Impact of Deafness on the Lateralized Brain Responses to Letters and Digits: A Fast Periodic Visual Stimulation Exploratory Study in Deaf and Hearing Children.
[en] Numbers and letters are culturally created symbols that acquire meaning through extensive training, significantly influencing brain function. The distinct hemispheric specialization of cortical regions for these categories has been hypothesized to relate to the co-activated brain networks: the left language regions for letters, and the right intra-parietal sulcus for numbers. However, the potential influence of deafness and sign language on hemispheric specialization for letters and numbers remains unclear. The present study aims to explore this issue by using a FPVS-EEG approach with an oddball paradigm. Deaf and hearing children aged 8-13 were exposed to rapid streams of visual stimuli (6 Hz), with a deviant category introduced periodically (every 5 items; at 1.2 Hz) and eliciting a neural response in the frequency domain if discriminated from the base category. Here, digits are served as base stimuli and letters as oddball stimuli, and vice-versa. Our results suggest disparities in hemispheric lateralization for letters between deaf and hearing children, while neural responses to digits did not significantly vary between the two groups. Both groups exhibited right-lateralized responses to digits, which were stronger compared to responses to letters. Importantly, in deaf children, the neural response to letters was stronger in the right hemisphere, whereas hearing children displayed a bilateral response with a nonsignificant trend toward left lateralization. The important implications of these exploratory results, suggesting an early impact of sensory deprivation and/or sign language on the organization of the brain, are discussed.
Disciplines :
Neurosciences & behavior
Author, co-author :
Crollen, Virginie ; Psychological Sciences Research Institute (IPSY) and Institute of NeuroScience (IoNS), Université Catholique de Louvain, Louvain-la-Neuve, Belgium
Buyle, Margot ✱; Psychological Sciences Research Institute (IPSY) and Institute of NeuroScience (IoNS), Université Catholique de Louvain, Louvain-la-Neuve, Belgium ; Department of Behavioural and Cognitive Sciences, Faculty of Humanities, Social and Educational Sciences, Institute of Cognitive Science and Assessment, University of Luxembourg, Esch-sur-Alzette, Luxembourg
SCHILTZ, Christine ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS) > Cognitive Science and Assessment
LOCHY, Aliette ; University of Luxembourg ; Psychological Sciences Research Institute (IPSY) and Institute of NeuroScience (IoNS), Université Catholique de Louvain, Louvain-la-Neuve, Belgium
✱ These authors have contributed equally to this work.
External co-authors :
yes
Language :
English
Title :
Impact of Deafness on the Lateralized Brain Responses to Letters and Digits: A Fast Periodic Visual Stimulation Exploratory Study in Deaf and Hearing Children.
This work was supported by the Faculty of Humanities, Education and Social Sciences of the University of Luxembourg, a Wallonie-Bruxelles-International Excellence World funding (JW/16092021/BM) granted to M.B. and a \u201CProjet De Recherche\u201D (PDR, Grant no. T.0036.22) granted by the Fund for Scientific Research\u2013National Fund for Scientific Research (FRS\u2013FNRS, Belgium) to V.C. A.L. is supported by the FNR (Fonds National de la Recherche Luxembourg, C21/SC/16241557/READINGBRAIN).We warmly thank the Centre de Logop\u00E9die (https://logopedie.lu) in Luxembourg, as well as all the children who participated, without whom this work would not have been possible. This work was supported by the Faculty of Humanities, Education and Social Sciences of the University of Luxembourg, a Wallonie-Bruxelles-International Excellence World funding (JW/16092021/BM) granted to MB and a \u201CProjet De Recherche\u201D (PDR, Grant no. T.0036.22) granted by the Fund for Scientific Research\u2013National Fund for Scientific Research (FRS\u2013FNRS, Belgium) to VC. AL is supported by the FNR (Fonds National de la Recherche Luxembourg, C21/SC/16241557/READINGBRAIN).: This work was supported by the Faculty of Humanities, Education and Social Sciences of the University of Luxembourg, a Wallonie\u2010Bruxelles\u2010International Excellence World funding (JW/16092021/BM) granted to M.B. and a \u201CProjet De Recherche\u201D (PDR, Grant no. T.0036.22) granted by the Fund for Scientific Research\u2013National Fund for Scientific Research (FRS\u2013FNRS, Belgium) to V.C. A.L. is supported by the FNR (Fonds National de la Recherche Luxembourg, C21/SC/16241557/READINGBRAIN). FundingWe warmly thank the Centre de Logop\u00E9die ( https://logopedie.lu ) in Luxembourg, as well as all the children who participated, without whom this work would not have been possible. This work was supported by the Faculty of Humanities, Education and Social Sciences of the University of Luxembourg, a Wallonie\u2010Bruxelles\u2010International Excellence World funding (JW/16092021/BM) granted to MB and a \u201CProjet De Recherche\u201D (PDR, Grant no. T.0036.22) granted by the Fund for Scientific Research\u2013National Fund for Scientific Research (FRS\u2013FNRS, Belgium) to VC. AL is supported by the FNR (Fonds National de la Recherche Luxembourg, C21/SC/16241557/READINGBRAIN).
