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White matter asymmetries in human situs inversus totalis

  • Lieselot Mannaert
  • Helena Verhelst
  • Robin Gerrits
  • Stephanie Bogaert
  • Guy VingerhoetsEmail author
Short Communication

Abstract

Diffusion weighted imaging (DWI) was used to investigate white matter asymmetries in participants with situs inversus totalis (SIT) and matched controls. Regardless of visceral condition, hemispheric differences were found for the arcuate fasciculus (ARC) and the superior longitudinal fasciculus (SLF), which are involved in language and visuospatial functioning, respectively. The ARC appears lateralized to the left hemisphere, analogous to the left lateralization of functional areas associated with language. The SLF, on the other hand, is lateralized to the right, corresponding with rightward lateralization of visuospatial functioning. Interestingly, SIT participants show a significantly lower number of streamlines in the Uncinate Fasciculus (UNC). In addition, UNC volume appears associated with measures of cognitive performance, a finding in line with previously reported performance differences between SIT participants and controls.

Keywords

Situs inversus totalis White matter asymmetry Lateralization Arcuate fasciculus Uncinate fasciculus Superior longitudinal fasciculus 

Notes

Funding

This study was funded by the Fonds Wetenschappelijk Onderzoek-Vlaanderen by FWO-grant n° G.0114.16 N assigned to Guy Vingerhoets.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Ameis SH (2015) Altered white matter connectivity as a neural substrate for social impairment in Autism Spectrum Disorder. Cortex 62:158–181.  https://doi.org/10.1016/J.CORTEX.2014.10.014 CrossRefGoogle Scholar
  2. 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.2015.10.019 CrossRefGoogle Scholar
  3. Ashtari M, Cottone J, Ardekani BA, Cervellione K, Szeszko PR, Wu J, Chen S, Kumra S (2007) Disruption of white matter integrity in the inferior longitudinal fasciculus in adolescents with schizophrenia as revealed by fiber tractography. Arch Gen Psychiatry 64(11):1270.  https://doi.org/10.1001/archpsyc.64.11.1270 CrossRefGoogle Scholar
  4. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44(4):625–632CrossRefGoogle Scholar
  5. Büchel C, Raedler T, Sommer M, Sach M, Weiller C, Koch MA (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb Cortex 14(9):945–951.  https://doi.org/10.1093/cercor/bhh055 CrossRefGoogle Scholar
  6. Bush A, Cole P, Hariri M, Mackay I, Phillips G, O’Callaghan C, Wilson R, Warner JO (1998) Primary ciliary dyskinesia: diagnosis and standards of care. Eur Respir J 12(4):982–988CrossRefGoogle Scholar
  7. Catani M, Mesulam M (2008) The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex J Devoted Study Nerv Syst Behav 44(8):953–961.  https://doi.org/10.1016/j.cortex.2008.04.002 CrossRefGoogle Scholar
  8. Catani M, Forkel S, Thiebaut de Schotten M (2010) Asymmetry of white matter pathways. The two halves of the brain. The MIT Press, Cambridge, pp 177–210CrossRefGoogle Scholar
  9. Good CD, Johnsrude I, Ashburner J, Henson RNA, Friston KJ, Frackowiak RSJ (2001) Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. NeuroImage 14(3):685–700.  https://doi.org/10.1006/nimg.2001.0857 CrossRefGoogle Scholar
  10. Goto K, Kurashima R, Gokan H, Inoue N, Ito I, Watanabe S (2010) Left–right asymmetry defect in the hippocampal circuitry impairs spatial learning and working memory in iv mice. PLoS One 5(11):e15468.  https://doi.org/10.1371/journal.pone.0015468 CrossRefGoogle Scholar
