KojoriEVolkowNDHigh-resolution functional connectivity density: Hub locations, sensitivity, specificity, reproducibility, and reliabilityCerebral Cortex20162673249325910.1093/cercor/bhv17126223259
Larson, P. S., & Cheung, S. W. (2012). Deep brain stimulation in area LC controllably triggers auditory phantom percepts. Neurosurgery, 70(2), 398–405; discussion 405–396. https://doi.org/10.1227/NEU.0b013e3182320ab5
ChenJHuBQinPGaoWLiuCZiDDingXYuYCuiGLuLAltered brain activity and functional connectivity in unilateral sudden sensorineural hearing lossNeural Plasticity2020202094603641:CAS:528:DC%2BB3MXktVWmsLc%3D10.1155/2020/9460364330291307527900
EickhoffSBLotzeMWietekBAmuntsKEnckPZillesKSegregation of visceral and somatosensory afferents: An fMRI and cytoarchitectonic mapping studyNeuroImage20063131004101410.1016/j.neuroimage.2006.01.02316529950
LiFLuLShangSHuLChenHWangPZhangHDisrupted Functional Network Connectivity Predicts Cognitive Impairment after Acute Mild Traumatic Brain Injury.202026101083109110.1111/cns.13430
MarkesberyWRSchmittFAKryscioRJDavisDGSmithCDWeksteinDRNeuropathologic substrate of mild cognitive impairmentArchives of Neurology2006631384610.1001/archneur.63.1.3816401735
QianZJChangPDMoonisGLalwaniAKA novel method of quantifying brain atrophy associated with age-related hearing lossNeuroimage Clin20171620520910.1016/j.nicl.2017.07.021288086175544491
ZhouGPChenYCLiWWWeiHLYuYSZhouQQYinXTaoYJZhangHAberrant functional and effective connectivity of the frontostriatal network in unilateral acute tinnitus patients with hearing lossBrain Imaging and Behavior202216115116010.1007/s11682-021-00486-934296381
KanYWangWZhangSXMaHWangZCYangJGNeural metabolic activity in idiopathic tinnitus patients after repetitive transcranial magnetic stimulationWorld J Clin Cases20197131582159010.12998/wjcc.v7.i13.1582313676176658381
RubinsteinDYCamarillo-RodriguezLSerruyaMDHerwegNAWaldmanZJWandaPASharanADWeissSASperlingMRContribution of left supramarginal and angular gyri to episodic memory encoding: An intracranial EEG studyNeuroImage202122511751410.1016/j.neuroimage.2020.11751433137477
HuangRWangABaXZhangGLiCLiuQAssociation functional MRI studies of resting-state amplitude of low frequency fluctuation and voxel-based morphometry in patients with occupational noise-induced hearing LossJournal of Occupational and Environmental Medicine202062747247710.1097/JOM.000000000000186932730022
Garcia-EsparciaPKonetiARodriguez-OrozMCGagoBDel RioJAFerrerIMitochondrial activity in the frontal cortex area 8 and angular gyrus in Parkinson's disease and Parkinson's disease with dementiaBrain Pathology201828143571:CAS:528:DC%2BC2sXitVCrsb%2FK10.1111/bpa.1247427984680
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XuXMJiaoYTangTYZhangJLuCQSalviRTengGJSensorineural hearing loss and cognitive impairments: Contributions of thalamus using multiparametric MRIJournal of Magnetic Resonance Imaging201950378779710.1002/jmri.2666530694013
PowerJDPetersenSEControl-related systems in the human brainCurrent Opinion in Neurobiology20132322232281:CAS:528:DC%2BC3sXht1Oks7g%3D10.1016/j.conb.2012.12.009233476453632325
JobAPonsYLamalleLJaillardABuckKSegebarthCDelon-MartinCAbnormal cortical sensorimotor activity during "Target" sound detection in subjects with acute acoustic trauma sequelae: An fMRI studyBrain and Behavior: A Cognitive Neuroscience Perspective20122218719910.1002/brb3.21
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BucknerRLSepulcreJTalukdarTKrienenFMLiuHHeddenTAndrews-HannaJRSperlingRAJohnsonKACortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to Alzheimer's diseaseJournal of Neuroscience2009296186018731:CAS:528:DC%2BD1MXit1Wiur0%3D10.1523/JNEUROSCI.5062-08.200919211893
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ShahMKurthFLudersEThe impact of aging on the subregions of the fusiform gyrus in healthy older adultsJournal of Neuroscience Research20219912632701:CAS:528:DC%2BB3cXksVWrurk%3D10.1002/jnr.2458632147882
XiongJYuCSuTGeQMShiWQTangLYShuHYPanYCLiangRBLiQYShaoYAltered brain network centrality in patients with mild cognitive impairment: an fMRI study using a voxel-wise degree centrality approachAging (Albany NY)2021131115491155001:CAS:528:DC%2BB3MXit1Cgur7F10.18632/aging.20310534106878
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BidelmanGMPriceCNShenDArnottSRAlainCAfferent-efferent connectivity between auditory brainstem and cortex accounts for poorer speech-in-noise comprehension in older adultsHearing Research201938210779510.1016/j.heares.2019.107795314799536778515
