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Understanding the time variant connectivity of the language network in developmental dyslexia: new insights using Granger causality

  • Biological Child and Adolescent Psychiatry - Original Article
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Abstract

The reading process takes place in a neuronal network comprising the inferior frontal, posterior dorsal and posterior ventral brain areas. It is suggested that developmental dyslexia is caused by a disruption of the two posterior network areas. What remains debatable is whether these areas are affected in their functionality or whether the neuronal networking (connectivity) of these areas suffer from a disturbed information transfer. Thus, it is of major interest to investigate the time flow of the directed information transfer (time variant connectivity) within the neuronal reading network of dyslexic subjects. We investigated adolescents with dyslexia and normal-reading controls with functional magnetic resonance imaging and electroencephalography (EEG) with a paradigm addressing basic visual, orthographic and phonological processing. EEG data were analyzed with the time variant Granger causality index (tvGCI) to investigate the temporal order of the directed information transfer (time variant causal connectivity: which network node passes when information to which network node) during reading in dyslexic readers. Results show that the reading network of dyslexic readers comprises the same brain areas as identified in normal-reading subjects. The tvGCI analysis of the network profiles of dyslexic readers indicates that dyslexics show a difference in timing and localization of connectivity within this reading network compared to normal readers. Dyslexic readers use right hemisphere language areas to counterbalance posterior left hemisphere processing deficits. The compensatory involvement of homologue right hemisphere brain areas for the reading process may be the neurobiological background for the significantly longer reading times by dyslexics.

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References

  • American Electroencepahlographic Society (1994) Guideline thirteen: guidelines for standard electrode position nomenclature. J Clin Neurophysiol 11(1):111–113

    Article  Google Scholar 

  • Arnold M, Miltner WHR, Witte H, Bauer R, Braun C (1998) Adaptive AR modeling of nonstationary time series by means of Kalman filtering. IEEE Trans Biomed Eng 45:553–562

    Article  CAS  PubMed  Google Scholar 

  • Booth JR, Mehdirattaa N, Burmana DD, Bitan T (2008) Developmental increases in effective connectivity to brain regions involved in phonological processing during tasks with orthographic demands. Brain Res 189:78–89

    Article  CAS  Google Scholar 

  • Epelbaum S, Pinel P, Gaillard R, Delmaire C, Perrin M, Dupont S et al (2008) Pure alexia as a disconnection syndrome: new diffusion imaging evidence for an old concept. Cortex 44(8):962–974

    Article  PubMed  Google Scholar 

  • Fiez JA, Tranel D, Seager-Frerichs D, Damasio H (2006) Specific reading and phonological processing deficits are associated with damage to the left frontal operculum. Cortex 42(4):624–643

    Article  PubMed  Google Scholar 

  • Granger CWJ (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37(3):424–438

    Article  Google Scholar 

  • Gratton G, Coles MGH, Donchin E (1983) A new method for off-line removal of ocular artefact. Electroencephalogr Clin Neurophysiol 55:468–484

    Article  CAS  PubMed  Google Scholar 

  • Grissemann H (2000) Zürcher Lesetest (ZLT). Hans Huber, Göttingen

    Google Scholar 

  • Grünling C, Ligges M, Huonker R, Klingert M, Mentzel HJ, Rzanny R et al (2004) Dyslexia: the possible benefit of multimodal integration of fMRI- and EEG-data. J Neural Transm 111(7):951–969

    Article  PubMed  Google Scholar 

  • Hampson M, Tokoglu F, Sun ZD, Schafer RJ, Skudlarski P, Gore JC et al (2006) Connectivity-behavior analysis reveals that functional connectivity between left BA39 and Broca’s area varies with reading ability. Neuroimage 31(2):513–519

    Article  PubMed  Google Scholar 

  • Hemmelmann D, Ungureanu M, Hesse W, Wüstenberg T, Reichenbach JR, Witte OW et al (2009) Modelling and analysis of time-variant directed interrelations between brain regions based on BOLD-signals. Neuroimage 45(3):722–737

    Article  CAS  PubMed  Google Scholar 

  • Hesse W, Möller E, Arnold M, Schack B (2003) The use of time-variant EEG Granger causality for inspecting directed interdependencies of neural assemblies. J Neurosci Methods 124(1):27–44

    Article  PubMed  Google Scholar 

  • Jäger A (1974) Rechtschreibtest R–T. Hogrefe, Göttingen

    Google Scholar 

  • Jobard G, Crivello F, Tzourio-Mazoyer N (2003) Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. Neuroimage 20(2):693–712

    Article  CAS  PubMed  Google Scholar 

  • Katzir T, Misra M, Poldrack RA (2005) Imaging phonology without print: assessing the neural correlates of phonemic awareness using fMRI. Neuroimage 27(1):106–115

    Article  PubMed  Google Scholar 

  • Klicpera C, Klicpera BG (1998) Psychologie der Lese- und Schreibschwierigkeiten. Psychologie Verlags Union, Weinheim

    Google Scholar 

  • Kronbichler M, Hutzler F, Staffen W, Mair A, Ladurner G, Wimmer H (2006) Evidence for a dysfunction of left posterior reading areas in German dyslexic readers. Neuropsychologia 44(10):1822–1832

