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01-03-2022 | Original Article

Structural perisylvian asymmetry in naturally occurring atypical language dominance

Authors: Robin Gerrits, Helena Verhelst, Thijs Dhollander, Li Xiang, Guy Vingerhoets

Published in: Brain Structure and Function | Issue 2/2022

Abstract

Functional and anatomical hemispheric asymmetries abound in the neural language system, yet the relationship between them remains elusive. One attractive proposal is that structural interhemispheric differences reflect or even drive functional language laterality. However, studies on structure–function couplings either find that left and right language dominant individuals display similar leftward structural asymmetry or yield inconsistent results. The current study aimed to replicate and extend prior work by comparing structural asymmetries between neurologically healthy left-handers with right hemispheric language dominance (N = 24) and typically lateralized left-handed controls (N = 39). Based on structural MRI data, anatomical measures of six ‘language-related’ perisylvian structures were derived, including the surface area of five gray matter regions with known language functions and the FDC (combined fiber density and fiber-bundle cross-sectional area) of the arcuate fasciculus. Only the surface area of the pars triangularis and the anterior insula differed significantly between participant groups, being on average leftward asymmetric in those with typical dominance, but right lateralized in volunteers with atypical language specialization. However, these findings did not survive multiple testing correction and the asymmetry of these structures demonstrated much inter-individual variability in either subgroup. By integrating our findings with those reported previously we conclude that while some perisylvian anatomical asymmetries may differ subtly between typical and atypical speech dominants at the group level, they serve as poor participant-specific predictors of hemispheric language specialization.

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Andersson JLR, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125:1063–1078. https://doi.org/10.1016/j.neuroimage.2015.10.019CrossRefPubMed

Andersson JLR, Skare S, Ashburner J (2003) How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage 20:870–888. https://doi.org/10.1016/S1053-8119(03)00336-7CrossRefPubMed

Bain JS, Yeatman JD, Schurr R, Rokem A, Mezer AA (2019) Evaluating arcuate fasciculus laterality measurements across dataset and tractography pipelines. Hum Brain Mapp. https://doi.org/10.1002/hbm.24626CrossRefPubMedPubMedCentral

Biduła SP, Króliczak G (2015) Structural asymmetry of the insula is linked to the lateralization of gesture and language. Eur J Neurosci 41:1438–1447. https://doi.org/10.1111/ejn.12888CrossRefPubMedPubMedCentral

Bradshaw AR, Bishop DVM, Woodhead ZVJ (2017) Methodological considerations in assessment of language lateralisation with fMRI: a systematic review. PeerJ 5:e3557. https://doi.org/10.7717/peerj.3557CrossRefPubMedPubMedCentral

Carey DP, Johnstone LT (2014) Quantifying cerebral asymmetries for language in dextrals and adextrals with random-effects meta analysis. Front Psychol. https://doi.org/10.3389/fpsyg.2014.01128CrossRefPubMedPubMedCentral

Catani M, Mesulam M (2008) The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state. Cortex 44:953–961. https://doi.org/10.1016/j.cortex.2008.04.002CrossRefPubMedPubMedCentral

Catani M, Jones DK, ffytche DH, (2005) Perisylvian language networks of the human brain. Ann Neurol 57:8–16. https://doi.org/10.1002/ana.20319CrossRefPubMed

Chance SA (2014) The cortical microstructural basis of lateralized cognition: a review. Front Psychol. https://doi.org/10.3389/fpsyg.2014.00820CrossRefPubMedPubMedCentral

Chiarello C, Vazquez D, Felton A, Leonard CM (2013) Structural asymmetry of anterior insula: behavioral correlates and individual differences. Brain Lang 126:109–122. https://doi.org/10.1016/j.bandl.2013.03.005CrossRefPubMedPubMedCentral

Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53:1–15. https://doi.org/10.1016/j.neuroimage.2010.06.010CrossRefPubMed

Dick AS, Bernal B, Tremblay P (2014) The language connectome: new pathways, new concepts. Neuroscientist 20:453–467. https://doi.org/10.1177/1073858413513502CrossRefPubMed

