Differential Hemispheric Predilection of Microstructural White Matter and Functional Connectivity Abnormalities between Respectively Semantic and Behavioral Variant Frontotemporal Dementia
Restricted accessResearch articleFirst published online January 24, 2017
Differential Hemispheric Predilection of Microstructural White Matter and Functional Connectivity Abnormalities between Respectively Semantic and Behavioral Variant Frontotemporal Dementia
Semantic dementia (SD) and behavioral variant frontotemporal dementia (bvFTD), subtypes of frontotemporal dementia, are characterized by distinct clinical symptoms and neuroimaging features, with predominant left temporal grey matter (GM) atrophy in SD and bilateral or right frontal GM atrophy in bvFTD. Such differential hemispheric predilection may also be reflected by other neuroimaging features, such as brain connectivity. This study investigated white matter (WM) microstructure and functional connectivity differences between SD and bvFTD, focusing on the hemispheric predilection of these differences. Eight SD and 12 bvFTD patients, and 17 controls underwent diffusion tensor imaging and resting state functional MRI at 3T. Whole-brain WM microstructure was assessed to determine distinct WM tracts affected in SD and bvFTD. For these tracts, diffusivity measures and lateralization indices were calculated. Functional connectivity was established for GM regions affected in early stage SD or bvFTD. Results of a direct comparison between SD and bvFTD are reported. Whole-brain WM microstructure abnormalities were more pronounced in the left hemisphere in SD and bilaterally— with a slight predilection for the right— in bvFTD. Lateralization of tract-specific abnormalities was seen in SD only, toward the left hemisphere. Functional connectivity of disease-specific regions was mainly decreased bilaterally in SD and in the right hemisphere in bvFTD. SD and bvFTD show WM microstructure and functional connectivity abnormalities in different regions, that are respectively more pronounced in the left hemisphere in SD and in the right hemisphere in bvFTD. This indicates differential hemispheric predilection of brain connectivity abnormalities between SD and bvFTD.
OcklenburgS, BesteC, ArningL, PeterbursJ, GüntürkünO (2014) The ontogenesis of language lateralization and its relation to handedness. Neurosci Biobehav Rev43, 191–198.
7.
CummingsJL (1993) Frontal-subcortical circuits and human behavior. Arch Neurol50, 873–880.
D’AnnaL, MesulamMM, Thiebaut de SchottenM, Dell’AcquaF, MurphyD, WienekeC, MartersteckA, CobiaD, RogalskiE, CataniM (2016) Frontotemporal networks and behavioral symptoms in primary progressive aphasia. Neurology86, 1393–1399.
11.
ZhangS, ArfanakisK (2014) White matter segmentation based on a skeletonized atlas: Effects on diffusion tensor imaging studies of regions of interest. J Magn Reson Imaging40, 1189–1198.
12.
WhitwellJL, AvulaR, SenjemML, KantarciK, WeigandSD, SamikogluA, EdmonsonHA, VemuriP, KnopmanDS, BoeveBF, PetersenRC, JosephsKA, JackCR (2010) Gray and white matter water diffusion in the syndromic variants of frontotemporal dementia. Neurology74, 1279–1287.
13.
SajjadiSA, Acosta-CabroneroJ, PattersonK, Diaz-de-GrenuLZ, WilliamsGB, NestorPJ (2013) Diffusion tensor magnetic resonance imaging for single subject diagnosis in neurodegenerative diseases. Brain136, 2253–2261.
14.
BothaH, DuffyJR, WhitwellJL, StrandEA, MachuldaMM, SchwarzCG, ReidRI, SpychallaAJ, SenjemML, JonesDT, LoweV, JackCR, JosephsKA (2015) Classification and clinicoradiologic features of primary progressive aphasia (PPA) and apraxia of speech. Cortex69, 220–236.
15.
AgostaF, HenryRG, MigliaccioR, NeuhausJ, MillerBL, DronkersNF, BrambatiSM, FilippiM, OgarJM, WilsonSM, Gorno-TempiniML (2010) Language networks in semantic dementia. Brain133, 286–299.
16.
Acosta-CabroneroJ, PattersonK, FryerTD, HodgesJR, PengasG, WilliamsGB, NestorPJ (2011) Atrophy, hypometabolism and white matter abnormalities in semantic dementia tell a coherent story. Brain134, 2025–2035.
