Beyond Reading Modulation: Temporo-Parietal tDCS Alters Visuo-Spatial Attention and Motion Perception in Dyslexia

Giulia Lazzaro, Sara Bertoni, Deny Menghini, Floriana Costanzo, Sandro Franceschini, Cristiana Varuzza, Luca Ronconi, Andrea Battisti, Simone Gori, Andrea Facoetti, Stefano Vicari, Giulia Lazzaro, Sara Bertoni, Deny Menghini, Floriana Costanzo, Sandro Franceschini, Cristiana Varuzza, Luca Ronconi, Andrea Battisti, Simone Gori, Andrea Facoetti, Stefano Vicari

Abstract

Dyslexia is a neurodevelopmental disorder with an atypical activation of posterior left-hemisphere brain reading networks (i.e., temporo-occipital and temporo-parietal regions) and multiple neuropsychological deficits. Transcranial direct current stimulation (tDCS) is a tool for manipulating neural activity and, in turn, neurocognitive processes. While studies have demonstrated the significant effects of tDCS on reading, neurocognitive changes beyond reading modulation have been poorly investigated. The present study aimed at examining whether tDCS on temporo-parietal regions affected not only reading, but also phonological skills, visuo-spatial working memory, visuo-spatial attention, and motion perception in a polarity-dependent way. In a within-subjects design, ten children and adolescents with dyslexia performed reading and neuropsychological tasks after 20 min of exposure to Left Anodal/Right Cathodal (LA/RC) and Right Anodal/Left Cathodal (RA/LC) tDCS. LA/RC tDCS compared to RA/LC tDCS improved text accuracy, word recognition speed, motion perception, and modified attentional focusing in our group of children and adolescents with dyslexia. Changes in text reading accuracy and word recognition speed-after LA/RC tDCS compared to RA/LC-were related to changes in motion perception and in visuo-spatial working memory, respectively. Our findings demonstrated that reading and domain-general neurocognitive functions in a group of children and adolescents with dyslexia change following tDCS and that they are polarity-dependent.

Keywords: attention; brain reading networks; children and adolescents; cortical excitability; magnocellular-dorsal pathway; neural noise; neuromodulation.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Coherent dot motion task.
Figure 2
Figure 2
Attentional zooming task.
Figure 3
Figure 3
Coherent dot motion (CDM) accuracy (raw data) for the two stimulation conditions; * represents the significant difference from the chance level of 0.25 and from the threshold of 0.5 of accuracy in LA/RC condition. + represents the significant difference from the chance level of 0.25 in RA/LC condition (panel (A)), p < 0.05 in 75% CDM threshold (panel (B)), and p < 0.05 in slope values (panel (C)), as a function of stimulation condition, obtained from the psychometric curve (logistic) fitted on individual data. Dots represent individual data points.
Figure 4
Figure 4
Reaction times (RTs) in attentional zooming task at 100 ms cue-target SOA (panel (A)), and at 800 ms cue-target SOA (panel (B)) in Left Anodal/Right Cathodal (LA/RC) and Right Anodal/Left Cathodal (RA/LC) conditions. Panel (A): RTs in large cue are significantly slower than small cue in LA/RC condition. Dots represent individual data points. * p < 0.05

References

    1. American Psychiatric Association . Diagnostic and Statistical Manual of Mental Disorders. 5th ed. American Psychiatric Association; Washington, DC, USA: 2013.
    1. Gabrieli J.D. Dyslexia: A new synergy between education and cognitive neuroscience. Science. 2009;325:280–283. doi: 10.1126/science.1171999.
    1. Peterson R.L., Pennington B.F. Developmental dyslexia. Annu. Rev. Clin. Psychol. 2015;11:283–307. doi: 10.1146/annurev-clinpsy-032814-112842.
    1. Richlan F. The Functional Neuroanatomy of Letter-Speech Sound Integration and Its Relation to Brain Abnormalities in Developmental Dyslexia. Front. Hum. Neurosci. 2019;13:21. doi: 10.3389/fnhum.2019.00021.
