DİSLEKSİ VE DİSGRAFİ OLAN ÇOCUKLARIN OKUMA SIRASINDA BEYİN AKTİVİTELERİNİN FONKSİYONEL MR PSİKOFİZYOLOJİK ETKİLEŞİM ANALİZİ İLE İNCELENMESİ

Yıl 2023, Cilt: 11 Sayı: 4, 1310 - 1327, 30.12.2023

Gizem Rüveyda Sağır , Semra İçer

https://doi.org/10.21923/jesd.1222428

Cited By: 1

Öz

Okuma ve yazma güçlükleri dünyada oldukça yaygın olan nörogelişimsel bozukluklardır. Okuma ve yazma güçlüğü olarak bilinen gelişimsel disleksi ve yazma güçlüğü olarak bilinen gelişimsel disgrafinin birlikte değerlendirildiği çalışma sayısı oldukça azdır. Bu çalışma, literatürdeki kısıtlı çalışmalara katkıda bulunmak amacıyla yapılmıştır. OpenfMRI’dan alınan veri setinde Almanca konuşan çocuklardan disleksi 20, disgrafi 16 ve kontrol grubundan 22 katılımcı bulunmaktadır. fMRI görevi, normal kelime ve sözde eş sesli kelimeleri sesli bir şekilde okumadır. Görevler sırasında tüm beyinde oluşan fonksiyonel aktivasyon analizi sonucunda, disgrafi grubu disleksi ve kontrol grubuna göre okuma ile ilgili olan bölgelerde hipoaktivasyon göstermiştir. Ek olarak disleksi grubunda ventral oksipitotemporal bölgede hipoaktivasyon gözlenmememiştir. Bununla birlikte fusiform girus, inferior frontal girus, precuneus ve precentral girus bölgeleri tohum olarak seçilip, ilgili tohum bölgesinin görevler sırasında fonksiyonel bağlantısını araştırmak amacıyla, psikofizyolojik etkileşim analizi yapılmıştır. Fonksiyonel bağlantı analizi sonucunda, disleksi grubunda diğer gruplara göre bağlantısallık yollarında bozulmalar gözlenmiştir. Disgrafi grubu ise kontrol grubu ile benzer bağlantı yolları göstermiştir.

Anahtar Kelimeler

Gelişimsel Disleksi, Gelişimsel Disgrafi, Görev Tabanlı fMRI, GLM Analizi, PPI Analizi

EXAMINATION OF THE BRAIN ACTIVITIES OF CHILDREN WITH DYSLEXIA AND DYSGRAPHIA DURING READING BY FUNCTIONAL MR PSYCHOPHYSIOLOGICAL INTERACTION ANALYSIS

Öz

Reading and writing difficulties are neurodevelopmental disorders that are very common in the world. There are very few studies evaluating developmental dyslexia, known as reading and writing difficulties, and developmental dysgraphia, known as writing difficulties, together. This study was conducted to contribute to the limited studies in the literature. The data set from OpenfMRI includes 20 German-speaking children with dyslexia, 16 dysgraphia and 22 participants from the control group. The fMRI task is to read aloud normal words and pseudohomophones. As a result of the functional activation analysis in the whole brain during the tasks, the dysgraphia group showed hypoactivation in the regions related to reading compared to the dyslexia and control groups. In addition, no hypoactivation was observed in the ventral occipitotemporal region in the dyslexia group. In addition, fusiform gyrus, inferior frontal gyrus, precuneus and precentral gyrus regions were selected as seeds, and psychophysiological interaction analysis was performed to investigate the functional connection of the relevant seed region during tasks. As a result of functional connectivity analysis, impairments in connectivity pathways were observed in the dyslexia group compared to the other groups. The dysgraphia group, on the other hand, showed similar pathways to the control group.

Anahtar Kelimeler

Developmental Dyslexia, Developmental Dysgraphia, Task Based fMRI, GLM Analysis, PPI Analysis

