Abstract
The engagement of the cerebellum during reading tasks is not unprecedented. However, it is still unclear which regions in the cerebellum are specifically involved in reading and how the cerebellum processes different languages. With functional magnetic resonance imaging, we compared the cerebellar neural activity in Chinese child learners of English between reading and non-reading tasks to identify functionally specialized areas for reading, and between Chinese characters and English words in a passive viewing paradigm to detect regions sensitive to different scripts. Two posterior subregions of right lobule VI, as well as right lobule VIIIA, demonstrated greater activation to viewing Chinese characters and English words compared to the non-reading tasks. However, we did not find any cerebellar regions that were differentially responsive to Chinese versus English print. Instead, we observed that functional connectivity between the two above-mentioned cerebellar regions (lobules VI and VIIIA) and the left inferior parietal lobule was significantly greater in English reading compared to Chinese reading. Overall, these results indicate that the posterior parts of right lobule VI and the right lobule VIIIA could be reading-specific regions, and deepen our understanding of how the cerebellum contributes to reading.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data and code available statement
All data and code used during the study are available from the corresponding author by request.
References
Alvarez TA, Fiez JA (2018) Current perspectives on the cerebellum and reading development. Neurosci Biobehav Rev 92:55–66. https://doi.org/10.1016/j.neubiorev.2018.05.006
Ang C, Zhang J, Chu M, Li H, Tian M, Feng X, Zhang M, Liu L, Meng X, Ding G (2020) Intrinsic cerebro-cerebellar functional connectivity reveals the function of cerebellum VI in reading-related skills. Front Psychol 11:420. https://doi.org/10.3389/fpsyg.2020.00420
Ashburn SM, Flowers DL, Napoliello EM, Eden GF (2020) Cerebellar function in children with and without dyslexia during single word processing. Hum Brain Mapp 41(1):120–138. https://doi.org/10.1002/hbm.24792
Barbeau EB, Chai XJ, Chen J-K, Soles J, Berken J, Baum S, Watkins KE, Klein D (2017) The role of the left inferior parietal lobule in second language learning: an intensive language training fMRI study. Neuropsychologia 98:169–176. https://doi.org/10.1016/j.neuropsychologia.2016.10.003
Battista C, Evans TM, Ngoon TJ, Chen T, Chen L, Kochalka J, Menon V (2018) Mechanisms of interactive specialization and emergence of functional brain circuits supporting cognitive development in children. Npj Sci Learn 3(1):1. https://doi.org/10.1038/s41539-017-0017-2
Booth JR, Burman DD, Meyer JR, Gitelman DR, Parrish TB, Mesulam MM (2004) Development of brain mechanisms for processing orthographic and phonologic representations. J Cogn Neurosci 16(7):1234–1249. https://doi.org/10.1162/0898929041920496
Booth JR, Wood L, Lu D, Houk JC, Bitan T (2007) The role of the basal ganglia and cerebellum in language processing. Brain Res 1133(1):136–144. https://doi.org/10.1016/j.brainres.2006.11.074
Boros M, Anton J-L, Pech-Georgel C, Grainger J, Szwed M, Ziegler JC (2016) Orthographic processing deficits in developmental dyslexia: beyond the ventral visual stream. Neuroimage 128:316–327. https://doi.org/10.1016/j.neuroimage.2016.01.014
Buchweitz A, Mason RA, Hasegawa M, Just MA (2009) Japanese and English sentence reading comprehension and writing systems: An fMRI study of first and second language effects on brain activation. Biling Lang Cogn 12(2):141–151. https://doi.org/10.1017/S1366728908003970
Buckner RL (2013) The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron 80(3):807–815. https://doi.org/10.1016/j.neuron.2013.10.044
Cao F, Kim SY, Liu Y, Liu L (2014) Similarities and differences in brain activation and functional connectivity in first and second language reading: evidence from Chinese learners of English. Neuropsychologia 63:275–284. https://doi.org/10.1016/j.neuropsychologia.2014.09.001