  11. Grimes DT, Burdine RD (2017) Left-right patterning: breaking symmetry to asymmetric morphogenesis. Trends Genet 33(9):616–628.  https://doi.org/10.1016/j.tig.2017.06.004 CrossRefGoogle Scholar
  12. Haines DE, Mihailoff GA (2018) The Telencephalon. Fundam Neurosci Basic Clin Appl 225–240:e1.  https://doi.org/10.1016/B978-0-323-39632-5.00016-5 Google Scholar
  13. Hervé P-Y, Crivello F, Perchey G, Mazoyer B, Tzourio-Mazoyer N (2006) Handedness and cerebral anatomical asymmetries in young adult males. NeuroImage 29(4):1066–1079.  https://doi.org/10.1016/j.neuroimage.2005.08.031 CrossRefGoogle Scholar
  14. Highley JR, Walker MA, Esiri MM, Crow TJ, Harrison PJ (2002) Asymmetry of the uncinate fasciculus: a post-mortem study of normal subjects and patients with schizophrenia. Cerebral Cortex (New York, 1991) 12(11):1218–1224CrossRefGoogle Scholar
  15. Hua K, Zhang J, Wakana S, Jiang H, Li X, Reich DS, Calabresi PA, Pekar JJ, van Zijl PCM, Mori S (2008) Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. NeuroImage 39(1):336–347.  https://doi.org/10.1016/j.neuroimage.2007.07.053 CrossRefGoogle Scholar
  16. Kamali A, Flanders AE, Brody J, Hunter JV, Hasan KM (2014) Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Struct Funct 219(1):269–281.  https://doi.org/10.1007/s00429-012-0498-y CrossRefGoogle Scholar
  17. Kumar A, Sundaram SK, Sivaswamy L, Behen ME, Makki MI, Ager J, Janisse J, Chugani HT, Chugani DC (2010) Alterations in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. Cereb Cortex 20(9):2103–2113.  https://doi.org/10.1093/cercor/bhp278 CrossRefGoogle Scholar
  18. Leemans A, Jones DK (2009) The B -matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61(6):1336–1349.  https://doi.org/10.1002/mrm.21890 CrossRefGoogle Scholar
  19. Leigh MW, Pittman JE, Carson JL, Ferkol TW, Dell SD, Davis SD, Knowles MR, Zariwala MA (2009) Clinical and genetic aspects of primary ciliary dyskinesia/Kartagener syndrome. Genet Med 11(7):473–487.  https://doi.org/10.1097/GIM.0b013e3181a53562 CrossRefGoogle Scholar
  20. Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS, Pandya DN (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cerebral Cortex 15(6):854–869.  https://doi.org/10.1093/cercor/bhh186 CrossRefGoogle Scholar
  21. Mega MS, Cummings JL, Salloway S, Malloy P (1997) The limbic system: an anatomic, phylogenetic, and clinical perspective. J Neuropsychiatry Clin Neurosci 9(3):315–330.  https://doi.org/10.1176/jnp.9.3.315 CrossRefGoogle Scholar
  22. Ocklenburg S, Güntürkün O (2018) Structural hemispheric asymmetries. Later Brain.  https://doi.org/10.1016/B978-0-12-803452-1.00009-6 Google Scholar
  23. Oishi K, Faria AV, van Zijl PCM, Mori S (2011) MRI atlas of human white matter. Academic PressGoogle Scholar
  24. Phan KL, Orlichenko A, Boyd E, Angstadt M, Coccaro EF, Liberzon I, Arfanakis K (2009) Preliminary evidence of white matter abnormality in the uncinate fasciculus in generalized social anxiety disorder. Biol Psychiatr 66(7):691–694.  https://doi.org/10.1016/j.biopsych.2009.02.028 CrossRefGoogle Scholar
  25. Pugliese L, Catani M, Ameis S, Dell’Acqua F, Thiebaut de Schotten M, Murphy C, Robertson D, Deeley Q, Daly E, Murphy DGM (2009) The anatomy of extended limbic pathways in Asperger syndrome: a preliminary diffusion tensor imaging tractography study. NeuroImage 47(2):427–434.  https://doi.org/10.1016/j.neuroimage.2009.05.014 CrossRefGoogle Scholar
  26. Randolph C (2002) Repeatable battery for the assessment of neuropsychological status. Pearson Assessment, London, UKGoogle Scholar