Kaynakça

• Bamiou, D.-E., Musiek, F. E., & Luxon, L. M., 2003. The insula (Island of Reil) and its role in auditory processing: Literature review. Brain Research Reviews, 42(2), 143-154.
• Banfi, C., Koschutnig, K., Moll, K., Schulte-Körne, G., Fink, A., & Landerl, K.,2019. White matter alterations and tract lateralization in children with dyslexia and isolated spelling deficits. Human Brain Mapping, 40(3), 765-776.
• Banfi, C., Koschutnig, K., Moll, K., Schulte-Körne, G., Fink, A., & Landerl, K.,2021. Reading-related functional activity in children with isolated spelling deficits and dyslexia. Language, Cognition and Neuroscience, 36(5), 543-561.
• Beckmann, C. F., Jenkinson, M., & Smith, S. M.,2003. General multilevel linear modeling for group analysis in FMRI. NeuroImage, 20(2), 1052-1063.
• Berninger, V. W., Richards, T. L., & Abbott, R. D.,2015. Differential diagnosis of dysgraphia, dyslexia, and OWL LD: Behavioral and neuroimaging evidence. Reading and Writing, 28(8), 1119-1153.
• Borghesani, V., Wang, C., Watson, C., Bouhali, F., Caverzasi, E., Battistella, G., Bogley, R., Yabut, N. A., Deleon, J., Miller, Z. A., Hoeft, F., Mandelli, M. L., & Gorno-Tempini, M. L.,2021. Functional and morphological correlates of developmental dyslexia: A multimodal investigation of the ventral occipitotemporal cortex. Journal of Neuroimaging, 31(5), 962-972.
• Brem, S., Maurer, U., Kronbichler, M., Schurz, M., Richlan, F., Blau, V., Reithler, J., van der Mark, S., Schulz, E., Bucher, K., Moll, K., Landerl, K., Martin, E., Goebel, R., Schulte-Körne, G., Blomert, L., Wimmer, H., & Brandeis, D.,2020. Visual word form processing deficits driven by severity of reading impairments in children with developmental dyslexia. Scientific Reports, 10(1), Art. 1.
• Buchweitz, A., Mason, R. A., Meschyan, G., Keller, T. A., & Just, M. A.,2014. Modulation of cortical activity during comprehension of familiar and unfamiliar text topics in speed reading and speed listening. Brain and Language, 139, 49-57.
• Cao, F., Yan, X., Spray, G. J., Liu, Y., & Deng, Y.,2018. Brain Mechanisms Underlying Visuo-Orthographic Deficits in Children With Developmental Dyslexia. Frontiers in Human Neuroscience, 12.
• Cao, F., Yan, X., Wang, Z., Liu, Y., Wang, J., Spray, G. J., & Deng, Y.,2017. Neural signatures of phonological deficits in Chinese developmental dyslexia. NeuroImage, 146, 301-311.
• Chung, P. J., Patel, D. R., & Nizami, I.,2020. Disorder of written expression and dysgraphia: Definition, diagnosis, and management. Translational Pediatrics, 9(Suppl 1), S46-S54.
• Cohen, L., Dehaene, S., Naccache, L., Lehericy, S., Henaff, M.-A., & Michel, F. (t.y.). The visual word form area. 17.
• Crottaz-Herbette, S., Anagnoson, R. T., & Menon, V.,2004. Modality effects in verbal working memory: Differential prefrontal and parietal responses to auditory and visual stimuli. NeuroImage, 21(1), 340-351.
• Dębska, A., Banfi, C., Chyl, K., Dzięgiel-Fivet, G., Kacprzak, A., Łuniewska, M., Plewko, J., Grabowska, A., Landerl, K., & Jednoróg, K., 2021. Neural patterns of word processing differ in children with dyslexia and isolated spelling deficit. Brain Structure and Function, 226(5), 1467-1478.
• Dębska, A., Chyl, K., Dzięgiel, G., Kacprzak, A., Łuniewska, M., Plewko, J., Marchewka, A., Grabowska, A., & Jednoróg, K., 2019. Reading and spelling skills are differentially related to phonological processing: Behavioral and fMRI study. Developmental Cognitive Neuroscience, 39, 100683.
• Döhla, D., & Heim, S., 2016. Developmental Dyslexia and Dysgraphia: What can We Learn from the One About the Other? Frontiers in Psychology, 6.
• Döhla, D., Willmes, K., & Heim, S., 2018. Cognitive Profiles of Developmental Dysgraphia. Frontiers in Psychology, 9.
• Eden, G. F., VanMeter, J. W., Rumsey, J. M., & Zeffiro, T. A.,1996. The Visual Deficit Theory of Developmental Dyslexia. NeuroImage, 4(3), S108-S117.
• Finn, E. S., Shen, X., Holahan, J. M., Scheinost, D., Lacadie, C., Papademetris, X., Shaywitz, S. E., Shaywitz, B. A., & Constable, R. T., 2014. Disruption of Functional Networks in Dyslexia: A Whole-Brain, Data-Driven Analysis of Connectivity. Biological Psychiatry, 76(5), 397-404.
• Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J., 1997. Psychophysiological and Modulatory Interactions in Neuroimaging. NeuroImage, 6(3), 218-229.
• Gebauer, D., Enzinger, C., Kronbichler, M., Schurz, M., Reishofer, G., Koschutnig, K., Kargl, R., Purgstaller, C., Fazekas, F., & Fink, A., 2012. Distinct patterns of brain function in children with isolated spelling impairment: New insights. Neuropsychologia, 50(7), 1353-1361.
• Gosse, C., Dricot, L., & Van Reybroeck, M. 2022. Evidence of graphomotor dysfunction in children with dyslexia: A combined behavioural and fMRI experiment. Cortex, 148, 68–88.
• Heim, S., Wehnelt, A., Grande, M., Huber, W., & Amunts, K., 2013. Effects of lexicality and word frequency on brain activation in dyslexic readers. Brain and Language, 125(2), 194-202.
• Jenkinson, M., Bannister, P., Brady, M., & Smith, S., 2002. Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images. NeuroImage, 17(2), 825-841.
• Jenkinson, M., & Smith, S., 2001. A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2), 143-156.
• Kovelman, I., Norton, E. S., Christodoulou, J. A., Gaab, N., Lieberman, D. A., Triantafyllou, C., Wolf, M., Whitfield-Gabrieli, S., & Gabrieli, J. D. E., 2012. Brain Basis of Phonological Awareness for Spoken Language in Children and Its Disruption in Dyslexia. Cerebral Cortex, 22(4), 754-764. https://doi.org/10.1093/cercor/bhr094
• Kronbichler, L., & Kronbichler, M., 2018. The Importance of the Left Occipitotemporal Cortex in Developmental Dyslexia. Current Developmental Disorders Reports, 5(1), 1-8.
• Kuhl, U., Neef, N. E., Kraft, I., Schaadt, G., Dörr, L., Brauer, J., Czepezauer, I., Müller, B., Wilcke, A., Kirsten, H., Emmrich, F., Boltze, J., Friederici, A. D., & Skeide, M. A., 2020. The emergence of dyslexia in the developing brain. NeuroImage, 211, 116633.
• Lachmann, T., Berti, S., Kujala, T., & Schröger, E., 2005. Diagnostic subgroups of developmental dyslexia have different deficits in neural processing of tones and phonemes. International Journal of Psychophysiology, 56(2), 105-120.
• Li, Y., & Bi, H.-Y. 2022. Comparative research on neural dysfunction in children with dyslexia under different writing systems: A meta-analysis study. Neuroscience & Biobehavioral Reviews, 137.
• Li, Y., Li, J., Yang, Y., & Bi, H.-Y. 2022. Disruption of dynamic functional connectivity in children with developmental dyslexia. Language, Cognition and Neuroscience, 38(5), 621–635.
• Ludersdorfer, P., Wimmer, H., Richlan, F., Schurz, M., Hutzler, F., & Kronbichler, M., 2016. Left ventral occipitotemporal activation during orthographic and semantic processing of auditory words. NeuroImage, 124, 834-842.
• Lyon, G. R., Shaywitz, S. E., & Shaywitz, B. A. (2003). A definition of dyslexia. Annals of Dyslexia, 53(1), 1-14.
• Martin, A., Kronbichler, M., & Richlan, F. (2016). Dyslexic brain activation abnormalities in deep and shallow orthographies: A meta-analysis of 28 functional neuroimaging studies. Human Brain Mapping, 37(7), 2676-2699.
• McLaren, D. G., Ries, M. L., Xu, G., & Johnson, S. C., 2012. A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches. NeuroImage, 61(4), 1277-1286.
• Moll, K., & Landerl, K., 2009. Double Dissociation Between Reading and Spelling Deficits. Scientific Studies of Reading, 13(5), 359-382.
• Nicolson, R. I., Fawcett, A. J., & Dean, P., 2001. Developmental dyslexia: The cerebellar deficit hypothesis. Trends in Neurosciences, 24(9), 508-511.
• Niendam, T. A., Laird, A. R., Ray, K. L., Dean, Y. M., Glahn, D. C., & Carter, C. S., 2012. Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cognitive, Affective, & Behavioral Neuroscience, 12(2), 241-268.
• Olulade, O. A., Flowers, D. L., Napoliello, E. M., & Eden, G. F., 2013. Developmental differences for word processing in the ventral stream. Brain and Language, 125(2), 134-145.