17.
Tovar-MollF, de Oliveira-SouzaR, BramatiIE, ZahnR, CavanaghA, TierneyM, MollJ, GrafmanJ (2014) White matter tract damage in the behavioral variant of frontotemporal and corticobasal dementia syndromes. PLoS One9, e102656.
18.
MahoneyCJ, RidgwayGR, MaloneIB, DowneyLE, BeckJ, KinnunenKM, SchmitzN, GoldenHL, RohrerJD, SchottJM, RossorMN, OurselinS, MeadS, FoxNC, WarrenJD (2014) Profiles of white matter tract pathology in frontotemporal dementia. Hum Brain Mapp35, 4163–4179.
19.
ZhangY, TartagliaMC, SchuffN, ChiangGC, ChingC, RosenHJ, Gorno-TempiniML, MillerBL, WeinerMW (2013) MRI signatures of brain macrostructural atrophy and microstructural degradation in frontotemporal lobar degeneration subtypes. J Alzheimers Dis33, 431–444.
FolsteinMF, FolsteinSE, McHughPR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res12, 189–198.
29.
BronEE, SteketeeRME, HoustonGC, OliverRA, AchterbergHC, LoogM, van SwietenJC, HammersA, NiessenWJ, SmitsM, KleinS (2014) Diagnostic classification of arterial spin labeling and structural MRI in presenile early stage dementia. Hum Brain Mapp35, 4916–4931.
WinklerAM, RidgwayGR, WebsterMA, SmithSM, NicholsTE (2014) Permutation inference for the general linear model. Neuroimage92, 381–397.
37.
SmithSM, NicholsTE (2009) Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage44, 83–98.
38.
de GrootM, VernooijMW, KleinS, IkramMA, VosFM, SmithSM, NiessenWJ, AnderssonJLR (2013) Improving alignment in Tract-based spatial statistics: Evaluation and optimization of image registration. Neuroimage76, 400–411.
39.
BehrensTEJ, BergHJ, JbabdiS, RushworthMFS, WoolrichMW (2007) Probabilistic diffusion tractography with multiple fibre orientations: What can we gain?Neuroimage34, 144–155.
40.
de GrootM, IkramMA, AkoudadS, KrestinGP, HofmanA, van der LugtA, NiessenWJ, VernooijMW (2015) Tract-specific white matter degeneration in aging: The Rotterdam Study. Alzheimers Dement11, 321–330.
41.
JenkinsonM, BannisterP, BradyM, SmithS (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage17, 825–841.
42.
HammersA, AllomR, KoeppMJ, FreeSL, MyersR, LemieuxL, MitchellTN, BrooksDJ, DuncanJS (2003) Three-dimensional maximum probability atlas of the human brain, with particular reference to the temporal lobe. Hum Brain Mapp19, 224–247.
43.
BeckmannCF, DeLucaM, DevlinJT, SmithSM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc L B Biol Sci360, 1001–1013.
44.
GelmanA, HillJ, YajimaM (2012) Why we (usually) don’t have to worry about multiple comparisons. J Res Educ Eff5, 189–211.
45.
DickAS, BernalB, TremblayP (2014) The language connectome: New pathways, new concepts. Neuroscientist20, 453–467.
46.
SaurD, KreherBW, SchnellS, KümmererD, KellmeyerP, VryM-S, UmarovaR, MussoM, GlaucheV, AbelS, HuberW, RijntjesM, HennigJ, WeillerC (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci U S A105, 18035–18040.
47.
Von Der HeideRJ, SkipperLM, KlobusickyE, OlsonIR (2013) Dissecting the uncinate fasciculus: Disorders, controversies and a hypothesis. Brain136, 1692–1707.
48.
HornbergerM, GengJ, HodgesJR (2011) Convergent grey and white matter evidence of orbitofrontal cortex changes related to disinhibition in behavioural variant frontotemporal dementia. Brain134, 2502–2512.
49.
PowersJP, MassimoL, McMillanCT, YushkevichPA, ZhangH, GeeJC, GrossmanM (2014) White matter disease contributes to apathy and disinhibition in behavioral variant frontotemporal dementia. Cogn Behav Neurol27, 206–214.
50.
