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Cognitive impairment affects 40-70% of patients with multiple sclerosis (MS)1. These impairments are seen in multiple domains of cognition including attention, memory, and speed of information processing2. In a previous study using resting-state fMRI, we found abnormal connectivity links for most patients with MS in the default mode network as well as other cognitive networks including attention, memory, language, and visual-spatial memory.

BACKGROUND

OBJECTIVES

CONCLUSIONS

Analysis of White Matter Tracts of Resting State Cognitive Networks in Multiple Sclerosis

METHODS

RESULTS

DepartmentofNeurology,HenryFordHospital,Detroit,MI;2WayneStateUniversity,SchoolofMedicine,Detroit,MI

RahilDharia,BS1,2;EsmaeilDavoodi-Bojd,PhD1;QuanJing,PhD1;LianLi,PhD1;MirelaCerghet,MD,PhD1

To analyze the white matter damage and topological organization of white matter tracts in specific brain regions responsible for cognition in MS patients compared with healthy controls.

Funding Provided by Henry Ford Hospital and Foundation of the Consortium of Multiple Sclerosis Centers

REFERENCES

VERBAL MEMORY

ATTENTION

DEFAULT MODE NETWORK

MRI measurements of DTI, T1, T2, and T2 FLAIR were acquired by GE clinical 3T system of 32 healthy subjects and 20 MS patients. DTI images were preprocessed in MATLAB to calculate the fractional anisotropy (FA) maps3,4,5,6. We investigated five circuits in the brain responsible for cognitive functions: •  Default Mode Network (DMN): (1) Medial Prefrontal Cortex (MPFC), (2) Rostral Anterior Cingulate Cortex (RACC), (3) Posterior Cingulate Cortex (PCC), (4) Precuneus (PC), and (5) Lateral Parietal Cortex (LPC)

• Attention: (1) Thalamus (Superior Colliculus and Pulvinar) (THAL), (2) Superior Parietal Lobule (SPL), (3) Middle Frontal Gyrus (MFG), (4) Superior Frontal Gyrus (SFG), (5) Angular Gyrus (AG), and (6) Supramarginal Gyrus (SMG) • Verbal memory: (1) Inferior Temporal Gyrus (ITG), (2) Medial Occipitotemporal Gyrus (MOG), (3) Middle Temporal Gyrus (MTG), (4) Temporal Pole (TP), (5) Angular Gyrus (AG), and (6) Inferior Frontal Gyrus (IFG)

• Memory: (1) Angular Gyrus (AG), (2) Fusiform Gyrus (FG), (3) Superior Parietal Lobule (SPL), (4) Supramarginal Gyrus (SMG), (5) Hippocampal Formation (HF), and (6) Superior Frontal Gyrus (SFG)

• Visual-Spatial Working Memory: (1) Cingulate Region (CR), (2) Superior Frontal Gyrus (SFG), (3) Fornix, (4) Superior Parietal Lobule (SPL), and (5) Supramarginal Gyrus (SMG)

VISUO-SPATIAL WORKING MEMORY

MEMORY

Sociodemographic, clinical, and radiological characteristics of subjects used for DTI and fMRI connectivity analysis

RRMS

CONTROLS Gender Female 15 16 Male 5 22 Race White 14 Black 6 Others 0 Age (median/range) 39.6 (26-54) 34.92 (17-64) Median disease duration (range) 7 (5-20) EDSS (mean/range) 3 (1-8) Cognitive complains 6

Sociodemographic and clinical characteristics of subjects

Side

AnteriorLimbofInternalCapsule

FrontalLobeWM

GlobusPalladus

Hippocampal

FormaKon

LateralOccipito-temporalGyrus

OccipitalLobeWM

ParietalLobeWM

TemporalLobeWM

UncusCorpusCallosum

Right 60% 60% 55% 65% 50% 50% 65% 60% 85% 70%

LeO 60% 60% 60% 55% 0 30% 60% 60% 55%

The percentile of the MS patients (N=20) having significant FA reduction (p<0.05) of ≥50%

VARIABLEMSsubjects

N=7HealthyControls

N=18 p-value

Meanageatscanyears(range) 35.7(28-54) 36.4(17-62)

Mean(range)diseaseduraKon,years 4.8(2-10)

Median(range)EDSSscore 2.25(1-7.5)