Allison, T., G. McCarthy, A. Nobre, A. Puce, and A. Belger. 1994. “Human Extrastriate Visual Cortex and the Perception of Faces, Words, Numbers, and Colors.” Cerebral Cortex 4, no. 5: 544–554. https://doi.org/10.1093/cercor/4.5.544.
Andin, J., Å. Elwér, and E. Mäki-Torkko. 2023. “Arithmetic in the Signing Brain: Differences and Similarities in Arithmetic Processing Between Deaf Signers and Hearing Non-Signers.” Journal of Neuroscience Research 101, no. 1: 172–195. https://doi.org/10.1002/jnr.25138.
Andin, J., P. Fransson, Ö. Dahlström, J. Rönnberg, and M. Rudner. 2019. “The Neural Basis of Arithmetic and Phonology in Deaf Signing Individuals.” Language, Cognition and Neuroscience 34, no. 7: 813–825. https://doi.org/10.1080/23273798.2019.1616103.
Andin, J., P. Fransson, J. Rönnberg, and M. Rudner. 2018. “fMRI Evidence of Magnitude Manipulation During Numerical Order Processing in Congenitally Deaf Signers.” Neural Plasticity 2018: 2576047. https://doi.org/10.1155/2018/2576047.
Aparicio, M., D. Gounot, E. Demont, and M. N. Metz-Lutz. 2007. “Phonological Processing in Relation to Reading: An fMRI Study in Deaf Readers.” NeuroImage 35: 1303–1316.
Berteletti, I., S. E. Kimbley, S. J. Sullivan, L. C. Quandt, and M. Miyakoshi. 2022. “Different Language Modalities Yet Similar Cognitive Processes in Arithmetic Fact Retrieval.” Brain Sciences 12: 145.
Blau, V., J. Reithler, N. van Atteveldt, et al. 2010. “Deviant Processing of Letters and Speech Sounds as Proximate Cause of Reading Failure: A Functional Magnetic Resonance Imaging Study of Dyslexic Children.” Brain 133, no. 3: 868–879. https://doi.org/10.1093/brain/awp308.
Brysbaert, M. 2019. “How Many Participants Do We Have to Include in Properly Powered Experiments? A Tutorial of Power Analysis With Reference Tables.” Journal of Cognition 2, no. 1: 16.
Buyle, M., A. Lochy, V. Vencato, and V. Crollen. 2023. “Stronger Neural Response to Canonical Finger-Number Configurations in Deaf Compared to Hearing Adults Revealed by FPVS-EEG.” Human Brain Mapping 44, no. 9: 3555–3567. https://doi.org/10.1002/hbm.26297.
Buyle, M., C. Marlair, and V. Crollen. 2021. “Sensory Deprivation: A Window to Study the Visual and Verbal Bases of the Number Sense.” In Diversity Dimensions in Mathematics and Language Learning, edited by A. Fritz-Stratmann, E. Gürsoy, and M. Herzog, 265–288. De Gruyter.