  27. Rilling JK, Glasser MF, Preuss TM, Ma X, Zhao T, Hu X, Behrens TEJ (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11(4):426–428.  https://doi.org/10.1038/nn2072 CrossRefGoogle Scholar
  28. Rodrigo S, Oppenheim C, Chassoux F, Golestani N, Cointepas Y, Poupon C, Seamh F, Mangin JF, Le Bihan D, Meder J-F (2007) Uncinate fasciculus fiber tracking in mesial temporal lobe epilepsy. Initial findings. Eur Radiol 17(7):1663–1668.  https://doi.org/10.1007/s00330-006-0558-x CrossRefGoogle Scholar
  29. Slater DA, Melie-Garcia L, Preisig M, Kherif F, Lutti A, Draganski B (2019) Evolution of white matter tract microstructure across the life span. Hum Brain Mapp.  https://doi.org/10.1002/hbm.24522 Google Scholar
  30. Thiebaut de Schotten M, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DGM, Catani M (2011a) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246.  https://doi.org/10.1038/nn.2905 CrossRefGoogle Scholar
  31. Thiebaut de Schotten M, Ffytche DH, Bizzi A, DellAcqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DGM, Catani M (2011b) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. NeuroImage 54(1):49–59.  https://doi.org/10.1016/J.NEUROIMAGE.2010.07.055 CrossRefGoogle Scholar
  32. Thiebaut de Schotten M, Dell’Acqua F, Valabregue R (2012) Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48(1):82–96.  https://doi.org/10.1016/J.CORTEX.2011.10.001 CrossRefGoogle Scholar
  33. Van Hecke W, Emsell L, Sunaert S (2016) Diffusion tensor imaging : a practical handbookGoogle Scholar
  34. Vingerhoets G, Gerrits R, Bogaert S (2018a) Atypical brain functional segregation is more frequent in situs inversus totalis. Cortex 106:12–25.  https://doi.org/10.1016/j.cortex.2018.04.012 CrossRefGoogle Scholar
  35. Vingerhoets G, Li X, Hou L, Bogaert S, Verhelst H, Gerrits R, Siugzdaite R, Roberts N (2018b) Brain structural and functional asymmetry in human situs inversus totalis. Brain Struct Funct 223(4):1937–1952.  https://doi.org/10.1007/s00429-017-1598-5 Google Scholar
  36. Von Der Heide RJ, Skipper LM, Klobusicky E, Olson IR (2013) Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. Brain 136(6):1692–1707.  https://doi.org/10.1093/brain/awt094 CrossRefGoogle Scholar
  37. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl P, Mori S (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. NeuroImage 36(3):630–644.  https://doi.org/10.1016/j.neuroimage.2007.02.049 CrossRefGoogle Scholar
  38. Wang R, Benner T, Sorensen AG, Wedeen VJ (2007) Diffusion toolkit: a software package for diffusion imaging data processing and tractography. Proc Intl Soc Mag Reson Med 15:3720Google Scholar
  39. Webb WG (2017) Organization of the nervous system I. Neurol the Speech Lang Pathol 10:13–43.  https://doi.org/10.1016/B978-0-323-10027-4.00002-6 CrossRefGoogle Scholar
  40. Yasmin H, Nakata Y, Aoki S, Abe O, Sato N, Nemoto K, Arima K, Furuta N, Uno M, Hirai S, Masutani Y, Ohtomo K (2008) Diffusion abnormalities of the uncinate fasciculus in Alzheimer’s disease: diffusion tensor tract-specific analysis using a new method to measure the core of the tract. Neuroradiology 50(4):293–299.  https://doi.org/10.1007/s00234-007-0353-7 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Experimental PsychologyGhent UniversityGhentBelgium
  2. 2.Ghent Institute for Functional and Metabolic Imaging (GIfMI), Ghent UniversityGhentBelgium
  3. 3.Department of RadiologyGhent University HospitalGhentBelgium

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