Useofdisease-modifyingtherapies(Y/N) 7/0

ComplainsofcogniKvedeficit 4

Mean(SD)structuralMRImetrics

BrainVolume(cm3) 1051.00(154.17 1196.84(99.84 0.005ThalamicVolume(cm3) 13.52(1.01) 16.32(1.59) 0.0006

Whitema]erVolume(cm3) 427.90(94.26) 500.76(40.92) 0.008Greyma]erVolume 623.10(67.96) 696.09(66.21) 0.01

1.MSpa/enthavesignificantwhitema`erdamageandreduc/oninvariousregionsinthebraininvolvedincogni/venetworks.Brainvolume,normalizedthalamicvolume,whitema`ervolume,andgreyma`ervolumeweresignificantlylowerinMSsubjectssimilarwithpreviousreports7,8.2.ForMSpa/entswithmul/plescansover/me,furtherprogressionofwhitema`erdamagewasfound.3.Wereportthatbothanatomicalandfunc/onalconnec/vityinsidedefaultmodenetworkandcogni/venetworksshowedsignificantdifferencescomparedwithhealthysubjects.Similarwithpreviousreportswefounddysfunc/oninfMRIconnec/vityinDMN9,10.4.Analysesofbothfunc/onalandstructuralconnec/vityofthefivecogni/venetworks(DMN,a`en/on,verbalmemory,memory,visuo-spa/almemory)showedasignificantdecreaseinstructuralconnec/vitybilaterallyinMSsubjectsalongwithadecreaseinfunc/onalconnec/vityofthesuperiormarginalgyrus,angulargyrus,fusiformgyrus,temporalpole,hippocampalforma/on,andthalamus.Thedecreaseinfunc/onalconnec/vitymostlikelyrelatestowhitema`erdamageinMS.Someregionsinthestudiednetworkshadheightenedconnec/vitywhichmayrepresentcompensatoryconnec/onsaspostulatedintheliterature11.

1.AmatoMP,PonzianiG,SiracusaG,SorbiS.Cogni/vedysfunc/oninearly-onsetmul/plesclerosis:areappraisalafer10yearsArchivesofNeurology2001;58910):1602-6.2.HuijbregtsSC,KalkresNF,deSommervilleLM,deCrestV,PolmanGH.Cogni/veimpairmentanddeclineindifferentMSsubtypes.JNeurolSci2006;245(1-2):187-943.O.Sporns,"Thehumanconnectome:acomplexnetwork,"AnnNYAcadSci,vol.1224,pp.109-25,Apr2011.4.B.Fischl,D.H.Salat,E.Busa,M.Albert,M.Dieterich,C.Haselgrove,etal.,"Wholebrainsegmenta/on:automatedlabelingofneuroanatomicalstructuresinthehumanbrain,"Neuron,vol.33,pp.341-55,Jan312002.5.J.D.Tournier,F.Calamante,andA.Connelly,"MRtrix:Diffusiontractographyincrossingfiberregions,"Interna/onalJournalofImagingSystemsandTechnology,vol.22,pp.53-66,2012.6.S.M.Smith,M.Jenkinson,M.W.Woolrich,C.F.Beckmann,T.E.Behrens,H.Johansen-Berg,etal.,"Advancesinfunc/onalandstructuralMRimageanalysisandimplementa/onasFSL,"Neuroimage,vol.23,pp.S208-S219,20047.HoutchensMK,BenedictRH,KillianyR,SharmaJ,JaisaniZ,SinghB,Weinstock-Gu`manB,Gu`manCR,BakshiR.Thalamicatrophyandcogni/oninmul/plesclerosis.Neurology2007;69:1213-23.8.SchoonheimMM,HulstHE,BrandtRB,StrikM,WinkAM,UitdehaagBMJ,BarkhofF,GeurtsJJG.Thalamusstructureandfunc/ondetermineseverityofcogni/veimpairmentinmul/plesclerosis.Neurology2015;84:776-83.9RoccaMA,ValsasinaP,AbsintaM,RiccitelliG,.RodegherME,MisciP,RossiP,FaliniA,ComiG,FilippiM.default-modenetworkdysfunc/onandcogni/veimpairmentinprogressiveMS.Neurology2010;74:1252-5910.JonesDT,MateenFJ,LucchinenCF,JackCR,WelkerKM.DefaultModenetworkdisrup/onsecondarytoalesionintheanteriorthalamus/ArchNeurol2011;68:242-246.11.AkbarN,GiorgioA,TillC,SledJG,DoesburgSM,DeStefanoN,BanwellB.Altera/onsoffunc/onalandstructuralconnec/vityinpediatric-onsetmul/plesclerosis.PloSOne2016;11:1-14.