Carreiras, M., P. J. Monahan, M. Lizarazu, J. A. Duñabeitia, and N. Molinaro. 2015. “Numbers Are Not like Words: Different Pathways for Literacy and Numeracy.” Neuroimage 118: 79–89. https://doi.org/10.1016/j.neuroimage.2015.06.021.
Costello, B., S. Caffarra, N. Fariña, J. A. Dunabeitia, and M. Carreiras. 2021. “Reading Without Phonology: ERP Evidence From Skilled Deaf Readers of Spanish.” Scientific Reports 11: 5202. https://doi.org/10.1038/s41598-021-84490-5.
Dehaene, S. 1992. “Varieties of Numerical Abilities.” Cognition 44, no. 1-2: 1–42. https://doi.org/10.1016/0010-0277(92)90049-n.
Dehaene, S., and L. Cohen. 2007. “Cultural Recycling of Cortical Maps.” Neuron 56, no. 2: 384–398. https://doi.org/10.1016/j.neuron.2007.10.004.
Dehaene, S., and L. Cohen. 2011. “The Unique Role of the Visual Word Form Area in Reading.” Trends in Cognitive Sciences 15, no. 6: 254–262. https://doi.org/10.1016/j.tics.2011.04.003.
Dehaene, S., M. Piazza, P. Pinel, and L. Cohen. 2003. “Three Parietal Circuits for Number Processing.” Cognitive Neuropsychology 20, no. 3: 487–506. https://doi.org/10.1080/02643290244000239.
de Heering, A., and B. Rossion. 2015. “Rapid Categorization of Natural Face Images in the Infant Right Hemisphere.” Elife 4: e06564. https://doi.org/10.7554/eLife.06564.
Dotan, D., and N. Friedmann. 2018. “A Cognitive Model for Multidigit Number Reading: Inferences From Individuals With Selective Impairments.” Cortex 101: 249–281.
Dufour, A., R. Brochard, O. Després, C. Scheiber, and C. Robert. 2004. “Perceptual Encoding of Fingerspelled and Printed Alphabet by Deaf Signers: An fMRI Study.” Perceptual and Motor Skills 98, no. 3 pt. 1: 971–982. https://doi.org/10.2466/pms.98.3.971-982.
Dzhelyova, M. C. Jacques, and B. Rossion. 2017. “At a Single Glance: Fast Periodic Visual Stimulation Uncovers the Spatio-Temporal Dynamics of Brief Facial Expression Changes in the Human Brain.” Cerebral Cortex 27: 4106–4123. https://doi.org/10.1093/cercor/bhw223.
Emmorey, K., and B. Lee. 2021. “The Neurocognitive Basis of Skilled Reading in Prelingually and Profoundly Deaf Adults.” Lang Linguist Compass 15, no. 2: e12407. https://doi.org/10.1111/lnc3.12407.
Emmorey, K., K. J. Midgley, C. B. Kohen, Z. S. Sehyr, and P. J. Holcomb. 2017. “The N170 ERP Component Differs in Laterality, Distribution, and Association With Continuous Reading Measures for Deaf and Hearing Readers.” Neuropsychologia 106: 298–309.
Emmorey, K., J. Weisberg, S. McCullough, and J. A. Petrich. 2013. “Mapping the Reading Circuitry for Skilled Deaf Readers: An fMRI Study of Semantic and Phonological Processing.” Brain and Language 126, no. 2: 169–180.
Glezer, L. S., J. Weisberg, O.'G. Farnady, et al. 2018. “Orthographic and Phonological Selectivity Across the Reading System in Deaf Skilled Readers.” Neuropsychologia 117: 500–512. https://doi.org/10.1016/j.neuropsychologia.2018.07.010.
