Abstract
Previous neuroimaging studies have found atypical cerebellar activation in individuals with dyslexia in either motor-related tasks or language tasks. However, studies investigating atypical cerebellar activation in individuals with dyslexia have mostly used tasks tapping phonological processing. A question that is yet unanswered is whether the cerebellum in individuals with dyslexia functions properly during orthographic processing of words, as growing evidence shows that the cerebellum is also involved in visual and spatial processing. Here, we investigated cerebellar activation and cerebro-cerebellar functional connectivity during word processing in dyslexic readers and typically developing readers using tasks that tap orthographic and phonological codes. In children with dyslexia, we observed an abnormally higher engagement of the bilateral cerebellum for the orthographic task, which was negatively correlated with literacy measures. The greater the reading impairment was for young dyslexic readers, the stronger the cerebellar activation was. This suggests a compensatory role of the cerebellum in reading for children with dyslexia. In addition, a tendency for higher cerebellar activation in dyslexic readers was found in the phonological task. Moreover, the functional connectivity was stronger for dyslexic readers relative to typically developing readers between the lobule VI of the right cerebellum and the left fusiform gyrus during the orthographic task and between the lobule VI of the left cerebellum and the left supramarginal gyrus during the phonological task. This pattern of results suggests that the cerebellum compensates for reading impairment through the connections with specific brain regions responsible for the ongoing reading task. These findings enhance our understanding of the cerebellum’s involvement in reading and reading impairment.
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References
Lyon GR, Shaywitz SE, Shaywitz BA. A definition of dyslexia. Annals of dyslexia. 2003;53(1):1–14.
Simos PG, Breier JI, Fletcher JM, Foorman BR, Bergman E, Fishbeck K, et al. Brain activation profiles in dyslexic children during non-word reading: a magnetic source imaging study. Neurosci Lett. 2000;290(1):61–5.
Shaywitz BA, Shaywitz SE, Pugh KR, Mencl WE, Fulbright RK, Skudlarski P, et al. Disruption of posterior brain systems for reading in children with developmental dyslexia. Biol Psychiat. 2002;52(2):101–10.
Richlan F, Kronbichler M, Wimmer H. Functional abnormalities in the dyslexic brain: a quantitative meta-analysis of neuroimaging studies. Hum Brain Mapp. 2009;30(10):3299–308.
Raschle NM, Zuk J, Gaab N. Functional characteristics of developmental dyslexia in left-hemispheric posterior brain regions predate reading onset. P Natl Acad Sci USA. 2012;109(6):2156–61.
Cohen L, Jobert A, Le Bihan D, Dehaene S. Distinct unimodal and multimodal regions for word processing in the left temporal cortex. NeuroImage. 2004;23(4):1256–70.
Schlaggar BL, McCandliss BD. Development of neural systems for reading. Annu Rev Neurosci. 2007;30:475–503.
Vicari S, Marotta L, Menghini D, Molinari M, Petrosini L. Implicit learning deficit in children with developmental dyslexia. Neuropsychologia. 2003;41(1):108–14.
Kronbichler M, Wimmer H, Staffen W, Hutzler F, Mair A, Ladurner G. Developmental dyslexia: gray matter abnormalities in the occipitotemporal cortex. Hum Brain Mapp. 2008;29(5):613–25.
Baillieux H, Vandervliet EJM, Manto M, Parizel PM, De Deyn PP, Marien P. Developmental dyslexia and widespread activation across the cerebellar hemispheres. Brain Lang. 2009;108(2):122–32.
Norton ES, Black JM, Stanley LM, Tanaka H, Gabrieli JDE, Sawyer C, et al. Functional neuroanatomical evidence for the double-deficit hypothesis of developmental dyslexia. Neuropsychologia. 2014;61:235–46.
Eckert MA, Leonard CM, Richards TL, Aylward EH, Thomson J, Berninger VW. Anatomical correlates of dyslexia: frontal and cerebellar findings. Brain. 2003;126:482–94.
Eckert M. Neuroanatomical markers for dyslexia: a review of dyslexia structural imaging studies. Neuroscientist. 2004;10(4):362–71.