BilateraldecreasedDTIconnec/vityinMSsubjectscomparedtocontrols.AsymmetricdecreasedfMRIconnec/vityinvolvinglefcingulateandparietalcortex.

Higherfunc/onalconnec/vitywasobservedinbilateralposteriorcingulatecortexandlefprecuneus.

DTI

DTI

fMRI

fMRI

BilateraldecreasedDTIconnec/vityinMSsubjectscomparedtocontrols.AsymmetricdecreasedfMRIconnec/vityinvolvingbilateralthalamusandleffrontalandparietallobes.

DTI

DTI

fMRI

fMRI

BilateraldecreasedDTIconnec/vityinMSsubjectscomparedtocontrols.DecreasedfMRIconnec/vityinvolvingbilateralhippocampus.

BilateraldecreasedDTIconnec/vityinMSsubjectscomparedtocontrols.DecreasedfMRIconnec/vityinvolvingbilateralfusiformgyrus,lefangulargyrus,andtemporalpole.

BilateraldecreasedDTIconnec/vityinMSsubjectscomparedtocontrols.Mixedpa`ernofdecreasedandincreasedfMRIconnec/vitybilaterally.

DTI

DTI

fMRI

fMRI

DTI

DTI fMRI

fMRI

fMRI

fMRI

DTI

DTI

0.0011 0.2154 0.2202 0.2202 0.2202

0.0002 0.0003 0.2202 0.2202 0.2202

0.3000 0.0885 0.2395

0.0000 0.2638 0.0000 0.1245

0.0005 0.1056 0.0004 0.2006 0.0017

0.1588 0.1045 0.3000 0.1262 0.1401 0.1326

0.1484 0.1574 0.0410 0.0256 0.3000 0.3000 0.0012

0.2589 0.0384 0.2468 0.3000 0.0034 0.3000 0.0037 0.0002

0.3000 0.1688 0.2973 0.1164 0.1732 0.0382 0.3000 0.0187 0.2455

0.1498 0.0155 0.0255 0.3000 0.0145 0.2067 0.0061 0.0271 0.0042 0.0051

0.0755 0.3000 0.2514 0.0546 0.2710 0.0006 0.0005 0.0844 0.0005 0.3000 0.0001

L ITG

L MOG

L MTG

L TP

L AG

L IFG

R ITG

R MOG

R MTG

R TP

R AG

R ITG

L ITG

L MOG

L MTG

L TP

L AG

L IFG

R ITG

R MOG

R MTG

R TP

R AG

R IFG

P-Value

Increased Connectivity in MS

Decreased Connectivity in MS

0.0000 0.2202 0.1123 0.1424 0.2202 0.1155

0.1832 0.0000 0.2202 0.1800 0.2202 0.2202

0.0001 0.0000 0.0000 0.2202 0.3000

0.0001 0.0000 0.0003 0.0000 0.2202 0.2202

0.0006 0.0782 0.1208 0.0022 0.0000

0.0000 0.0002 0.2852 0.0411 0.0638 0.0000

0.0007 0.3000 0.2382 0.3000 0.1655 0.0992 0.0000

0.0019 0.0013 0.0197 0.0027 0.1123 0.0003 0.0034

0.0281 0.0037 0.0385 0.0024 0.0027 0.0001 0.0001 0.0050

0.1479 0.3000 0.3000 0.0020 0.0145 0.0001 0.3000 0.3000 0.0022 0.0000

L MPFC

L RACC

L PCC

L PC

L LPC

R MPFC

R RACC

R PCC

R PC

R LPC

L MPFC

L RACC

L PCC

L PC

L LPC

R MPFC

R RACC

R PCC

R PC

R LPC

P-Value

Increased Connectivity in MS

Decreased Connectivity in MS

0.1143 0.2803 0.2633 0.1414 0.3000 0.1801

0.1566 0.2202 0.0910

0.3000 0.0063 0.1062 0.2202 0.2202 0.3000

0.0277 0.0005 0.0296 0.3000

0.0328 0.0010 0.0006 0.0000 0.1527

0.0484 0.0002 0.0015 0.0001 0.0040 0.1295

0.0026 0.0000 0.0550 0.0040 0.0001 0.0000

0.0203 0.2443 0.0000 0.0000 0.1581 0.2003 0.0001

0.0012 0.1478 0.0000 0.0000 0.0019 0.3000 0.0002 0.0029

0.0093 0.0021 0.0747 0.0095 0.0145 0.0765 0.0011 0.0001 0.0000

0.1491 0.0000 0.0333 0.1281 0.2399 0.0048 0.0003 0.0018 0.0001 0.0003

L THAL

(1)