Cattinelli I, Borghese NA, Gallucci M, Paulesu E (2013) Reading the reading brain: a new meta-analysis of functional imaging data on reading. J Neurolinguist 26(1):214–238. https://doi.org/10.1016/j.jneuroling.2012.08.001
Chan AH, Luke KK, Li P, Yip V, Li G, Weekes B, Tan LH (2008) Neural correlates of nouns and verbs in early bilinguals. Ann N Y Acad Sci 1145(1):30–40
Cherodath S, Singh NC (2015) The influence of orthographic depth on reading networks in simultaneous biliterate children. Brain Lang 143:42–51. https://doi.org/10.1016/j.bandl.2015.02.001
Cisler JM, Bush K, Steele JSJN (2014) A comparison of statistical methods for detecting context-modulated functional connectivity in fMRI. Neuroimage 84:1042–1052. https://doi.org/10.1016/j.neuroimage.2013.09.018
Das T, Bapi RS, Padakannaya P, Singh NC (2011) Cortical network for reading linear words in an alphasyllabary. Read Writ 24(6):697–707. https://doi.org/10.1007/s11145-010-9241-3
Dehaene S, Pegado F, Braga LW, Ventura P, Nunes Filho G, Jobert A, Dehaene-Lambertz G, Kolinsky R, Morais J, Cohen L (2010) How learning to read changes the cortical networks for vision and language. Science 330(6009):1359–1364. https://doi.org/10.1126/science.1194140
Dehaene-Lambertz G, Monzalvo K, Dehaene S (2018) The emergence of the visual word form: longitudinal evolution of category-specific ventral visual areas during reading acquisition. PLoS Biol 16(3):e2004103. https://doi.org/10.1371/journal.pbio.2004103
Diedrichsen J (2006) A spatially unbiased atlas template of the human cerebellum. Neuroimage 33(1):127–138. https://doi.org/10.1016/j.neuroimage.2006.05.056
Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N (2009) A probabilistic MR atlas of the human cerebellum. Neuroimage 46(1):39–46. https://doi.org/10.1016/j.neuroimage.2009.01.045
D’Mello AM, Turkeltaub PE, Stoodley CJ (2017) Cerebellar tDCS modulates neural circuits during semantic prediction: a combined tDCS-fMRI study. J Neurosci 37(6):1604–1613. https://doi.org/10.1523/JNEUROSCI.2818-16.2017
D’Mello AM, Centanni TM, Gabrieli JD, Christodoulou JA (2020) Cerebellar contributions to rapid semantic processing in reading. Brain Lang 208:104828. https://doi.org/10.1016/j.bandl.2020.104828
Eckert MA, Leonard CM, Richards TL, Aylward EH, Thomson J, Berninger VW (2003) Anatomical correlates of dyslexia: frontal and cerebellar findings. Brain 126(2):482–494. https://doi.org/10.1093/brain/awg026
Eckert MA, Berninger VW, Vaden KI, Gebregziabher M, Tsu L, Consortium DD (2016) Gray matter features of reading disability: a combined meta-analytic and direct analysis approach. Eneuro. https://doi.org/10.1523/ENEURO.0103-15.2015
Feng X, Li L, Zhang ML, Yang XJ, Tian MY, Xie WY, Lu Y, Liu L, Belanger NN, Meng XZ, Ding GS (2017) Dyslexic children show atypical cerebellar activation and cerebro-cerebellar functional connectivity in orthographic and phonological processing. Cerebellum 16(2):496–507. https://doi.org/10.1007/s12311-016-0829-2
Feng X, Altarelli I, Monzalvo K, Ding G, Ramus F, Shu H, Dehaene S, Meng X, Dehaene-Lambertz G (2019) Shared anomalies in cortical reading networks in Chinese and French dyslexic children. bioRxiv 834945
Frings M, Dimitrova A, Schorn CF, Elles H-G, Hein-Kropp C, Gizewski ER, Diener HC, Timmann D (2006) Cerebellar involvement in verb generation: an fMRI study. Neurosci Lett 409(1):19–23. https://doi.org/10.1016/j.neulet.2006.08.058
Gao Q, Wang J, Yu C, Chen H (2015) Effect of handedness on brain activity patterns and effective connectivity network during the semantic task of Chinese characters. Sci Rep 5(1):1–11. https://doi.org/10.1038/srep18262
Gatti D, van Vugt F, Vecchi T (2020) A causal role for the cerebellum in semantic integration: a transcranial magnetic stimulation study. Sci Rep 10(1):1–12. https://doi.org/10.1038/s41598-020-75287-z
Hancock R, Richlan F, Hoeft F (2017) Possible roles for fronto-striatal circuits in reading disorder. Neurosci Biobehav Rev 72:243–260. https://doi.org/10.1016/j.neubiorev.2016.10.025
Ip KI, Marks RA, Hsu LS-J, Desai N, Kuan JL, Tardif TJB, Kovelman I (2019) Morphological processing in Chinese engages left temporal regions. Brain Lang 199:104696. https://doi.org/10.1016/j.bandl.2019.104696