    Article  PubMed  Google Scholar 

  • Kujala J, Pammer K, Cornelissen P, Roebroeck A, Formisano E, Salmelin R (2007) Phase coupling in a cerebro-cerebellar network at 8–13 Hz during reading. Cereb Cortex 17(6):1476–1485

    Article  PubMed  Google Scholar 

  • Leistritz L, Hesse W, Wustenberg T, Fitzek C, Reichenbach JR, Witte H (2006) Time-variant analysis of fast-fMRI and dynamic contrast agent MRI sequences as examples of 4-dimensional image analysis. Methods Inf Med 45(6):643–650

    CAS  PubMed  Google Scholar 

  • Ligges M (2002) fMRI-Untersuchung von Sprachverarbeitungsprozessen bei der Lese-Rechtschreibstörung. Thesis, Friedrich-Schiller-Universität, Jena

  • Ligges C, Blanz B (2007) Survey of fMRI results regarding a phonological deficit in children and adults with dyslexia: fundamental deficit or indication of compensation? Z Kind Jugendpsych Psychother 35(2):107–117

    Article  Google Scholar 

  • Maisog JM, Einbinder ER, Flowers DL, Turkeltaub PE, Eden GF (2006) A metes-analysis of functional neuroimaging studies of dyslexia. Paper presented at the 25th Rodin remediation conference, 11–13 Oct 2006, Washington, DC

  • Paulesu E, Frith U, Snowling M, Gallagher A, Morton J, Frackowiak RSJ et al (1996) Is developmental dyslexia a disconnection syndrome? Evidence from PET scanning. Brain 119:143–157

    Article  PubMed  Google Scholar 

  • Pugh KR, Mencl WE, Jenner AR, Katz L, Frost SJ, Lee JR et al (2000) Functional neuroimaging studies of reading and reading disability (developmental dyslexia). Ment Retard Dev Disabil Res Rev 6(3):207–213

    Article  CAS  PubMed  Google Scholar 

  • Quaglino V, Bourdin B, Czternasty G, Vrignaud P, Fall S, Meyer ME et al (2008) Differences in effective connectivity between dyslexic children and normal readers during a pseudoword reading task: an fMRl study. Clin Neurophysiol 38(2):73–82

    Article  CAS  Google Scholar 

  • Ramus F (2003) Developmental dyslexia: specific phonological deficit or general sensorimotor dysfunction? Curr Opin Neurobiol 13(2):212–218

    Article  CAS  PubMed  Google Scholar 

  • Rathenow P (1980) Westermann Rechtschreibtest 6+. Braunschweig

  • Raven J (1996) Matrizen-test-manual band 1. Beltz-Test GmbH, Göttingen

    Google Scholar 

  • Richards TL, Berninger VW (2008) Abnormal fMRI connectivity in children with dyslexia during a phoneme task: before but not after treatment. J Neuroling 21(4):294–304

    Article  Google Scholar 

  • Saur D, Kreher BW, Schnell S, Kummerer D, Kellmeyer P, Vry MS et al (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci USA 105(46):18035–18040

    Article  CAS  PubMed  Google Scholar 

  • Shaywitz BA, Skudlarski P, Holahan JM, Marchione KE, Constable RT, Fulbright RK et al (2007) Age-related changes in reading systems of dyslexic children. Ann Neurol 61(4):363–370

    Article  PubMed  Google Scholar 

  • Vigneau M, Beaucousin V, Herve PY, Duffau H, Crivello F, Houde O et al (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30(4):1414–1432

    Article  CAS  PubMed  Google Scholar 

  • Weiss T, Hesse W, Ungureanu M, Hecht H, Leistritz L, Witte H et al (2008) How do brain areas communicate during the processing of noxious stimuli? An analysis of laser-evoked event-related potentials using the Granger causality index. J Neurophysiol 99(5):2220–2231

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was supported by grants from the Deutsche Forschungsgemeinschaft (DFG BL 435/3-2 and Wi 1166/10-1) and by a Marie-Curie-Intra-European Fellowship (M.U., 041 452, NADIBA).

Conflict of interest statement

The authors declare that they have no conflict of interest with the funding institution.

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Authors and Affiliations

  1. Department of Child and Adolescent Psychiatry, Friedrich Schiller University, Philosophenweg 3-5, 07743, Jena, Germany

    Carolin Ligges, M. Ligges & B. Blanz

  2. Institute of Medical Statistics, Computer Sciences and Documentation, Friedrich Schiller University, Bachstr. 18, 07743, Jena, Germany

    M. Ungureanu & H. Witte

Authors
  1. Carolin Ligges
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  2. M. Ungureanu
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  3. M. Ligges
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  4. B. Blanz
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  5. H. Witte
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Corresponding author

Correspondence to Carolin Ligges.

Additional information

C. Ligges and M. Ungureanu contributed equally to the publication and therefore both are considered as first authors.

Carolin Ligges: Birth name Grünling.

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Ligges, C., Ungureanu, M., Ligges, M. et al. Understanding the time variant connectivity of the language network in developmental dyslexia: new insights using Granger causality. J Neural Transm 117, 529–543 (2010). https://doi.org/10.1007/s00702-010-0367-x

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  • DOI: https://doi.org/10.1007/s00702-010-0367-x

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