    1. Richlan F., Kronbichler M., Wimmer H. Meta-analyzing brain dysfunctions in dyslexic children and adults. NeuroImage. 2011;56:1735–1742. doi: 10.1016/j.neuroimage.2011.02.040.
    1. Richlan F. Developmental dyslexia: Dysfunction of a left hemisphere reading network. Front. Hum. Neurosci. 2012;6:120. doi: 10.3389/fnhum.2012.00120.
    1. Hoeft F., Hernandez A., McMillon G., Taylor-Hill H., Martindale J.L., Meyler A., Keller T.A., Siok W.T., Deutsch G.K., Just M.A., et al. Neural basis of dyslexia: A comparison between dyslexic and nondyslexic children equated for reading ability. J. Neurosci. 2006;26:10700–10708. doi: 10.1523/JNEUROSCI.4931-05.2006.
    1. Corbetta M., Patel G., Shulman G.L. The reorienting system of the human brain: From environment to theory of mind. Neuron. 2008;58:306–324. doi: 10.1016/j.neuron.2008.04.017.
    1. Bertoni S., Franceschini S., Puccio G., Mancarella M., Gori S., Facoetti A. Action Video Games Enhance Attentional Control and Phonological Decoding in Children with Developmental Dyslexia. Brain Sci. 2021;11:171. doi: 10.3390/brainsci11020171.
    1. Menghini D., Finzi A., Benassi M., Bolzani R., Facoetti A., Giovagnoli S., Ruffino M., Vicari S. Different underlying neurocognitive deficits in developmental dyslexia: A comparative study. Neuropsychologia. 2010;48:863–872. doi: 10.1016/j.neuropsychologia.2009.11.003.
    1. Franceschini S., Gori S., Ruffino M., Pedrolli K., Facoetti A. A causal link between visual spatial attention and reading acquisition. Curr. Biol. 2012;22:814–819. doi: 10.1016/j.cub.2012.03.013.
    1. Gori S., Molteni M., Facoetti A. Visual Illusions: An Interesting Tool to Investigate Developmental Dyslexia and Autism Spectrum Disorder. Front. Hum. Neurosci. 2016;10:175. doi: 10.3389/fnhum.2016.00175.
    1. Carroll J.M., Solity J., Shapiro L.R. Predicting dyslexia using prereading skills: The role of sensorimotor and cognitive abilities. J. Child. Psychol. Psychiatry. 2016;57:750–758. doi: 10.1111/jcpp.12488.
    1. Franceschini S., Trevisan P., Ronconi L., Bertoni S., Colmar S., Double K., Facoetti A., Gori S. Action video games improve reading abilities and visual-to-auditory attentional shifting in English-speaking children with dyslexia. Sci. Rep. 2017;7:5863. doi: 10.1038/s41598-017-05826-8.
    1. Bertoni S., Franceschini S., Ronconi L., Gori S., Facoetti A. Is excessive visual crowding causally linked to developmental dyslexia? Neuropsychologia. 2019;130:107–117. doi: 10.1016/j.neuropsychologia.2019.04.018.
    1. Snowling M.J., Lervåg A., Nash H.M., Hulme C. Longitudinal relationships between speech perception, phonological skills and reading in children at high-risk of dyslexia. Dev. Sci. 2019;22:e12723. doi: 10.1111/desc.12723.
    1. Bradley L., Bryant P.E. Categorizing sounds and learning to read: A causal connection. Nature. 1983;301:419–421. doi: 10.1038/301419a0.
    1. Franceschini S., Gori S., Ruffino M., Viola S., Molteni M., Facoetti A. Action video games make dyslexic children read better. Curr. Biol. 2013;23:462–466. doi: 10.1016/j.cub.2013.01.044.
    1. Dehaene S., Cohen L., Morais J., Kolinsky R. Illiterate to literate: Behavioural and cerebral changes induced by reading acquisition. Nat. Rev. Neurosci. 2015;16:234–244. doi: 10.1038/nrn3924.