TartagliaMC, ZhangY, RacineC, LaluzV, NeuhausJ, ChaoL, KramerJ, RosenH, MillerB, WeinerM (2012) Executive dysfunction in frontotemporal dementia is related to abnormalities in frontal white matter tracts. J Neurol259, 1071–1080.
51.
CrespiC, CeramiC, DodichA, CanessaN, ArponeM, IannacconeS, CorboM, LunettaC, ScolaE, FaliniA, CappaSF (2014) Microstructural white matter correlates of emotion recognition impairment in amyotrophic lateral sclerosis. Cortex53, 1–8.
52.
TaddeiM, TettamantiM, ZanoniA, CappaS, BattagliaM (2012) Brain white matter organisation in adolescence is related to childhood cerebral responses to facial expressions and harm avoidance. Neuroimage61, 1394–1401.
53.
SchmidtAT, HantenG, LiX, WildeEA, IbarraAP, ChuZD, HelblingAR, ShahS, LevinHS (2013) Emotional prosody and diffusion tensor imaging in children after traumatic brain injury. Brain Inj27, 1528–1535.
54.
Pérez-IglesiasR, Tordesillas-GutiérrezD, McGuirePK, BarkerGJ, Roiz-SantiañezR, MataI, de LucasEM, Rodríguez-SánchezJM, Ayesa-ArriolaR, Vazquez-BarqueroJL, Crespo-FacorroB (2010) White matter integrity and cognitive impairment in first-episode psychosis. Am J Psychiatry167, 451–458.
55.
SongS-K, SunS-W, JuW-K, LinS-J, CrossAH, NeufeldAH (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage20, 1714–1722.
56.
SongS-K, SunS-W, RamsbottomMJ, ChangC, RussellJ, CrossAH (2002) Dysmyelination revealed through MRI as Increased radial (but unchanged axial) diffusion of water. Neuroimage17, 1429–1436.
57.
WongC, GallateJ (2012) The function of the anterior temporal lobe: A review of the empirical evidence. Brain Res1449, 94–116.
58.
GainottiG (2015) Is the difference between right and left ATLs due to the distinction between general and social cognition or between verbal and non-verbal representations?Neurosci Biobehav Rev51, 296–312.
59.
BroeM, HodgesJR, SchofieldE, ShepherdCE, KrilJJ, HallidayGM (2003) Staging disease severity in pathologically confirmed cases of frontotemporal dementia. Neurology60, 1005–1011.
60.
MummeryCJ, PattersonK, PriceCJ, AshburnerJ, FrackowiakRS, HodgesJR (2000) A voxel-based morphometry study of semantic dementia: Relationship between temporal lobe atrophy and antic memory. Ann Neurol47, 36–45.
61.
OlsonIR, McCoyD, KlobusickyE, RossLA (2013) Social cognition and the anterior temporal lobes: A review and theoretical framework. Soc Cogn Affect Neurosci8, 123–133.
62.
CabezaR, NybergL (2000) Imaging cognition II: An empirical review of 275 PET and fMRI studies. J Cogn Neurosci12, 1–47.
63.
HarveyDY, SchnurTT (2015) Distinct loci of lexical and semantic access deficits in aphasia: Evidence from voxel-based lesion-symptom mapping and diffusion tensor imaging. Cortex67, 37–58.
64.
BookheimerSY, StrojwasMH, CohenMS, SaundersAM, Pericak-VanceMA, MazziottaJC, SmallGW (2000) Patterns of brain activation in people at risk for Alzheimer’s disease. N Engl J Med343, 450–456.
65.
BorroniB, AlbericiA, CercignaniM, PremiE, SerraL, CeriniC, CossedduM, PettenatiC, TurlaM, ArchettiS, GasparottiR, CaltagironeC, PadovaniA, BozzaliM (2012) Granulin mutation drives brain damage and reorganization from preclinical to symptomatic FTLD. Neurobiol Aging33, 2506–2520.
66.
AllisonT, McCarthyG, NobreA, PuceA, BelgerAHuman extrastriate visual cortex and the perception of faces, words, numbers, and colors. Cereb Cortex4, 544–554.
67.
BüchelC, PriceC, FristonK (1998) A multimodal language region in the ventral visual pathway. Nature394, 274–277.
68.
AxelrodV, BarM, ReesG, YovelG (2015) Neural correlates of subliminal language processing. Cereb Cortex25, 2160–2169.
69.