Fernandez VG, Stuebing K, Juranek J, Fletcher JM. Volumetric analysis of regional variability in the cerebellum of children with dyslexia. Cerebellum. 2013;12(6):906–15.
Yang YH, Yang Y, Chen BG, Zhang YW, Bi HY. Anomalous cerebellar anatomy in Chinese children with dyslexia. Front Psychol. 2016;7:324.
Leonard CM, Eckert MA, Lombardino LJ, Oakland T, Kranzler J, Mohr CM, et al. Anatomical risk factors for phonological dyslexia. Cereb Cortex. 2001;11(2):148–57.
Rae C, Harasty JA, Dzendrowskyj TE, Talcott JB, Simpson JM, Blamire AM, et al. Cerebellar morphology in developmental dyslexia. Neuropsychologia. 2002;40(8):1285–92.
Linkersdorfer J, Lonnemann J, Lindberg S, Hasselhorn M, Fiebach CJ. Grey matter alterations co-localize with functional abnormalities in developmental dyslexia: an ALE meta-analysis. PLoS One. 2012;7(8):e43122.
Stoodley CJ. Distinct regions of the cerebellum show gray matter decreases in autism, ADHD, and developmental dyslexia. Front Syst Neurosci. 2014;8.
Pernet CR, Poline JB, Demonet JF, Rousselet GA. Brain classification reveals the right cerebellum as the best biomarker of dyslexia. BMC Neurosci. 2009;10.
Yang Y, Bi H-Y, Long Z-Y, Tao S. Evidence for cerebellar dysfunction in Chinese children with developmental dyslexia: an fMRI study. Int J Neurosci. 2013;123(5):300–10.
Berry EL, Jenkins IH, Nicolson RI, Fawcett AJ, Dean P, Brooks DJ. Cerebellar function is impaired in dyslexia: a PET activation study. Neurology. 1998;50(4):A3–A.
Nicolson RI, Fawcett AJ, Berry EL, Jenkins IH, Dean P, Brooks DJ. Association of abnormal cerebellar activation with motor learning difficulties in dyslexic adults. Lancet. 1999;353(9165):1662–7.
Fawcett AJ, Nicolson RI. Persistent deficits in motor skill of children with dyslexia. J Motor Behav. 1995;27(3):235–40.
Nicolson RI, Fawcett AJ. Comparison of deficits in cognitive and motor skills among children with dyslexia. Annals of Dyslexia. 1994;44(1):147–64.
Yang Y, Hong-Yan B. Unilateral implicit motor learning deficit in developmental dyslexia. Int J Psychol. 2011;46(1):1–8.
Barth AE, Denton CA, Stuebing KK, Fletcher JM, Cirino PT, Francis DJ, et al. A test of the cerebellar hypothesis of dyslexia in adequate and inadequate responders to reading intervention. J Int Neuropsych Soc. 2010;16(3):526–36.
Irannejad S, Savage R. Is a cerebellar deficit the underlying cause of reading disabilities? Annals of Dyslexia. 2011;62(1):22–52.
Beaton A, Marien P. Language, cognition and the cerebellum: grappling with an enigma. Cortex. 2010;46(7):811–20.
Murdoch BE. The cerebellum and language: historical perspective and review. Cortex. 2010;46(7):858–68.
Booth JR, Bebko G, Burman DD, Bitan T. Children with reading disorder show modality independent brain abnormalities during semantic tasks. Neuropsychologia. 2007;45(4):775–83.
Stanberry LI, Richards TL, Berninger VW, Nandy RR, Aylward EH, Maravilla KR, et al. Low-frequency signal changes reflect differences in functional connectivity between good readers and dyslexics during continuous phoneme mapping. Magn Reson Imaging. 2006;24(3):217–29.
Davis CJ. The spatial coding model of visual word identification. Psychol Rev. 2010;117(3):713.
Szwed M, Cohen L, Qiao E, Dehaene S. The role of invariant line junctions in object and visual word recognition. Vis Res. 2009;49(7):718–25.
Fink GR, Marshall JC, Shah NJ, Weiss PH, Halligan PW, Grosse-Ruyken M, et al. Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI. Neurology. 2000;54(6):1324–31.