    1. Johnson M.H. Interactive specialization: A domain-general framework for human functional brain development? Dev. Cogn. Neurosci. 2011;1:7–21. doi: 10.1016/j.dcn.2010.07.003.
    1. Snowling M. Dyslexia. 2nd ed. Blackwell Publishing; Oxford, UK: 2000.
    1. Vellutino F.R., Fletcher J.M., Snowling M.J., Scanlon D.M. Specific reading disability (dyslexia): What have we learned in the past four decades? J. Child. Psychol. Psychiatry. 2004;45:2–40. doi: 10.1046/j.0021-9630.2003.00305.x.
    1. Melby-Lervåg M., Lyster S.A., Hulme C. Phonological skills and their role in learning to read: A meta-analytic review. Psychol. Bull. 2012;138:322–352. doi: 10.1037/a0026744.
    1. Horowitz-Kraus T., Hutton J.S. From emergent literacy to reading: How learning to read changes a child’s brain. Acta Paediatr. 2015;104:648–656. doi: 10.1111/apa.13018.
    1. Kosmidis M.H., Zafiri M., Politimou N. Literacy versus formal schooling: Influence on working memory. Arch. Clin. Neuropsychol. 2011;26:575–582. doi: 10.1093/arclin/acr063.
    1. Kosmidis M.H., Tsapkini K., Folia V. Lexical processing in illiteracy: Effect of literacy or education? Cortex. 2006;42:1021–1027. doi: 10.1016/S0010-9452(08)70208-9.
    1. Petersson K.M., Reis A., Ingvar M. Cognitive processing in literate and illiterate subjects: A review of some recent behavioral and functional neuroimaging data. Scand. J. Psychol. 2001;42:251–267. doi: 10.1111/1467-9450.00235.
    1. Lazzaro G., Varuzza C., Costanzo F., Fucà E., Di Vara S., De Matteis M.E., Vicari S., Menghini D. Memory Deficits in Children with Developmental Dyslexia: A Reading-Level and Chronological-Age Matched Design. Brain Sci. 2021;11:40. doi: 10.3390/brainsci11010040.
    1. Tallal P. Auditory temporal perception, phonics, and reading disabilities in children. Brain Lang. 1980;9:182–198. doi: 10.1016/0093-934X(80)90139-X.
    1. Tallal P. Improving language and literacy is a matter of time. Nat. Rev. Neurosci. 2004;5:721–728. doi: 10.1038/nrn1499.
    1. Hornickel J., Kraus N. Unstable representation of sound: A biological marker of dyslexia. J. Neurosci. 2013;33:3500–3504. doi: 10.1523/JNEUROSCI.4205-12.2013.
    1. Hari R., Renvall H. Impaired processing of rapid stimulus sequences in dyslexia. Trends Cogn. Sci. 2001;5:525–532. doi: 10.1016/S1364-6613(00)01801-5.
    1. Bosse M.L., Tainturier M.J., Valdois S. Developmental dyslexia: The visual attention span deficit hypothesis. Cognition. 2007;104:198–230. doi: 10.1016/j.cognition.2006.05.009.
    1. Roach N.W., Hogben J.H. Impaired filtering of behaviourally irrelevant visual information in dyslexia. Brain. 2007;130:771–785. doi: 10.1093/brain/awl353.
    1. Facoetti A., Trussardi A.N., Ruffino M., Lorusso M.L., Cattaneo C., Galli R., Molteni M., Zorzi M. Multisensory spatial attention deficits are predictive of phonological decoding skills in developmental dyslexia. J. Cogn. Neurosci. 2010;22:1011–1025. doi: 10.1162/jocn.2009.21232.
    1. Lallier M., Tainturier M.J., Dering B., Donnadieu S., Valdois S., Thierry G. Behavioral and ERP evidence for amodal sluggish attentional shifting in developmental dyslexia. Neuropsychologia. 2010;48:4125–4135. doi: 10.1016/j.neuropsychologia.2010.09.027.
    1. Zorzi M., Barbiero C., Facoetti A., Lonciari I., Carrozzi M., Montico M., Bravar L., George F., Pech-Georgel C., Ziegler J.C. Extra-large letter spacing improves reading in dyslexia. Proc. Natl. Acad. Sci. USA. 2012;109:11455–11459. doi: 10.1073/pnas.1205566109.