Dorsaint-Pierre R, Penhune VB, Watkins KE, Neelin P, Lerch JP, Bouffard M, Zatorre RJ (2006) Asymmetries of the planum temporale and Heschl’s gyrus: relationship to language lateralization. Brain 129:1164–1176. https://doi.org/10.1093/brain/awl055CrossRefPubMed

Ellmore TM, Beauchamp MS, Breier JI, Slater JD, Kalamangalam GP, O’Neill TJ, Disano MA, Tandon N (2010) Temporal lobe white matter asymmetry and language laterality in epilepsy patients. Neuroimage 49:2033–2044. https://doi.org/10.1016/j.neuroimage.2009.10.055CrossRefPubMed

Fernández G, de Greiff A, von Oertzen J, Reuber M, Lun S, Klaver P, Ruhlmann J, Reul J, Elger CE (2001) Language mapping in less than 15 minutes: real-time functional MRI during routine clinical investigation. Neuroimage 14:585–594. https://doi.org/10.1006/nimg.2001.0854CrossRefPubMed

Forkel SJ, Thiebaut de Schotten M, Dell’Acqua F, Kalra L, Murphy DGM, Williams SCR, Catani M (2014) Anatomical predictors of aphasia recovery: a tractography study of bilateral perisylvian language networks. Brain 137:2027–2039. https://doi.org/10.1093/brain/awu113CrossRefPubMed

Foundas AL, Leonard CM, Gilmore R, Fennell E, Heilman KM (1994) Planum temporale asymmetry and language dominance. Neuropsychologia 32:1225–1231. https://doi.org/10.1016/0028-3932(94)90104-XCrossRefPubMed

Foundas AL, Leonard CM, Gilmore RL, Fennell EB, Heilman KM (1996) Pars triangularis asymmetry and language dominance. Proc Natl Acad Sci 93:719–722. https://doi.org/10.1073/pnas.93.2.719CrossRefPubMedPubMedCentral

Geschwind N, Levitsky W (1968) Human brain: left-right asymmetries in temporal speech region. Science 161:186–187. https://doi.org/10.1126/science.161.3837.186CrossRefPubMed

Glasser MF, Rilling JK (2008) DTI tractography of the human brain’s language pathways. Cereb Cortex 18:2471–2482. https://doi.org/10.1093/cercor/bhn011CrossRefPubMed

Greve DN, Van der Haegen L, Cai Q, Stufflebeam S, Sabuncu MR, Fischl B, Brysbaert M (2013) A surface-based analysis of language lateralization and cortical asymmetry. J Cogn Neurosci 25:1477–1492. https://doi.org/10.1162/jocn_a_00405CrossRefPubMedPubMedCentral

Hartwigsen G, Saur D (2019) Neuroimaging of stroke recovery from aphasia—insights into plasticity of the human language network. Neuroimage 190:14–31. https://doi.org/10.1016/j.neuroimage.2017.11.056CrossRefPubMed

Honnedevasthana Arun A, Connelly A, Smith RE, Calamante F (2021) Characterisation of white matter asymmetries in the healthy human brain using diffusion MRI fixel-based analysis. Neuroimage 225:117505. https://doi.org/10.1016/j.neuroimage.2020.117505CrossRefPubMed

Hutsler JJ (2003) The specialized structure of human language cortex: pyramidal cell size asymmetries within auditory and language-associated regions of the temporal lobes. Brain Lang 86:226–242. https://doi.org/10.1016/S0093-934X(02)00531-XCrossRefPubMed

Jäncke L, Steinmetz H (1993) Auditory lateralization and planum temporale asymmetry. NeuroReport 5:169–172. https://doi.org/10.1097/00001756-199311180-00019CrossRefPubMed

Jansen A, Menke R, Sommer J, Förster AF, Bruchmann S, Hempleman J, Weber B, Knecht S (2006) The assessment of hemispheric lateralization in functional MRI—robustness and reproducibility. Neuroimage 33:204–217. https://doi.org/10.1016/j.neuroimage.2006.06.019CrossRefPubMed