Karipidis I, Pleisch G, Röthlisberger M, Hofstetter C, Dornbierer D, Stämpfli P, Brem S (2017) Neural initialization of audiovisual integration in prereaders at varying risk for developmental dyslexia. Hum Brain Mapp 38(2):1038–1055. https://doi.org/10.1002/hbm.23437 (Epub 2016 Oct 14)
Karipidis II, Pleisch G, Brandeis D, Roth A, Röthlisberger M, Schneebeli M, Walitza S, Brem S (2018) Simulating reading acquisition: the link between reading outcome and multimodal brain signatures of letter–speech sound learning in prereaders. Sci Rep 8(1):7121. https://doi.org/10.1038/s41598-018-24909-8
Kibby MY, Fancher JB, Markanen R, Hynd GW (2008) A quantitative magnetic resonance imaging analysis of the cerebellar deficit hypothesis of dyslexia. J Child Neurol 23(4):368–380. https://doi.org/10.1177/0883073807309235
Kumar U, Das T, Bapi RS, Padakannaya P, Joshi RM, Singh NC (2010) Reading different orthographies: an fMRI study of phrase reading in Hindi–English bilinguals. Read Writ 23(2):239–255. https://doi.org/10.1007/s11145-009-9176-8
Langer N, Benjamin C, Minas J, Gaab N (2015) The neural correlates of reading fluency deficits in children. Cereb Cortex 25(6):1441–1453. https://doi.org/10.1093/cercor/bht330
Leppink J, Osullivan P, Winston K, Pome J (2017) Evidence against vs in favour of a null hypothesis. Perspect Med Educ 6(2):115–118
Li H, Booth JR, Bélanger NN, Feng X, Tian M, Xie W, Zhang M, Gao Y, Ang C, Yang X, Liu L, Meng X, Ding G (2018) Structural correlates of literacy difficulties in the second language: evidence from Mandarin-speaking children learning English. Neuroimage 179:288–297. https://doi.org/10.1016/j.neuroimage.2018.06.037
Li H, Booth JR, Feng X, Wei N, Zhang M, Zhang J, Zhong H, Lu C, Liu L, Ding G, Meng X (2020) Functional parcellation of the right cerebellar lobule VI in children with normal or impaired reading. Neuropsychologia 148:107630. https://doi.org/10.1016/j.neuropsychologia.2020.107630
Li H, Kepinska O, Caballero JN, Zekelman L, Marks RA, Uchikoshi Y, Kovelman I, Hoeft F (2021a) Decoding the role of the cerebellum in the early stages of reading acquisition. Cortex 141:262–279. https://doi.org/10.1016/j.cortex.2021.02.033
Li H, Zhang J, Ding G (2021b) Reading across writing systems: a meta-analysis of the neural correlates for first and second language reading. Biling Lang Cogn 24(3):1–12. https://doi.org/10.1017/S136672892000070X
Liu L, Li H, Zhang M, Wang Z, Wei N, Liu L, Meng X, Ding G (2016) Aberrant topologies and reconfiguration pattern of functional brain network in children with second language reading impairment. Dev Sci 19(4):657–672. https://doi.org/10.1111/desc.12440
Mariën P, Ackermann H, Adamaszek M, Barwood CH, Beaton A, Desmond J, De Witte E, Fawcett AJ, Hertrich I, Küper M (2014) Consensus paper: language and the cerebellum: an ongoing enigma. The Cerebellum 13(3):386–410. https://doi.org/10.1007/s12311-013-0540-5
Martin A, Schurz M, Kronbichler M, Richlan F (2015) Reading in the brain of children and adults: a meta-analysis of 40 functional magnetic resonance imaging studies. Hum Brain Mapp 36(5):1963–1981. https://doi.org/10.1002/hbm.22749
Mazaika PK, Hoeft F, Glover GH, Reiss AL (2009) Methods and software for fMRI analysis of clinical subjects. Neuroimage 47(Suppl 1):S58. https://doi.org/10.1016/S1053-8119(09)70238-1
McLaren DG, Ries ML, Xu G, Johnson SC (2012) A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61(4):1277–1286
Michels L, O’Gorman R, Kucian KJD (2018) Functional hyperconnectivity vanishes in children with developmental dyscalculia after numerical intervention. Dev Cogn Neurosci 30:291–303. https://doi.org/10.1016/j.dcn.2017.03.005
Monzalvo K, Fluss J, Billard C, Dehaene S, Dehaene-Lambertz G (2012) Cortical networks for vision and language in dyslexic and normal children of variable socio-economic status. Neuroimage 61(1):258–274. https://doi.org/10.1016/j.neuroimage.2012.02.035
Moore DM, D’Mello AM, McGrath LM, Stoodley CJJD (2017) The developmental relationship between specific cognitive domains and grey matter in the cerebellum. Dev Cogn Neurosci 24:1–11. https://doi.org/10.1016/j.dcn.2016.12.001