Albers, M. W., Gilmore, G. C., Kaye, J., Murphy, C., Wingfield, A., Bennett, D. A., Boxer, A. L., Buchman, A. S., Cruickshanks, K. J., Devanand, D. P., Duffy, C. J., Gall, C. M., Gates, G. A., Granholm, A. C., Hensch, T., Holtzer, R., Hyman, B. T., Lin, F. R., McKee, A. C., …, & Zhang, L. I. (2015). At the interface of sensory and motor dysfunctions and Alzheimer’s disease. Alzheimer’s & Dementia,11(1), 70–98. https://doi.org/10.1016/j.jalz.2014.04.514
RenFMaWZongWLiNLiXLiFWuLLiHLiMGaoFBrain frequency-specific changes in the spontaneous neural activity are associated with cognitive impairment in patients with PresbycusisFront Aging Neurosci20211364987410.3389/fnagi.2021.649874343352248316979
ChenYCYongWXingCFengYHaidariNAXuJJGuJPYinXWuYDirected functional connectivity of the hippocampus in patients with presbycusisBrain Imaging and Behavior202014391792610.1007/s11682-019-00162-z31270776
RosemannSThielCMAudio-visual speech processing in age-related hearing loss: Stronger integration and increased frontal lobe recruitmentNeuroImage201817542543710.1016/j.neuroimage.2018.04.02329655940
WangYZhongSJiaYSunYWangBLiuTPanJHuangLDisrupted resting-state functional connectivity in nonmedicated bipolar disorderRadiology2016280252953610.1148/radiol.201615164126909649
WeiMShiJLiTNiJZhangXLiYKangSMaFXieHQinBFanDZhangLWangYTianJDiagnostic accuracy of the chinese version of the trail-making test for screening cognitive impairmentJournal of the American Geriatrics Society2018661929910.1111/jgs.1513529135021
GuoZLiuXHouHWeiFLiuJChenXAbnormal degree centrality in Alzheimer's disease patients with depression: A resting-state functional magnetic resonance imaging studyExperimental Gerontology201679616610.1016/j.exger.2016.03.01727079332
LuanYWangCJiaoYTangTZhangJLuCSalviRTengGJAbnormal functional connectivity and degree centrality in anterior cingulate cortex in patients with long-term sensorineural hearing lossBrain Imaging and Behavior202014368269510.1007/s11682-018-0004-030511112
GolubJSSharmaRKRipponBQBrickmanAMLuchsingerJAThe association between early age-related hearing loss and brain beta-AmyloidThe Laryngoscope202113136336381:CAS:528:DC%2BB3MXjvF2itbk%3D10.1002/la
RL Buckner (734_CR4) 2009; 29
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GM Bidelman (734_CR2) 2019; 382
Z Guo (734_CR12) 2016; 79
Z Jafari (734_CR17) 2019; 56
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C Xing (734_CR43) 2021; 15
Y Wei (734_CR42) 2021; 15
F Li (734_CR23) 2020; 26
JD Power (734_CR30) 2013; 23
J Jastorff (734_CR18) 2016; 37
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MC Fitzhugh (734_CR9) 2019; 10
T Li (734_CR24) 2022
Y Kan (734_CR20) 2019; 7
DY Rubinstein (734_CR35) 2021; 225
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Y Wang (734_CR40) 2016; 280
M Shah (734_CR37) 2021; 99
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YC Chen (734_CR6) 2020; 14
J Henderson-Sabes (734_CR13) 2019; 9
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J Xiong (734_CR44) 2021; 13
H Yamasaki (734_CR47) 2002; 99
Y Du (734_CR7) 2016; 7
SB Eickhoff (734_CR8) 2006; 31
Z Zhou (734_CR48) 2021; 307
JS Golub (734_CR11) 2021; 131
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J Chen (734_CR5) 2020; 2020
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NK Schaal (734_CR36) 2015; 64
M Wei (734_CR41) 2018; 66
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J Pauquet (734_CR29) 2021; 2021
S Rosemann (734_CR34) 2018; 175
FR Lin (734_CR25) 2011; 68
S Wada (734_CR39) 2021; 16
XM Xu (734_CR45) 2019; 2019
J Jaeger (734_CR16) 2018; 38
K Hua (734_CR14) 2018; 19
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Snippet Presbycusis is a major public issue that affecting elderly adults. However, the neural substrates between normal cognition and cognitive deficits in these...
Abstract Presbycusis is a major public issue that affecting elderly adults. However, the neural substrates between normal cognition and cognitive deficits in...
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StartPage 2725
SubjectTerms Biomarkers
Biomedical and Life Sciences
Biomedicine
Cerebellum
Cognition
Cognition & reasoning
Cognitive ability
Connectivity analysis
Cortex (cingulate)
Frontal gyrus
Hippocampus
Neuroimaging
Neuropsychology
Neuroradiology
Neurosciences
Nodes
Operculum
Original Research
Psychiatry
Seed set
Seeds
Substrates
Superior temporal gyrus
Temporal cortex
Temporal gyrus
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Title Degree centrality and functional connections in presbycusis with and without cognitive impairments
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