Jansen A, Liuzzi G, Deppe M, Kanowski M, Ölschläger C, Albers JM, Schlaug G, Knecht S (2010) Structural correlates of functional language dominance: a voxel-based morphometry study. J Neuroimaging 20:148–156. https://doi.org/10.1111/j.1552-6569.2009.00367.xCrossRefPubMed

Jeurissen B, Tournier J-D, Dhollander T, Connelly A, Sijbers J (2014) Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. Neuroimage 103:411–426. https://doi.org/10.1016/j.neuroimage.2014.07.061CrossRefPubMed

Josse G, Tzourio-Mazoyer N (2004) Hemispheric specialization for language. Brain Res Rev 44:1–12. https://doi.org/10.1016/j.brainresrev.2003.10.001CrossRefPubMed

Josse G, Kherif F, Flandin G, Seghier ML, Price CJ (2009) Predicting language lateralization from gray matter. J Neurosci 29:13516–13523. https://doi.org/10.1523/JNEUROSCI.1680-09.2009CrossRefPubMedPubMedCentral

Keller SS, Roberts N, García-Fiñana M, Mohammadi S, Ringelstein EB, Knecht S, Deppe M (2011) Can the language-dominant hemisphere be predicted by brain anatomy? J Cogn Neurosci 23:2013–2029. https://doi.org/10.1162/jocn.2010.21563CrossRefPubMed

Keller SS, Roberts N, Baker G, Sluming V, Cezayirli E, Mayes A, Eldridge P, Marson AG, Wieshmann UC (2018) A voxel-based asymmetry study of the relationship between hemispheric asymmetry and language dominance in Wada tested patients. Hum Brain Mapp 39:3032–3045. https://doi.org/10.1002/hbm.24058CrossRefPubMedPubMedCentral

Kellner E, Dhital B, Kiselev VG, Reisert M (2016) Gibbs-ringing artifact removal based on local subvoxel-shifts: Gibbs-Ringing Artifact Removal. Magn Reson Med 76:1574–1581. https://doi.org/10.1002/mrm.26054CrossRefPubMed

Knecht S, Deppe M, Dräger B, Bobe L, Lohmann H, Ringelstein E-B, Henningsen H (2000a) Language lateralization in healthy right-handers. Brain 123:74–81. https://doi.org/10.1093/brain/123.1.74CrossRefPubMed

Knecht S, Dräger B, Deppe M, Bobe L, Lohmann H, Floel A, Ringelstein E-B, Henningsen H (2000b) Handedness and hemispheric language dominance in healthy humans. Brain 123:2512–2518. https://doi.org/10.1093/brain/123.12.2512CrossRefPubMed

Kong XZ, Mathias SR, Guadalupe T, ENIGMA Laterality Working Group, Glahn DC, Franke B, Crivello F, Tzourio-Mazoyer N, Fisher SE, Thompson PM, Francks C (2018) Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA Consortium. Proc Natl Acad Sci USA 115:E5154–E5163. Doi: https://doi.org/10.1073/pnas.1718418115

Matsumoto R, Okada T, Mikuni N, Mitsueda-Ono T, Taki J, Sawamoto N, Hanakawa T, Miki Y, Hashimoto N, Fukuyama H, Takahashi R, Ikeda A (2008) Hemispheric asymmetry of the arcuate fasciculus: a preliminary diffusion tensor tractography study in patients with unilateral language dominance defined by Wada test. J Neurol 255:1703–1711. https://doi.org/10.1007/s00415-008-0005-9CrossRefPubMed

Mazoyer B, Zago L, Jobard G, Crivello F, Joliot M, Perchey G, Mellet E, Petit L, Tzourio-Mazoyer N (2014) Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS ONE 9:e101165. https://doi.org/10.1371/journal.pone.0101165CrossRefPubMedPubMedCentral