Nicolson RI, Fawcett AJ, Dean P (2001) Developmental dyslexia: the cerebellar deficit hypothesis. Trends Neurosci 24(9):508–511. https://doi.org/10.1016/S0166-2236(00)01896-8
Oldfield (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113. https://doi.org/10.1016/0028-3932(71)90067-4
Park HR, Badzakova-Trajkov G, Waldie KE (2012) Language lateralisation in late proficient bilinguals: a lexical decision fMRI study. Neuropsychologia 50(5):688–695. https://doi.org/10.1016/j.neuropsychologia.2012.01.005
Paz-Alonso PM, Oliver M, Lerma-Usabiaga G, Caballero-Gaudes C, Quiñones I, Suárez-Coalla P, Duñabeitia JA, Cuetos F, Carreiras M (2018) Neural correlates of phonological, orthographic and semantic reading processing in dyslexia. NeuroImage Clin 20:433–447. https://doi.org/10.1016/j.nicl.2018.08.018
Quintana DS, Williams DRJB (2018) Bayesian alternatives for common null-hypothesis significance tests in psychiatry: a non-technical guide using JASP. BMC Psychiatry 18(1):1–8. https://doi.org/10.1186/s12888-018-1761-4
Rae C, Harasty JA, Dzendrowskyj TE, Talcott JB, Simpson JM, Blamire AM, Dixon RM, Lee MA, Thompson CH, Styles P (2002) Cerebellar morphology in developmental dyslexia. Neuropsychologia 40(8):1285–1292. https://doi.org/10.1016/S0028-3932(01)00216-0
Raschle NM, Zuk J, Gaab N (2012) Functional characteristics of developmental dyslexia in left-hemispheric posterior brain regions predate reading onset. Proc Natl Acad Sci 109(6):2156–2161. https://doi.org/10.1073/pnas.1107721109
Raven JC, Court JH (1998) Raven’s progressive matrices and vocabulary scales. Oxford Psychologists Press, Oxford, UK
Riva D, Giorgi C (2000) The cerebellum contributes to higher functions during development. Brain A J Neurol 5:5. https://doi.org/10.1093/brain/123.5.1051
Rueckl JG, Paz-Alonso PM, Molfese PJ, Kuo W-J, Bick A, Frost SJ, Hancock R, Wu DH, Mencl WE, Duñabeitia JA (2015) Universal brain signature of proficient reading: Evidence from four contrasting languages. Proc Natl Acad Sci 112(50):15510–15515. https://doi.org/10.1073/pnas.1509321112
Schmahmann JD (1996) From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing. Hum Brain Mapp 4(3):174–198. https://doi.org/10.1002/(SICI)1097-0193(1996)4:3%3c174::AID-HBM3%3e3.0.CO;2-0
Scott RB, Stoodley CJ, Anslow P, Paul C, Stein JF, Sugden EM, Mitchell CD (2001) Lateralized cognitive deficits in children following cerebellar lesions. Dev Med Child Neurol 43(10):685–691
Sokolov Arseny A, Miall RC, Ivry Richard B (2017) The cerebellum: adaptive prediction for movement and cognition. Trends Cogn Sci 21(5):313–332. https://doi.org/10.1016/j.tics.2017.02.005
Stoodley CJ (2014) Distinct regions of the cerebellum show gray matter decreases in autism, ADHD, and developmental dyslexia. Front Syst Neurosci. https://doi.org/10.3389/fnsys.2014.00092
Stoodley CJ, Schmahmann JD (2009) Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44(2):489–501. https://doi.org/10.1016/j.neuroimage.2008.08.039
Stoodley CJ, Stein JF (2013) Cerebellar function in developmental dyslexia. Cerebellum 12(2):267–276. https://doi.org/10.1007/s12311-012-0407-1
Stoodley CJ, Valera EM, Schmahmann JD (2012) Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. Neuroimage 59(2):1560–1570. https://doi.org/10.1016/j.neuroimage.2011.08.065
Tan LH, Laird AR, Li K, Fox PT (2005) Neuroanatomical correlates of phonological processing of Chinese characters and alphabetic words: a meta-analysis. Hum Brain Mapp 25(1):83–91. https://doi.org/10.1002/hbm.20134
Thürling M, Küper M, Stefanescu R, Maderwald S, Gizewski E, Ladd ME, Timmann DJN (2011) Activation of the dentate nucleus in a verb generation task: a 7 T MRI study. J NeuroIamage 57(3):1184–1191. https://doi.org/10.1016/j.neuroimage.2011.05.045
Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA (2002) Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 16(3):765–780. https://doi.org/10.1006/nimg.2002.1131
Van de Putte E, De Baene W, Brass M, Duyck W (2017) Neural overlap of L1 and L2 semantic representations in speech: a decoding approach. Neuroimage 162:106–116. https://doi.org/10.1016/j.neuroimage.2017.08.082