L SPL (2)

L MFG

(3)

L SFG (4)

L AG (5)

L SMG

(6)

R THAL

(1)

R SPL (2)

R MFG

(3)

R SFG (4)

R AG (5)

R SMG

(6)

L THAL (1)

L SPL (2)

L MFG (3)

L SFG (4) L

AG (5)

L SMG (6)

R THAL

(1)

R SPL (2)

R MFG

(3)

R SFG (4)

R AG (5) R

SMG (6)

P-Value

Increased Connectivity in MS

Decreased Connectivity in MS

0.2014 0.2023

0.0001 0.1062 0.2202 0.0260 0.1062 0.0882

0.0010 0.0001 0.0000 0.0872 0.2202 0.1501

0.0040 0.1117 0.0002 0.0000 0.1857 0.3000

0.0011 0.0003 0.0064 0.0031 0.0000 0.3000 0.3000

0.3000 0.1431 0.0059 0.3000 0.1340 0.0000 0.1491

0.0145 0.0410 0.0021 0.0765 0.0143 0.0090 0.0000

0.1841 0.0547 0.0069 0.1673 0.0263 0.2499 0.1044 0.0000

0.0001 0.3000 0.0000 0.0000 0.0166 0.3000 0.0011 0.0393 0.0000

0.2399 0.1411 0.0000 0.0048 0.2091 0.2592 0.0003 0.0861 0.0003

0.0095 0.0048 0.0006 0.0242 0.1760 0.1886 0.0112 0.0066 0.0004 0.0007 0.0000

0.0691 0.1386 0.2795 0.3000 0.3000 0.0006 0.3000 0.3000 0.0011 0.3000 0.0145 0.0000

L AG

L FG

L SPL

L SMG

L HF

L SFG

R AG

R FG

R SPL

R SMG

R HF

R SFG

L AG

L FG

L SPL

L SMG

L HF

L SFG

R AG

R FG

R SPL

R SMG

R HF

R SFG

P-Value

Increased Connectivity in MS

Decreased Connectivity in MS

0.0000 0.1845 0.1728 0.3000 0.1371 0.0970 0.3000 0.0749 0.2373

0.0221 0.0000 0.1892 0.3000 0.1345 0.2553 0.2003 0.3000 0.3000

0.0006 0.0229 0.0000 0.3000 0.2957 0.3000 0.3000 0.3000 0.3000

0.0175 0.0006 0.2319 0.0000 0.3000 0.3000 0.1348 0.0132 0.2346

0.2641 0.0022 0.0241 0.1163 0.0000 0.0725 0.1848 0.1778 0.1661

0.0008 0.0022 0.3000 0.3000 0.0142 0.0000 0.2971 0.0180 0.1315

0.0099 0.3000 0.0000 0.0082 0.0538 0.0054 0.0000 0.2983 0.1652

0.0624 0.2859 0.0027 0.0017 0.3000 0.3000 0.1148 0.0000 0.1332

0.3000 0.3000 0.2901 0.1085 0.2391 0.1924 0.1350 0.0391 0.0000

L CR

L SFG

L SPL

L SMG

R CR

R SFG

R SPL

R SMG FORNIX

L CR

L SFG

L SPL

L SMG

R CR

R SFG

R SPL

R SMG

FORNIX

P-Value

Increased Connectivity in MS

Decreased Connectivity in MS

Side

Anterior Limb of Internal Capsule

Frontal Lobe WM

Globus Palladus

Hippocampal Formation

Lateral Occipito-

temporal Gyrus

Occipital Lobe WM

Parietal Lobe WM

Temporal Lobe WM

Uncus Corpus Callosum

Time point 1st 2nd 1st 2nd 1st 2nd 1st 2nd 1st 2nd 1st 2nd 1st 2nd 1st 2nd 1st 2nd 1st 2nd

Right 62.5 62.5 62.5 75 37.5 62.5 62.5 75 50 62.5 50 62.5 75 75 87.5 75 62.5 75

75 75Left 75 75 75 75 75 62.5 62.5 62.5 0 0 37.5 37.5 62.5 75 62.5 62.5 75 75

The percentile of the MS patients (N=8) having increase in FA reduction at 1 year follow up