    1. Galaburda A., Livingstone M. Evidence for a magnocellular defect in developmental dyslexia. Ann. N. Y. Acad. Sci. 1993;682:70–82. doi: 10.1111/j.1749-6632.1993.tb22960.x.
    1. Kevan A., Pammer K. Visual deficits in pre-readers at familial risk for dyslexia. Vis. Res. 2008;48:2835–2839. doi: 10.1016/j.visres.2008.09.022.
    1. Kevan A., Pammer K. Predicting early reading skills from pre-reading measures of dorsal stream functioning. Neuropsychologia. 2009;47:3174–3181. doi: 10.1016/j.neuropsychologia.2009.07.016.
    1. Boets B., Vandermosten M., Cornelissen P., Wouters J., Ghesquière P. Coherent motion sensitivity and reading development in the transition from prereading to reading stage. Child. Dev. 2011;82:854–869. doi: 10.1111/j.1467-8624.2010.01527.x.
    1. Gori S., Cecchini P., Bigoni A., Molteni M., Facoetti A. Magnocellular-dorsal pathway and sub-lexical route in developmental dyslexia. Front. Hum. Neurosci. 2014;8:460. doi: 10.3389/fnhum.2014.00460.
    1. Lawton T. Improving Dorsal Stream Function in Dyslexics by Training Figure/Ground Motion Discrimination Improves Attention, Reading Fluency, and Working Memory. Front. Hum. Neurosci. 2016;10:397. doi: 10.3389/fnhum.2016.00397.
    1. Walsh V. Dyslexia. Reading between the laminae. Curr. Biol. 1995;5:1216–1217. doi: 10.1016/S0960-9822(95)00240-5.
    1. Stein J., Walsh V. To see but not to read; the magnocellular theory of dyslexia. Trends Neurosci. 1997;20:147–152. doi: 10.1016/S0166-2236(96)01005-3.
    1. Boden C., Giaschi D. M-stream deficits and reading-related visual processes in developmental dyslexia. Psychol. Bull. 2007;133:346–366. doi: 10.1037/0033-2909.133.2.346.
    1. Laycock R., Crewther S.G. Towards an understanding of the role of the ‘magnocellular advantage’ in fluent reading. Neurosci. Biobehav. Rev. 2008;32:1494–1506. doi: 10.1016/j.neubiorev.2008.06.002.
    1. Vidyasagar T.R., Pammer K. Dyslexia: A deficit in visuo-spatial attention, not in phonological processing. Trends Cogn. Sci. 2010;14:57–63. doi: 10.1016/j.tics.2009.12.003.
    1. Gori S., Facoetti A. How the visual aspects can be crucial in reading acquisition? The intriguing case of crowding and developmental dyslexia. J. Vis. 2015;15:15.1.8. doi: 10.1167/15.1.8.
    1. Menghini D., Finzi A., Carlesimo G.A., Vicari S. Working memory impairment in children with developmental dyslexia: Is it just a phonological deficit? Dev. Neuropsychol. 2011;36:199–213. doi: 10.1080/87565641.2010.549868.
    1. Bestmann S., Walsh V. Transcranial electrical stimulation. Curr. Biol. 2017;27:R1258–R1262. doi: 10.1016/j.cub.2017.11.001.
    1. Woods A.J., Antal A., Bikson M., Boggio P.S., Brunoni A.R., Celnik P., Cohen L.G., Fregni F., Herrmann C.S., Kappenman E.S., et al. A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin. Neurophysiol. 2016;127:1031–1048. doi: 10.1016/j.clinph.2015.11.012.
    1. Kirimoto H., Ogata K., Onishi H., Oyama M., Goto Y., Tobimatsu S. Transcranial direct current stimulation over the motor association cortex induces plastic changes in ipsilateral primary motor and somatosensory cortices. Clin. Neurophysiol. 2011;122:777–783. doi: 10.1016/j.clinph.2010.09.025.