• Olulade, O. A., Flowers, D. L., Napoliello, E. M., & Eden, G. F., 2015. Dyslexic children lack word selectivity gradients in occipito-temporal and inferior frontal cortex. NeuroImage: Clinical, 7, 742-754.
• Paulesu, E., Danelli, L., & Berlingeri, M., 2014. Reading the dyslexic brain: Multiple dysfunctional routes revealed by a new meta-analysis of PET and fMRI activation studies. Frontiers in Human Neuroscience, 8.
• PII: S0166-2236(00)01896-8 | Elsevier Enhanced Reader. (t.y.). https://doi.org/10.1016/S0166-2236(00)01896-8
• Pugh, K. R., Mencl, W. E., Jenner, A. R., Katz, L., Frost, S. J., Lee, J. R., Shaywitz, S. E., & Shaywitz, B. A., 2000. Functional neuroimaging studies of reading and reading disability (developmental dyslexia). Mental Retardation and Developmental Disabilities Research Reviews, 6(3), 207-213.
• Purcell, J. J., Jiang, X., & Eden, G. F., 2017. Shared orthographic neuronal representations for spelling and reading. NeuroImage, 147, 554-567.
• Purcell, J. J., Napoliello, E. M., & Eden, G. F., 2011. A combined fMRI study of typed spelling and reading. NeuroImage, 55(2), 750-762.
• Ramus, F., 2003. Theories of developmental dyslexia: Insights from a multiple case study of dyslexic adults. Brain, 126(4), 841-865.
• Ramus, F., 2004. Neurobiology of dyslexia: A reinterpretation of the data. Trends in Neurosciences, 27(12), 720-726.
• Richards, T. L., Berninger, V. W., & Fayol, M., 2009. FMRI activation differences between 11-year-old good and poor spellers’ access in working memory to temporary and long-term orthographic representations. Journal of Neurolinguistics, 22(4), 327-353.
• Richards, T. L., Grabowski, T. J., Boord, P., Yagle, K., Askren, M., Mestre, Z., Robinson, P., Welker, O., Gulliford, D., Nagy, W., & Berninger, V., 2015. Contrasting brain patterns of writing-related DTI parameters, fMRI connectivity, and DTI–fMRI connectivity correlations in children with and without dysgraphia or dyslexia. NeuroImage: Clinical, 8, 408-421.
• Richlan, F., 2020. The Functional Neuroanatomy of Developmental Dyslexia Across Languages and Writing Systems. Frontiers in Psychology, 11.
• Richlan, F., Kronbichler, M., & Wimmer, H., 2009. Functional abnormalities in the dyslexic brain: A quantitative meta-analysis of neuroimaging studies. Human Brain Mapping, 30(10), 3299-3308.
• Richlan, F., Kronbichler, M., & Wimmer, H., 2011. Meta-analyzing brain dysfunctions in dyslexic children and adults. NeuroImage, 56(3), 1735-1742.
• Richlan, F., Sturm, D., Schurz, M., Kronbichler, M., Ladurner, G., & Wimmer, H., 2010. A Common Left Occipito-Temporal Dysfunction in Developmental Dyslexia and Acquired Letter-By-Letter Reading? PLOS ONE, 5(8), e12073.
• Salience Network–Based Classification and Prediction of Symptom Severity in Children With Autism | Autism Spectrum Disorders | JAMA Psychiatry | JAMA Network. (t.y.).
• Sağir, G. R., & İçer, S. 2022, October. Investigation of Brain Activities During Reading of Children with Dyslexia and Dysgraphia by using Region of Interest Analysis. In 2022 Medical Technologies Congress (TIPTEKNO) (pp. 1-4). IEEE.
• Schurz, M., Wimmer, H., Richlan, F., Ludersdorfer, P., Klackl, J., & Kronbichler, M., 2015. Resting-State and Task-Based Functional Brain Connectivity in Developmental Dyslexia. Cerebral Cortex, 25(10), 3502-3514.
• Share, D. L., 1995. Phonological recoding and self-teaching: Sine qua non of reading acquisition. Cognition, 55(2), 151-218.
• Shaywitz, B. A., Skudlarski, P., Holahan, J. M., Marchione, K. E., Constable, R. T., Fulbright, R. K., Zelterman, D., Lacadie, C., & Shaywitz, S. E., 2007. Age-related changes in reading systems of dyslexic children. Annals of Neurology, 61(4), 363-370.
• Shaywitz, S. E., & Shaywitz, B. A., 2005. Dyslexia (Specific Reading Disability). Biological Psychiatry, 57(11), 1301-1309.
• Shaywitz, S. E., & Shaywitz, B. A., 2008. Paying attention to reading: The neurobiology of reading and dyslexia. Development and Psychopathology, 20(4), 1329-1349
• Smith, S. M., 2002. Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143-155.
• Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-Berg, H., Bannister, P. R., De Luca, M., Drobnjak, I., Flitney, D. E., Niazy, R. K., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J. M., & Matthews, P. M., 2004. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23, S208-S219.
• Sporns, O., 2013. The human connectome: Origins and challenges. NeuroImage, 80, 53-61.
• Stein, J., & Walsh, V., 1997. To see but not to read; the magnocellular theory of dyslexia. Trends in Neurosciences, 20(4), 147-152.
• Tallal, P., 1980. Auditory temporal perception, phonics, and reading disabilities in children. Brain and Language, 9(2), 182-198.
• Taran, N., Farah, R., DiFrancesco, M., Altaye, M., Vannest, J., Holland, S., Rosch, K., Schlaggar, B. L., & Horowitz-Kraus, T., 2022. The role of visual attention in dyslexia: Behavioral and neurobiological evidence. Human Brain Mapping, 43(5), 1720-1737.
• Taylor, J. S. H., Rastle, K., & Davis, M. H., 2013. Can cognitive models explain brain activation during word and pseudoword reading? A meta-analysis of 36 neuroimaging studies. Psychological Bulletin, 139, 766-791.
• Twait, E., Farah, R., & Horowitz-Kraus, T., 2018. Decreased functional connectivity of the salience network during narrative comprehension in children with reading difficulties: An fMRI study. NeuroImage: Clinical, 20, 987-992.
• U, F.,1980. Unexpected spelling problems. Cognitive Processes in Spelling, 495-515.
• Van der Mark, S., Klaver, P., Bucher, K., Maurer, U., Schulz, E., Brem, S., Martin, E., & Brandeis, D., 2011. The left occipitotemporal system in reading: Disruption of focal fMRI connectivity to left inferior frontal and inferior parietal language areas in children with dyslexia. NeuroImage, 54(3), 2426-2436.
• Vellutino, F. R., Fletcher, J. M., Snowling, M. J., & Scanlon, D. M., 2004. Specific reading disability (dyslexia): What have we learned in the past four decades? Journal of Child Psychology and Psychiatry, 45(1), 2-40.
• Waldie, K. E., & Mosley, J. L., 2000. Hemispheric Specialization for Reading. Brain and Language, 75(1), 108-122.
• Wang, Z., Yan, X., Liu, Y., Spray, G. J., Deng, Y., & Cao, F., 2019. Structural and functional abnormality of the putamen in children with developmental dyslexia. Neuropsychologia, 130, 26-37.
• Wimmer, H., Schurz, M., Sturm, D., Richlan, F., Klackl, J., Kronbichler, M., & Ladurner, G., 2010. A dual-route perspective on poor reading in a regular orthography: An fMRI study. Cortex, 46(10), 1284-1298.
• Woolrich, M. W., Behrens, T. E. J., Beckmann, C. F., Jenkinson, M., & Smith, S. M., 2004. Multilevel linear modelling for FMRI group analysis using Bayesian inference. NeuroImage, 21(4), 1732-1747.
• Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M., 2001. Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data. NeuroImage, 14(6), 1370-1386.
• Worsley, K. J., 2001. Statistical analysis of activation images, Functional MRI: An introduction to methods, 14 (1), 251-70.
• Xu, B., Grafman, J., Gaillard, W. D., Ishii, K., Vega-Bermudez, F., Pietrini, P., Reeves-Tyer, P., DiCamillo, P., & Theodore, W., 2001. Conjoint and Extended Neural Networks for the Computation of Speech Codes: The Neural Basis of Selective Impairment in Reading Words and Pseudowords. Cerebral Cortex, 11(3), 267-277.
• Yagle, K., Richards, T., Askren, K., Mestre, Z., Beers, S., Abbott, R., Nagy, W., Boord, P., & Berninger, V., 2017. Relationships between Eye Movements during Sentence Reading Comprehension, Word Spelling and Reading, and DTI and fmri Connectivity In Students with and without Dysgraphia or Dyslexia. Journal of systems and integrative neuroscience, 3(1), 10.15761/JSIN.1000150.
• Yu, X., Ferradal, S., Dunstan, J., Carruthers, C., Sanfilippo, J., Zuk, J., Zöllei, L., Gagoski, B., Ou, Y., Grant, P. E., & Gaab, N. 2022. Atypical functional connectivity of the left fusiform gyrus in infants at familial risk for developmental dyslexia. MedRxiv
• Zoubrinetzky, R., Bielle, F., & Valdois, S., 2014. New Insights on Developmental Dyslexia Subtypes: Heterogeneity of Mixed Reading Profiles. PLOS ONE, 9(6), e99337.