SöderlundH, BlackSE, MillerBL, FreedmanM, LevineB (2008) Episodic memory and regional atrophy in frontotemporal lobar degeneration. Neuropsychologia46, 127–136.
KippsCM, NestorPJ, Acosta-CabroneroJ, ArnoldR, HodgesJR (2009) Understanding social dysfunction in the behavioural variant of frontotemporal dementia: The role of emotion and sarcasm processing. Brain132, 592–603.
72.
HutchingsR, HodgesJR, PiguetO, KumforF, Boutoleau-BretonniéreC (2015) Why should i care? Dimensions of socio-emotional cognition in younger-onset dementia. J Alzheimers Dis48, 135–147.
73.
JefferiesE (2013) The neural basis of semantic cognition: Converging evidence from neuropsychology, neuroimaging and TMS. Cortex49, 611–625.
74.
WirthM, JannK, DierksT, FederspielA, WiestR, HornH (2011) Semantic memory involvement in the default mode network: A functional neuroimaging study using independent component analysis. Neuroimage54, 3057–3066.
75.
ChanY-C, LavalleeJP (2015) Temporo-parietal and fronto-parietal lobe contributions to theory of mind and executive control: An fMRI study of verbal jokes. Front Psychol6, 1285.
76.
Sans-SansaB, McKennaPJ, Canales-RodríguezEJ, Ortiz-GilJ, López-AraquistainL, SarróS, DueñasRM, BlanchJ, SalvadorR, Pomarol-ClotetE (2013) Association of formal thought disorder in schizophrenia with structural brain abnormalities in language-related cortical regions. Schizophr Res146, 308–313.
77.
AwadM, WarrenJE, ScottSK, TurkheimerFE, WiseRJS (2007) A common system for the comprehension and production of narrative speech. J Neurosci27, 11455–11464.
78.
Graff-RadfordJ, JonesDT, Graff-RadfordNR (2014) Pathophysiology of language, speech and emotions in neurodegenerative disease. Parkinsonism Relat Disord20(Suppl 1), S49–S53.
79.
DuvalC, BejaninA, PiolinoP, LaisneyM, de La SayetteV, BelliardS, EustacheF, DesgrangesB (2012) Theory of mind impairments in patients with semantic dementia. Brain135, 228–241.
80.
KumforF, PiguetO (2012) Disturbance of emotion processing in frontotemporal dementia: A synthesis of cognitive and neuroimaging findings. Neuropsychol Rev22, 280–297.
81.
GoodkindMS, SturmVE, AscherEA, ShdoSM, MillerBL, RankinKP, LevensonRW (2015) Emotion recognition in frontotemporal dementia and Alzheimer’s disease: A new film-based assessment. Emotion15, 416–427.
82.
VuilleumierP, PourtoisG (2007) Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging. Neuropsychologia45, 174–194.
83.
CeramiC, CrespiC, Della RosaPA, DodichA, MarconeA, MagnaniG, CoppiE, FaliniA, CappaSF, PeraniD (2015) Brain changes within the visuo-spatial attentional network in posterior cortical atrophy. J Alzheimers Dis43, 385–395.
84.
DamoiseauxJS, RomboutsSA, BarkhofF, ScheltensP, StamCJ, SmithSM, BeckmannCF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A103, 13848–13853.
85.
KaplanE, GoodglassH, WeintraubS (1978) The Boston Naming Test, Lea & Febiger, Philadelphia.
86.
ReyA (1958) L’examen clinique en psychologie, Presses Universitaires de France, Paris, France.
87.
WechslerD (2005) WAIS-II Nederlandse Bewerking. Technische handleiding. Harcourt Test Publishers, Lisse.
88.
War Department (1994) Army Individual Test Battery. Manual of directions and scoring., War Department, Adjutant General’s office, Washington, DC.
89.
StroopJ (1935) Studies of interference in serial verbal reactions. J Exp Psychol18, 643–662.
90.
ThurstoneL, ThurstoneT (1962) Primary mental abilities, Science Research Associates, Chigago.
91.
NelsonHE (1976) A modified card sorting test sensitive to frontal lobe defects. Cortex12, 313–324.
92.
JollesJ, HouxPJ, Van BoxtelMPJ (1995) Maastricht Aging Study: Determinants of cognitive aging, Neuropsych publishers, Maastricht, The Netherlands.