Moffat S (1998) Morphology of the planum temporale and corpus callosum in left handers with evidence of left and right hemisphere speech representation. Brain 121:2369–2379. https://doi.org/10.1093/brain/121.12.2369CrossRefPubMed

Ocklenburg S, Friedrich P, Güntürkün O, Genç E (2016) Intrahemispheric white matter asymmetries: the missing link between brain structure and functional lateralization? Rev Neurosci 27:465–480. https://doi.org/10.1515/revneuro-2015-0052CrossRefPubMed

Osa García A, Brambati SM, Brisebois A, Désilets-Barnabé M, Houzé B, Bedetti C, Rochon E, Leonard C, Desautels A, Marcotte K (2020) Predicting early post-stroke aphasia outcome from initial aphasia severity. Front Neurol 11:120. https://doi.org/10.3389/fneur.2020.00120CrossRefPubMedPubMedCentral

Penhune VB, Zatorre RJ, MacDonald JD, Evans AC (1996) Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex 6:661–672. https://doi.org/10.1093/cercor/6.5.661CrossRefPubMed

Powell HWR, Parker GJM, Alexander DC, Symms MR, Boulby PA, Wheeler-Kingshott CAM, Barker GJ, Noppeney U, Koepp MJ, Duncan JS (2006) Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage 32:388–399. https://doi.org/10.1016/j.neuroimage.2006.03.011CrossRefPubMed

Price CJ (2012) A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. Neuroimage 62:816–847. https://doi.org/10.1016/j.neuroimage.2012.04.062CrossRefPubMed

Propper RE, O’Donnell LJ, Whalen S, Tie Y, Norton IH, Suarez RO, Zollei L, Radmanesh A, Golby AJ (2010) A combined fMRI and DTI examination of functional language lateralization and arcuate fasciculus structure: effects of degree versus direction of hand preference. Brain Cogn 73:85–92. https://doi.org/10.1016/j.bandc.2010.03.004CrossRefPubMedPubMedCentral

Raffelt D, Tournier J-D, Crozier S, Connelly A, Salvado O (2012a) Reorientation of fiber orientation distributions using apodized point spread functions. Magn Reson Med 67:844–855. https://doi.org/10.1002/mrm.23058CrossRefPubMed

Raffelt D, Tournier J-D, Rose S, Ridgway GR, Henderson R, Crozier S, Salvado O, Connelly A (2012b) Apparent fibre density: a novel measure for the analysis of diffusion-weighted magnetic resonance images. Neuroimage 59:3976–3994. https://doi.org/10.1016/j.neuroimage.2011.10.045CrossRefPubMed

Raffelt DA, Tournier J-D, Smith RE, Vaughan DN, Jackson G, Ridgway GR, Connelly A (2017) Investigating white matter fibre density and morphology using fixel-based analysis. Neuroimage 144:58–73. https://doi.org/10.1016/j.neuroimage.2016.09.029CrossRefPubMed

Schmitz J, Fraenz C, Schlüter C, Friedrich P, Jung RE, Güntürkün O, Genç E, Ocklenburg S (2019) Hemispheric asymmetries in cortical gray matter microstructure identified by neurite orientation dispersion and density imaging. Neuroimage 189:667–675. https://doi.org/10.1016/j.neuroimage.2019.01.079CrossRefPubMed

Shapleske J, Rossell SL, Woodruff PWR, David AS (1999) The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Rev 29:26–49. https://doi.org/10.1016/S0165-0173(98)00047-2CrossRefPubMed

Silva G, Citterio A (2017) Hemispheric asymmetries in dorsal language pathway white-matter tracts: a magnetic resonance imaging tractography and functional magnetic resonance imaging study. Neuroradiol J 30:470–476. https://doi.org/10.1177/1971400917720829CrossRefPubMedPubMedCentral

Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DGM, Catani M (2011) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54:49–59. https://doi.org/10.1016/j.neuroimage.2010.07.055CrossRefPubMed

Tournier JD, Calamante F, Connelly A (2010) Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distribution. In: Proceedings of the international society for magnetic resonance in medicine, pp 1670