Deluca C, Golzar A, Santandrea E, Lo Gerfo E, Estocinova J, Moretto G, et al. The cerebellum and visual perceptual learning: evidence from a motion extrapolation task. Cortex. 2014;58:52–71.
Gogos A, Gavrilescu M, Davison S, Searle K, Adams J, Rossell SL, et al. Greater superior than inferior parietal lobule activation with increasing rotation angle during mental rotation: an fMRI study. Neuropsychologia. 2010;48(2):529–35.
Gross-Tsur V, Ben-Bashat D, Shalev RS, Levav M, Sira LB. Evidence of a developmental cerebello-cerebral disorder. Neuropsychologia. 2006;44(12):2569–72.
Scott RB, Stoodley CJ, Anslow P, Paul C, Stein JF, Sugden EM, et al. Lateralized cognitive deficits in children following cerebellar lesions. Dev Med Child Neurol. 2001;43(10):685–91.
Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. NeuroImage. 2009;46(1):39–46.
Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113.
Raven J, Raven JC, Court JH Manual for Raven’s Progressive Matrices and vocabulary scales: Oxford Psychologists Press.
Conners C. Conners’ rating scales-revised. Multi-Health Systems. Inc: North Tonawanda, New York; 1997.
Wang X, Tao B. Chinese character recognition test battery and assessment scale for primary school children. Shanghai: Shanghai Education Press; 1993.
Shu H, Peng H, McBride-Chang C. Phonological awareness in young Chinese children. Dev Sci. 2008;11(1):171–81.
Zhou W, Xia Z, Bi Y, Shu H. Altered connectivity of the dorsal and ventral visual regions in dyslexic children: a resting-state fMRI study. Front Hum Neurosci. 2015;9:495.
Cui Z, Xia Z, Su M, Shu H, Gong G. Disrupted white matter connectivity underlying developmental dyslexia: a machine learning approach. Hum Brain Mapp. 2016;37(4):1443–58.
Liu L, Wang W, You W, Li Y, Awati N, Zhao X, et al. Similar alterations in brain function for phonological and semantic processing to visual characters in Chinese dyslexia. Neuropsychologia. 2012;50(9):2224–32.
Shu H, Chen X, Anderson RC, Wu NN, Xuan Y. Properties of school Chinese: implications for learning to read. Child Dev. 2003;74(1):27–47.
You H, Gaab N, Wei N, Cheng-Lai A, Wang Z, Jian J, et al. Neural deficits in second language reading: fMRI evidence from Chinese children with English reading impairment. NeuroImage. 2011;57(3):760–70.
Frederickson N, Frith, U, Reason R Phonological Assessment Battery (Manual and Test Materials). 1997.
Mirsky AF, Anthony BJ, Duncan CC, Ahearn MB, Kellam SG. Analysis of the elements of attention: a neuropsychological approach. Neuropsychol Rev. 1991;2(2):109–45.
Temple E, Poldrack RA, Salidis J, Deutsch GK, Tallal P, Merzenich MM, et al. Disrupted neural responses to phonological and orthographic processing in dyslexic children: an fMRI study. Neuroreport. 2001;12(2):299–307.
Siok WT, Spinks JA, Jin Z, Tan LH. Developmental dyslexia is characterized by the co-existence of visuospatial and phonological disorders in Chinese children. Curr Biol. 2009;19(19):R890–2.
Hoeft F, Meyler A, Hernandez A, Juel C, Taylor-Hill H, Martindale JL, et al. Functional and morphometric brain dissociation between dyslexia and reading ability. P Natl Acad Sci USA. 2007;104(10):4234–9.
Fulbright RK, Jenner AR, Mencl WE, Pugh KR, Shaywitz BA, Shaywitz SE, et al. The cerebellum’s role in reading: a functional MR imaging study. Am J Neuroradiol. 1999;20(10):1925–30.
Dehaene S, Pegado F, Braga LW, Ventura P, Nunes G, Jobert A, et al. How learning to read changes the cortical networks for vision and language. Science. 2010;330(6009):1359–64.
Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. NeuroImage. 2006;33(1):127–38.