    1. Turkeltaub P.E., Benson J., Hamilton R.H., Datta A., Bikson M., Coslett H.B. Left lateralizing transcranial direct current stimulation improves reading efficiency. Brain Stimul. 2012;5:201–207. doi: 10.1016/j.brs.2011.04.002.
    1. Younger J.W., Randazzo Wagner M., Booth J.R. Weighing the cost and benefit of transcranial direct current stimulation on different reading subskills. Front. Neurosci. 2016;10 doi: 10.3389/fnins.2016.00262.
    1. Younger J.W., Booth J.R. Parietotemporal stimulation affects acquisition of novel grapheme-phoneme mappings in adult readers. Front. Hum. Neurosci. 2018;12 doi: 10.3389/fnhum.2018.00109.
    1. Heth I., Lavidor M. Improved reading measures in adults with dyslexia following transcranial direct current stimulation treatment. Neuropsychologia. 2015;70:107–113. doi: 10.1016/j.neuropsychologia.2015.02.022.
    1. Costanzo F., Varuzza C., Rossi S., Sdoia S., Varvara P., Oliveri M., Koch G., Vicari S., Menghini D. Reading changes in children and adolescents with dyslexia after transcranial direct current stimulation. Neuroreport. 2016;27:295–300. doi: 10.1097/WNR.0000000000000536.
    1. Costanzo F., Varuzza C., Rossi S., Sdoia S., Varvara P., Oliveri M., Giacomo K., Vicari S., Menghini D. Evidence for reading improvement following tDCS treatment in children and adolescents with dyslexia. Restor. Neurol. Neurosci. 2016;34:215–226. doi: 10.3233/RNN-150561.
    1. Costanzo F., Rossi S., Varuzza C., Varvara P., Vicari S., Menghini D. Long-lasting improvement following tDCS treatment combined with a training for reading in children and adolescents with dyslexia. Neuropsychologia. 2019;130:38–43. doi: 10.1016/j.neuropsychologia.2018.03.016.
    1. Rios D.M., Rios C.M., Bandeira I.D., Queiros Campbell F., de Carvalho Vaz D., Lucena R. Impact of transcranial direct current stimulation on reading skills of children and adolescents with dyslexia. Child. Neurol. Open. 2018;5:2329048X1879825. doi: 10.1177/2329048X18798255.
    1. Lazzaro G., Costanzo F., Varuzza C., Rossi S., De Matteis M.E., Vicari S., Menghini D. Individual Differences Modulate the Effects of tDCS on Reading in Children and Adolescents with Dyslexia. Sci. Stud. Read. 2020 doi: 10.1080/10888438.2020.1842413.
    1. Raven J.C. Coloured Progressive Matrices. Giunti OS Organizzazioni Speciali; Firenze, Italy: 2008.
    1. Raven J.C. Standard Progressive Matrices. Giunti OS Organizzazioni Speciali; Firenze, Italy: 2008.
    1. Oldfield R.C. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia. 1971;9:97–113. doi: 10.1016/0028-3932(71)90067-4.
    1. Sartori G., Job R., Tressoldi P.E. DDE-2. Batteria per la Valutazione della Dislessia e della Disortografia Evolutiva. Giunti OS Organizzazioni Speciali; Firenze, Italy: 2007.
    1. Stella G., Tintoni C. Indagine e rilevazione sulle abilità di lettura nelle scuole secondarie di secondo grado. Dislessia. 2007;4:271–285.
    1. Cornoldi C., Pra Baldi A., Friso G. MT avanzate 2—Prove MT Avanzate di Lettura e Matematica 2° per il Biennio della Scuola Secondaria di Secondo Grado. Giunti OS Organizzazioni Speciali; Firenze, Italy: 2010.
    1. Cornoldi C., Colpo G. Nuove Prove MT per la Scuola Secondaria di I Grado. Giunti OS Organizzazioni Speciali; Firenze, Italy: 2012.
    1. Conners C.K. In: Conners’ Rating Scales–Revised. Nobile M., Alberti B., Zuddas A., editors. Giunti OS Organizzazioni Speciali; Firenze, Italy: 2007.