Tzourio-Mazoyer N, Crivello F, Mazoyer B (2017a) Is the planum temporale surface area a marker of hemispheric or regional language lateralization? Brain Struct Funct. https://doi.org/10.1007/s00429-017-1551-7CrossRefPubMed

Tzourio-Mazoyer N, Perrone-Bertolotti M, Jobard G, Mazoyer B, Baciu M (2017b) Multi-factorial modulation of hemispheric specialization and plasticity for language in healthy and pathological conditions: a review. Cortex 86:314–339. https://doi.org/10.1016/j.cortex.2016.05.013CrossRefPubMed

Uylings HBM, Jacobsen AM, Zilles K, Amunts K (2006) Left-right asymmetry in volume and number of neurons in adult Broca’s area. Cortex 42:652–658. https://doi.org/10.1016/S0010-9452(08)70401-5CrossRefPubMed

Van der Haegen L, Cai Q, Seurinck R, Brysbaert M (2011) Further fMRI validation of the visual half field technique as an indicator of language laterality: a large-group analysis. Neuropsychologia 49:2879–2888. https://doi.org/10.1016/j.neuropsychologia.2011.06.014CrossRefPubMed

Vassal F, Schneider F, Boutet C, Jean B, Sontheimer A, Lemaire J-J (2016) Combined DTI tractography and functional MRI study of the language connectome in healthy volunteers: extensive mapping of white matter fascicles and cortical activations. PLoS ONE 11:e0152614. https://doi.org/10.1371/journal.pone.0152614CrossRefPubMedPubMedCentral

Veraart J, Novikov DS, Christiaens D, Ades-aron B, Sijbers J, Fieremans E (2016) Denoising of diffusion MRI using random matrix theory. Neuroimage 142:394–406. https://doi.org/10.1016/j.neuroimage.2016.08.016CrossRefPubMed

Verhelst H, Dhollander T, Gerrits R, Vingerhoets G (2021) Fibre-specific laterality of white matter in left and right language dominant people. Neuroimage 230:117812. https://doi.org/10.1016/j.neuroimage.2021.117812CrossRefPubMed

Vernooij MW, Smits M, Wielopolski PA, Houston GC, Krestin GP, van der Lugt A (2007) Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: a combined fMRI and DTI study. Neuroimage 35:1064–1076. https://doi.org/10.1016/j.neuroimage.2006.12.041CrossRefPubMed

Wada JA (1975) Cerebral hemispheric asymmetry in humans: cortical speech zones in 100 adult and 100 infant brains. Arch Neurol 32:239. https://doi.org/10.1001/archneur.1975.00490460055007CrossRefPubMed

Woodhead ZVJ, Rutherford HA, Bishop DVM (2020) Measurement of language laterality using functional transcranial Doppler ultrasound: a comparison of different tasks. Wellcome Open Res 3:104. https://doi.org/10.12688/wellcomeopenres.14720.3CrossRefPubMedPubMedCentral

Xiang L, Crow TJ, Hopkins WD, Roberts N (2020) Comparison of surface area and cortical thickness asymmetry in the human and chimpanzee brain. Cereb Cortex. https://doi.org/10.1093/cercor/bhaa202CrossRefPubMed

Zatorre RJ, Belin P, Penhune VB (2002) Structure and function of auditory cortex: music and speech. Trends Cogn Sci 6:37–46. https://doi.org/10.1016/S1364-6613(00)01816-7CrossRefPubMed

Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61:1000–1016. https://doi.org/10.1016/j.neuroimage.2012.03.072CrossRefPubMed

Title: Structural perisylvian asymmetry in naturally occurring atypical language dominance
Authors: Robin Gerrits
Helena Verhelst
Thijs Dhollander
Li Xiang
Guy Vingerhoets
Publication date: 01-03-2022
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 2/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-021-02323-7

At a glance: The STEP trials

Springer Medicine

Structural perisylvian asymmetry in naturally occurring atypical language dominance

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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