Hamilton, J. P., M. Mirkin, and T. A. Polk. 2006. “Category-Level Contributions to the Alphanumeric Category Effect in Visual Search.” Psychonomic Bulletin & Review 13, no. 6: 1074–1077. https://doi.org/10.3758/BF03213928.
Heinrich, S. P., D. Mell, and M. Bach. 2009. “Frequency-Domain Analysis of Fast Oddball Responses to Visual Stimuli: A Feasibility Study.” International Journal of Psychophysiology 73: 287–293. https://doi.org/10.1016/j.ijpsycho.2009.04.011.
James, K. H., T. W. James, G. Jobard, A. C. N. Wong, and I. Gauthier. 2005. “Letter Processing in the Visual System: Different Activation Patterns for Single Letters and Strings.” Cognitive, Affective & Behavioral Neuroscience 5, no. 4: 452–466. https://doi.org/10.3758/CABN.5.4.452.
Langener, A. M., A.-W. Kramer, W. den Bos, and H. M. Huizenga. 2022. “A Shortened Version of Raven's Standard Progressive Matrices for Children and Adolescents.” British Journal of Developmental Psychology 40, no. 1: 35–45.
Lee, B., and K. Secora. 2022. “Fingerspelling and Its Role in Translanguaging.” Languages 7, no. 4: 278. https://doi.org/10.3390/languages7040278.
Li, Y., D. Peng, L. Liu, J. R. Booth, and G. Ding. 2014. “Brain Activation During Phonological and Semantic Processing of Chinese Characters in Deaf Signers.” Frontiers in Human Neuroscience 8: 211. https://doi.org/10.3389/fnhum.2014.00211.
Liu-Shuang, J., A. M. Norcia, and B. Rossion. 2014. “An Objective Index of Individual Face Discrimination in the Right Occipitotemporal Cortex by Means of Fast Periodic Oddball Stimulation.” Neuropsychologia 52: 57–72.
Lochy, A., and C. Schiltz. 2019. “Lateralized Neural Responses to Letters and Digits in First Graders.” Child Development 90, no. 6: 1866–1874. https://doi.org/10.1111/cdev.13337.
Lochy, A., G. Van Belle, and B. Rossion. 2015. “A Robust Index of Lexical Representation in the Left Occipito-Temporal Cortex as Evidenced by EEG Responses to Fast Periodic Visual Stimulation.” Neuropsychologia 66: 18–31. https://doi.org/10.1016/j.neuropsychologia.2014.11.007.
Lochy, A., M. Van Reybroeck, and B. Rossion. 2016. “Left Cortical Specialization for Visual Letter Strings Predicts Rudimentary Knowledge of Letter-Sound Association in Preschoolers.” PNAS 113, no. 30: 8544–8559. https://doi.org/10.1073/pnas.1520366113.
Marcelino, L., Sousa, and C. Costa. 2019. “Cognitive Foundations of Mathematics Learning in Deaf Students: A Systematic Literature Review.” EDULEARN19 Proceedings, 5914–5923.
Masataka, N., T. Ohnishi, E. Imabayashi, M. Hirakata, and H. Matsuda. 2006. “Neural Correlates for Numerical Processing in the Manual Mode.” Journal of Deaf Studies and Deaf Education 11, no. 2: 144–152. https://doi.org/10.1093/deafed/enj017.
Maurer, U., S. Brem, F. Kranz, et al. 2006. “Coarse Neural Tuning for Print Peaks When Children Learn to Read.” Neuroimage 33, no. 2: 749–758.
Maurer, U., and B. D. McCandliss. 2008. “The Development of Visual Expertise for Words: The Contribution of Electrophysiology.” In Single-Word Reading: Behavioral and Biological Perspectives, edited by E. L. Grigorenko and A. J. Naples, 43–63. Lawrence Erlbaum Associates Publishers.
Mayberry, R. I., A. A. del Giudice, and A. M. Lieberman. 2011. “Reading Achievement in Relation to Phonological Coding and Awareness in Deaf Readers: A Meta-Analysis.” Journal of Deaf Studies and Deaf Education 16, no. 2: 164–188. https://doi.org/10.1093/deafed/enq049.