    1. Costanzo F., Menghini D., Caltagirone C., Oliveri M., Vicari S. High frequency rTMS over the left parietal lobule increases non-word reading accuracy. Neuropsychologia. 2012;50:2645–2651. doi: 10.1016/j.neuropsychologia.2012.07.017.
    1. Costanzo F., Menghini D., Caltagirone C., Oliveri M., Vicari S. How to improve reading skills in dyslexics: The effect of high frequency rTMS. Neuropsychologia. 2013;51:2953–2959. doi: 10.1016/j.neuropsychologia.2013.10.018.
    1. Denckla M.B., Rudel R.G. Rapid “automatized” naming (R.A.N): Dyslexia differentiated from other learning disabilities. Neuropsychologia. 1976;14:471–479. doi: 10.1016/0028-3932(76)90075-0.
    1. Britten K.H., Shadlen M.N., Newsome W.T., Movshon J.A. The analysis of visual motion: A comparison of neuronal and psychophysical performance. J. Neurosci. 1992;12:4745–4765. doi: 10.1523/JNEUROSCI.12-12-04745.1992.
    1. Pilly P.K., Seitz A.R. What a difference a parameter makes: A psychophysical comparison of random dot motion algorithms. Vis. Res. 2009;49:1599–1612. doi: 10.1016/j.visres.2009.03.019.
    1. Ronconi L., Gori S., Ruffino M., Franceschini S., Urbani B., Molteni M., Facoetti A. Decreased coherent motion discrimination in autism spectrum disorder: The role of attentional zoom-out deficit. PLoS ONE. 2012;7:e49019. doi: 10.1371/journal.pone.0049019.
    1. Facoetti A., Molteni M. The gradient of visual attention in developmental dyslexia. Neuropsychologia. 2001;39:352–357. doi: 10.1016/S0028-3932(00)00138-X.
    1. Ronconi L., Gori S., Ruffino M., Molteni M., Facoetti A. Zoom-out attentional impairment in children with autism spectrum disorder. Cortex. 2013;49:1025–1033. doi: 10.1016/j.cortex.2012.03.005.
    1. Gori S., Yazdanbakhsh A. The riddle of the Rotating-Tilted-Lines illusion. Perception. 2008;37:631–635. doi: 10.1068/p5770.
    1. Cancer A., Antonietti A. tDCS Modulatory Effect on Reading Processes: A Review of Studies on Typical Readers and Individuals with Dyslexia. Front. Behav. Neurosci. 2018;12:162. doi: 10.3389/fnbeh.2018.00162.
    1. Livingstone M.S., Rosen G.D., Drislane F.W., Galaburda A.M. Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. Proc. Natl. Acad. Sci. USA. 1991;88:7943–7947. doi: 10.1073/pnas.88.18.7943.
    1. Eden G.F., VanMeter J.W., Rumsey J.M., Maisog J.M., Woods R.P., Zeffiro T.A. Abnormal processing of visual motion in dyslexia revealed by functional brain imaging. Nature. 1996;382:66–69. doi: 10.1038/382066a0.
    1. Demb J.B., Boynton G.M., Best M., Heeger D.J. Psychophysical evidence for a magnocellular pathway deficit in dyslexia. Vis. Res. 1998;38:1555–1559. doi: 10.1016/S0042-6989(98)00075-3.
    1. Ben-Shachar M., Dougherty R.F., Deutsch G.K., Wandell B.A. Contrast responsivity in MT+ correlates with phonological awareness and reading measures in children. NeuroImage. 2007;37:1396–1406. doi: 10.1016/j.neuroimage.2007.05.060.
    1. Gori S., Seitz A.R., Ronconi L., Franceschini S., Facoetti A. Multiple Causal Links between Magnocellular-Dorsal Pathway Deficit and Developmental Dyslexia. Cereb. Cortex. 2016;26:4356–4369. doi: 10.1093/cercor/bhv206.