Houde O, Rossi S, Lubin A, Joliot M. Mapping numerical processing, reading, and executive functions in the developing brain: an fMRI meta-analysis of 52 studies including 842 children. Dev Sci. 2010;13(6):876–85.
Bolger DJ, Perfetti CA, Schneider W. Cross-cultural effect on the brain revisited: universal structures plus writing system variation. Hum Brain Mapp. 2005;25(1):92–104.
Koyama MS, Di Martino A, Zuo XN, Kelly C, Mennes M, Jutagir DR, et al. Resting-state functional connectivity indexes reading competence in children and adults. J Neurosci. 2011;31(23):8617–24.
Koyama MS, Di Martino A, Kelly C, Jutagir DR, Sunshine J, Schwartz SJ, et al. Cortical signatures of dyslexia and remediation: an intrinsic functional connectivity approach. PLoS One. 2013;8(2):e55454.
Snowling M. Dyslexia as a phonological deficit: evidence and implications. Child Psychology & Psychiatry Review. 2003;3(1):4–11.
Nicolson RI, Fawcett AJ, Dean P. Developmental dyslexia: the cerebellar deficit hypothesis. Trends Neurosci. 2001;24(9):508–11.
Menghini D, Hagberg GE, Caltagirone C, Petrosini L, Vicari S. Implicit learning deficits in dyslexic adults: an fMRI study. NeuroImage. 2006;33(4):1218–26.
Richlan F, Sturm D, Schurz M, Kronbichler M, Ladurner G, Wimmer H. A common left occipito-temporal dysfunction in developmental dyslexia and acquired letter-by-letter reading? PLoS One. 2010;5(8).
D’Mello AM, Stoodley CJ. Cerebro-cerebellar circuits in autism spectrum disorder. Front Neurosci-Switz. 2015;9.
Marien P, Ackermann H, Adamaszek M, Barwood CHS, Beaton A, Desmond J, et al. Consensus paper: language and the cerebellum: an ongoing enigma. Cerebellum. 2014;13(3):386–410.
Fernandez VG, Juranek J, Romanowska-Pawliczek A, Stuebing K, Williams VJ, Fletcher JM. White matter integrity of cerebellar-cortical tracts in reading impaired children: A probabilistic tractography study. Brain and Language. 2015.
Wu CY, Ho MHR, Chen SHA. A meta-analysis of fMRI studies on Chinese orthographic, phonological, and semantic processing. NeuroImage. 2012;63(1):381–91.
Pinel P, Lalanne C, Bourgeron T, Fauchereau F, Poupon C, Artiges E, et al. Genetic and environmental influences on the visual word form and fusiform face areas. Cereb Cortex. 2015;25(9):2478–93.
Ma LF, Jiang Y, Bai JE, Gong QY, Liu HC, Chen HC, et al. Robust and task-independent spatial profile of the visual word form activation in fusiform cortex. PLoS One. 2011;6(10).
Wang JJ, Bi HY, Gao LQ, Wydell TN. The visual magnocellular pathway in Chinese-speaking children with developmental dyslexia. Neuropsychologia. 2010;48(12):3627–33.
Hu W, Lee HL, Zhang Q, Liu T, Geng LB, Seghier ML, et al. Developmental dyslexia in Chinese and English populations: dissociating the effect of dyslexia from language differences. Brain. 2010;133(Pt 6):1694–706.
Yang Y, Jia F, Siok WT, Tan LH. Altered functional connectivity in persistent developmental stuttering. Sci Rep. 2016;6:19128.
Acknowledgments
This work was supported by grants from the National Natural Science Foundation of China (NSFC: 81171016, 81371206, 31571158) and the National Key Basic Research Program of China (2014CB846102). We sincerely thank the children, parents, and schools for their participation and cooperation in our study.
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Feng, X., Li, L., Zhang, M. et al. Dyslexic Children Show Atypical Cerebellar Activation and Cerebro-Cerebellar Functional Connectivity in Orthographic and Phonological Processing. Cerebellum 16, 496–507 (2017). https://doi.org/10.1007/s12311-016-0829-2
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DOI: https://doi.org/10.1007/s12311-016-0829-2