McCandliss, B. D., L. Cohen, and S. Dehaene. 2003. “The Visual Word Form Area: Expertise for Reading in the Fusiform Gyrus.” Trends in Cognitive Sciences 7, no. 7: 293–299. https://doi.org/10.1016/s1364-6613(03)00134-7.
Nara, S., H. Raza, M. Carreiras, and N. Molinaro. 2023. “Decoding Numeracy and Literacy in the Human Brain: Insights From MEG and MVPA.” Scientific Reports 13: 10979. https://doi.org/10.1038/s41598-023-37113-0.
Neville, H. J., D. Bavelier, D. Corina, et al. 1998. “Cerebral Organization for Language in Deaf and Hearing Subjects: Biological Constraints and Effects of Experience.” PNAS 95, no. 3: 922–929. https://doi.org/10.1073/pnas.95.3.922.
Norcia, A. M., L. G. Appelbaum, J. M. Ales, B. R. Cottereau, and B. Rossion. 2015. “The Steady-State Visual Evoked Potential in Vision Research: A Review.” Journal of Vision (Charlottesville, Va.) 15, no. 6: 4. https://doi.org/10.1167/15.6.4.
Park, J., C. Chiang, E. M. Brannon, and M. G. Woldorff. 2014. “Experience-Dependent Hemispheric Specialization of Letters and Numbers Is Revealed in Early Visual Processing.” Journal of Cognitive Neuroscience 26, no. 10: 2239–2249. https://doi.org/10.1162/jocn_a_00621.
Park, J., A. Hebrank, T. A. Polk, and D. C. Park. 2012. “Neural Dissociation of Number From Letter Recognition and Its Relationship to Parietal Numerical Processing.” Journal of Cognitive Neuroscience 24, no. 1: 39–50. https://doi.org/10.1162/jocn_a_00085.
Park, J., B. van den Berg, C. Chiang, M. G. Woldorff, and E. M. Brannon. 2017. “Developmental Trajectory of Neural Specialization for Letter and Number Visual Processing.” Developmental Science 21: 1–14. https://doi.org/10.1111/desc.12578.
Price, C. J., and J. T. Devlin. 2011. “The Interactive Account of Ventral Occipitotemporal Contributions to Reading.” Trends in Cognitive Sciences 15, no. 6: 246–253. https://doi.org/10.1016/j.tics.2011.04.001.
Raven, J. 1989. “The Raven Progressive Matrices: A Review of National Norming Studies and Ethnic and Socioeconomic Variation Within the United States.” Journal of Educational Measurement 26, no. 1: 1–16. http://www.jstor.org/stable/1434619.
Regan, D. 1968. “Evoked Potentials and Sensation.” Perception & Psychophysics 4: 347–350. https://doi.org/10.3758/BF03209531.
Retter, T. L., and B. Rossion. 2016. “Uncovering the Neural Magnitude and Spatio-Temporal Dynamics of Natural Image Categorization in a Fast Visual Stream.” Neuropsychologia 91: 9–28.
Retter, T. L., B. Rossion, and C. Schiltz. 2021. “Harmonic Amplitude Summation for Frequency-Tagging Analysis.” Journal of Cognitive Neuroscience 33, no. 11: 2372–2393. https://doi.org/10.1162/jocn_a_01763.
Richlan, F., M. Kronbichler, and H. Wimmer. 2011. “Meta-Analyzing Brain Dysfunctions in Dyslexic Children and Adults.” Neuroimage 56, no. 3: 1735–1742. https://doi.org/10.1016/j.neuroimage.2011.02.040.
Rossion, B., E. A. Prieto, A. Boremanse, D. Kuefner, and G. Van Belle. 2012. “A Steady-State Visual Evoked Potential Approach to Individual Face Perception: Effect of Inversion, Contrast-Reversal and Temporal Dynamics.” Neuroimage 63: 1585–1600. https://doi.org/10.1016/j.neuroimage.2012.08.033.