    1. Ronconi L., Facoetti A., Bulf H., Franchin L., Bettoni R., Valenza E. Paternal autistic traits are predictive of infants visual attention. J. Autism Dev. Disord. 2014;44:1556–1564. doi: 10.1007/s10803-013-2018-1.
    1. Franceschini S., Bertoni S., Gianesini T., Gori S., Facoetti A. A different vision of dyslexia: Local precedence on global perception. Sci. Rep. 2017;7:17462. doi: 10.1038/s41598-017-17626-1.
    1. de Schotten M.T., Dell’Acqua F., Forkel S.J., Simmons A., Vergani F., Murphy D.G., Catani M.A. Lateralized brain network for visuospatial attention. Nat. Neurosci. 2011;14:1245–1246. doi: 10.1038/nn.2905.
    1. Fink G.R., Halligan P.W., Marshall J.C., Frith C.D., Frackowiak R.S., Dolan R.J. Where in the brain does visual attention select the forest and the trees? Nature. 1996;382:626–628. doi: 10.1038/382626a0.
    1. Sergent J. The cerebral balance of power: Confrontation or cooperation? J. Exp. Psychol. Hum. Percept. Perform. 1982;8:253–272. doi: 10.1037/0096-1523.8.2.253.
    1. Hoeft F., McCandliss B.D., Black J.M., Gantman A., Zakerani N., Hulme C., Lyytinen H., Whitfield-Gabrieli S., Glover G.H., Reiss A.L., et al. Neural systems predicting long-term outcome in dyslexia. Proc. Natl. Acad. Sci. USA. 2011;108:361–366. doi: 10.1073/pnas.1008950108.
    1. Maisog J.M., Einbinder E.R., Flowers D.L., Turkeltaub P.E., Eden G.F. A meta-analysis of functional neuroimaging studies of dyslexia. Ann. N. Y. Acad. Sci. 2008;1145:237–259. doi: 10.1196/annals.1416.024.
    1. Vandermosten M., Hoeft F., Norton E.S. Integrating MRI brain imaging studies of pre-reading children with current theories of developmental dyslexia: A review and quantitative meta-analysis. Curr. Opin. Behav. Sci. 2016;10:155–161. doi: 10.1016/j.cobeha.2016.06.007.
    1. Sireteanu R., Goertz R., Bachert I., Wandert T. Children with developmental dyslexia show a left visual “minineglect”. Vis. Res. 2005;45:3075–3082. doi: 10.1016/j.visres.2005.07.030.
    1. Hancock R., Pugh K.R., Hoeft F. Neural Noise Hypothesis of Developmental Dyslexia. Trends Cogn. Sci. 2017;21:434–448. doi: 10.1016/j.tics.2017.03.008.
    1. Pugh K.R., Frost S.J., Rothman D.L., Hoeft F., Del Tufo S.N., Mason G.F., Molfese P.J., Mencl W.E., Grigorenko E.L., Landi N., et al. Glutamate and choline levels predict individual differences in reading ability in emergent readers. J. Neurosci. 2014;34:4082–4089. doi: 10.1523/JNEUROSCI.3907-13.2014.
    1. Vigneau M., Beaucousin V., Hervé P.Y., Jobard G., Petit L., Crivello F., Mellet E., Zago L., Mazoyer B., Tzourio-Mazoyer N. What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis. NeuroImage. 2011;54:577–593. doi: 10.1016/j.neuroimage.2010.07.036.
    1. Chen Q., Marshall J.C., Weidner R., Fink G.R. Zooming in and zooming out of the attentional focus: An FMRI study. Cereb. Cortex. 2009;19:805–819. doi: 10.1093/cercor/bhn128.
    1. Masuda F., Nakajima S., Miyazaki T., Kazunari Yoshida K., Tsugawa S., Wada M., Ogyu K., Croarkin P.E., Blumberger D.M., Daskalakis Z.J., et al. Motor cortex excitability and inhibitory imbalance in autism spectrum disorder assessed with transcranial magnetic stimulation: A systematic review. Transl. Psychiatry. 2019;9:110. doi: 10.1038/s41398-019-0444-3.

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