Wang X, Tao B (1993) Chinese character recognition test battery and assessment scale for primary school children. Shanghai Education Press, Shanghai
Weiss Y, Cweigenberg HG, Booth JR (2018) Neural specialization of phonological and semantic processing in young children. Hum Brain Mapp. https://doi.org/10.1002/hbm.24274
Woodcock R (1987) Manual for the woodcock reading mastery test-revised. American Guidance Service, Circle Pines
Wu C-Y, Ho M-HR, Chen S-HA (2012) A meta-analysis of fMRI studies on Chinese orthographic, phonological, and semantic processing. Neuroimage 63(1):381–391. https://doi.org/10.1016/j.neuroimage.2012.06.047
Xia Z, Hoeft F, Zhang L, Shu H (2016) Neuroanatomical anomalies of dyslexia: disambiguating the effects of disorder, performance, and maturation. Neuropsychologia 81:68–78. https://doi.org/10.1016/j.neuropsychologia.2015.12.003
Xu M, Wang T, Chen S, Fox PT, Tan LH (2015) Effective connectivity of brain regions related to visual word recognition: an fMRI study of Chinese reading. Hum Brain Mapp 36(7):2580–2591. https://doi.org/10.1002/hbm.22792
Xu M, Baldauf D, Chang CQ, Desimone R, Tan LH (2017) Distinct distributed patterns of neural activity are associated with two languages in the bilingual brain. Sci Adv 3(7):e1603309. https://doi.org/10.1126/sciadv.1603309
You H, Gaab N, Wei N, Cheng-Lai A, Wang Z, Jian J, Song M, Meng X, Ding G (2011) Neural deficits in second language reading: fMRI evidence from Chinese children with English reading impairment. Neuroimage 57(3):760–770. https://doi.org/10.1016/j.neuroimage.2010.12.003
Younger JW, Tucker-Drob E, Booth JR (2017) Longitudinal changes in reading network connectivity related to skill improvement. Neuroimage 158:90–98. https://doi.org/10.1016/j.neuroimage.2017.06.044
Zhang H, Wang X (1985) Raven’s IQ reasoning standardized test. Beijing Normal University Press, Beijing
Zhang Y, Shao H, Gaspar CM, Chen W, Zhu J, Tang Y, He S, Weng XJCSB (2015) Face information processing in the left inferior temporal lobe: an ECoG case study. Chin Sci Bull 60(25):2438–2446. https://doi.org/10.1360/N972015-00366
Acknowledgements
This work was supported by Grants from the National Natural Science Foundation of China (NSFC: 31971039, 31971036, 32100846) and Shenzhen-Hong Kong institute of Brain Science-Shenzhen Fundamental Research Institutions (2021SHIBS0003). It was also supported by Project funded by China Postdoctoral Science Foundation (Grant No. 2020M682846) and the Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning (Grant No. CNLYB2005).
Author information
Authors and Affiliations
Contributions
HL: conceptualization, methodology, investigation, formal analysis, writing—original draft, funding acquisition. RAM: writing—original draft, writing—review and editing. LL: writing—original draft, writing—review and editing. XF: investigation, writing—review and editing. MZ: investigation, writing—review and editing. FA: investigation, writing—review and editing. YG: investigation, writing—review and editing. MT: investigation, writing—review and editing. XY: investigation, writing—review and editing. JZ: writing—review and editing. HZ: writing—review and editing. LL: investigation, writing—review and editing, project administration. XM: conceptualization, investigation, methodology, writing—review and editing, project administration, supervision, funding acquisition. GD: conceptualization, investigation, methodology, writing—original draft, writing—review and editing, project administration, supervision, funding acquisition.
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare.
Ethics approval
The use of human subjects for this study has been approved by the Ethical Review Board of Beijing Normal University.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, H., Marks, R.A., Liu, L. et al. The selective contributions of right cerebellar lobules to reading. Brain Struct Funct 227, 963–977 (2022). https://doi.org/10.1007/s00429-021-02434-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-021-02434-1