Roux, F. E., V. Lubrano, V. Lauwers-Cances, C. Giussani, and J. F. Démonet. 2008. “Cortical Areas Involved in Arabic Number Reading.” Neurology 70, no. 3: 210–217. https://doi.org/10.1212/01.wnl.0000297194.14452.a0.
Santos, S., and S. Cordes. 2022. “Math Abilities in Deaf and Hard of Hearing Children: The Role of Language in Developing Number Concepts.” Psychological Review 129, no. 1: 199–211. https://doi.org/10.1037/rev0000303.
Schlaggar, B. L., and B. D. McCandliss. 2007. “Development of Neural Systems for Reading.” Annual Review of Neuroscience 30: 475–503. https://doi.org/10.1146/annurev.neuro.28.061604.135645.
Sehyr, Z. S., and K. Emmorey. 2022. “Contribution of Lexical Quality and Sign Language Variables to Reading Comprehension.” The Journal of Deaf Studies and Deaf Education 27, no. 4: 355–372. https://doi.org/10.1093/deafed/enac018.
Sehyr, Z. S., K. J. Midgley, K. Emmorey, and P. J. Holcomb. 2023. “Asymetric Event-Related Potential Priming Effects Between English Letters and American Sign Language Fingerspelling Fonts.” Neurobiology of Language 4, no. 2: 361–381. https://doi.org/10.1162/nol_a_00104.
Shum, J., D. Hermes, B. L. Foster, et al. 2013. “A Brain Area for Visual Numerals.” Journal of Neuroscience 33, no. 16: 6709–6715. https://doi.org/10.1523/JNEUROSCI.4558-12.2013.
Srinivasan, D., D. P. Russell, G. M. Edelman, and G. Tononi. 1999. “Increased Synchronization of Neuromagnetic Responses During Conscious Perception.” Journal of Neuroscience 19, no. 13: 5435–5448. https://doi.org/10.1523/JNEUROSCI.19-13-05435.1999.
Stone, A., G. Kartheiser, P. C. Hauser, L.-A. Petitto, and T. E. Allen. 2015. “Fingerspelling as a Novel Gateway into Reading Fluency in Deaf Bilinguals.” PLOS ONE 10, no. 10: e0139610. https://doi.org/10.1371/journal.pone.0139610.
Sutton-Spence, R., and B. Woll. 1999. The Linguistics of British Sign Language: An Introduction. Cambridge University Press. https://doi.org/10.1017/CBO9781139167048.
van der Mark, S., K. Bucher, U. Maurer, et al. 2009. “Children With Dyslexia Lack Multiple Specializations Along the Visual Word-Form (VWF) System.” Neuroimage 47, no. 4: 1940–1949. https://doi.org/10.1016/j.neuroimage.2009.05.021.
van de Walle de Ghelcke, A., B. Rossion, C. Schiltz, and A. Lochy. 2020. “Impact of Learning to Read in a Mixed Approach on Neural Tuning to Words in Beginning Readers.” Frontiers in Psychology 10: 3043. https://doi.org/10.3389/fpsyg.2019.03043.
van de Walle de Ghelcke, A., B. Rossion, C. Schiltz, and A. Lochy. 2021. “Developmental Changes in Neural Letter-Selectivity: A 1-Year Follow-Up of Beginning Readers.” Developmental Science 24, no. 1: e12999. https://doi.org/10.1111/desc.12999.
Wang, X., A. Caramazza, M. V. Peelen, Z. Han, and Y. Bi. 2015. “Reading Without Speech Sounds: VWFA and Its Connectivity in the Congenitally Deaf.” Cerebral Cortex 25, no. 9: 2416–2426. https://doi.org/10.1093/cercor/bhu044.
Welcome, S. E., and M. F. Joanisse. 2012. “Individual Differences in Skilled Adult Readers Reveal Dissociable Patterns of Neural Activity Associated With Component Processes of Reading.” Brain and Language 120, no. 3: 360–371. https://doi.org/10.1016/j.bandl.2011.12.011.