Parietotemporal Stimulation Affects Acquisition of Novel Grapheme-Phoneme Mappings in Adult Readers

Jessica W Younger, James R Booth, Jessica W Younger, James R Booth

Abstract

Neuroimaging work from developmental and reading intervention research has suggested a cause of reading failure may be lack of engagement of parietotemporal cortex during initial acquisition of grapheme-phoneme (letter-sound) mappings. Parietotemporal activation increases following grapheme-phoneme learning and successful reading intervention. Further, stimulation of parietotemporal cortex improves reading skill in lower ability adults. However, it is unclear whether these improvements following stimulation are due to enhanced grapheme-phoneme mapping abilities. To test this hypothesis, we used transcranial direct current stimulation (tDCS) to manipulate parietotemporal function in adult readers as they learned a novel artificial orthography with new grapheme-phoneme mappings. Participants received real or sham stimulation to the left inferior parietal lobe (L IPL) for 20 min before training. They received explicit training over the course of 3 days on 10 novel words each day. Learning of the artificial orthography was assessed at a pre-training baseline session, the end of each of the three training sessions, an immediate post-training session and a delayed post-training session about 4 weeks after training. Stimulation interacted with baseline reading skill to affect learning of trained words and transfer to untrained words. Lower skill readers showed better acquisition, whereas higher skill readers showed worse acquisition, when training was paired with real stimulation, as compared to readers who received sham stimulation. However, readers of all skill levels showed better maintenance of trained material following parietotemporal stimulation, indicating a differential effect of stimulation on initial learning and consolidation. Overall, these results indicate that parietotemporal stimulation can enhance learning of new grapheme-phoneme relationships in readers with lower reading skill. Yet, while parietotemporal function is critical to new learning, its role in continued reading improvement likely changes as readers progress in skill.

Keywords: artificial orthography; parietotemporal cortex; reading acquisition; reading skill; transcranial direct current stimulation.

Figures

Figure 1
Figure 1
Depiction of the training procedures.
Figure 2
Figure 2
Illustration of training trial.
Figure 3
Figure 3
Model estimated training (A) and retention (B) slopes for trained words. During training (A), low skill readers (blue) benefitted from real stimulation (solid), showing steeper learning curves compared to those who received sham stimulation (dashed). High skill readers (red), showed less training related gains following stimulation (solid) compared to those who received sham stimulation (dashed). During retention (B), those who received real stimulation (solid) showed less forgetting compared to those who received sham stimulation (dashed). Plots reflect the model estimated performance for an 18-year-old male with average intelligence (reflecting mean centered scores of 0) at two standard deviations below (low) and above (high) group mean reading skill.
Figure 4
Figure 4
Model estimated training (A) and retention (B) slopes for transfer words. During training (A), low skill readers (blue) who received real stimulation (solid) showed steeper learning curves for transfer to novel words compared to those who received sham stimulation (dashed). High skill readers (red) were less able to transfer letter knowledge to newly learned words following stimulation (solid) compared to those who received sham stimulation (dashed). During retention (B), high skill readers regardless of stimulation group (red) showed less decline in transfer compared to low skill readers (blue) who show a decrease in transfer. Plots reflect the model estimated performance for an 18-year-old male with average intelligence (reflecting mean centered scores of 0) at two standard deviations below (low) and above (high) group mean reading skill.

References

    1. Alonzoa A., Brassila J., Taylor J. L., Martin D., Loo C. K. (2012). Daily transcranial direct current stimulation (tDCS) leads to greater increases in cortical excitability than second daily transcranial direct current stimulation. Brain Stimul. 5, 208–213. 10.1016/j.brs.2011.04.006
    1. Antal A., Terney D., Poreisz C., Paulus W. (2007). Towards unravelling task-related modulations of neuroplastic changes induced in the human motor cortex. Eur. J. Neurosci. 26, 2687–2691. 10.1111/j.1460-9568.2007.05896.x
    1. Antonenko D., Külzow N., Sousa A., Prehn K., Grittner U., Flöel A. (2018). Neuronal and behavioral effects of multi-day brain stimulation and memory training. Neurobiol. Aging 61, 245–254. 10.1016/j.neurobiolaging.2017.09.017
    1. Au J., Katz B., Buschkuehl M., Bunarjo K., Senger T., Zabel C., et al. . (2016). Enhancing working memory training with transcranial direct current stimulation. J. Cogn. Neurosci. 28, 1419–1432. 10.1162/jocn_a_00979
    1. Benwell C. S. Y., Learmonth G., Miniussi C., Harvey M., Thut G. (2015). Non-linear effects of transcranial direct current stimulation as a function of individual baseline performance: evidence from biparietal tDCS influence on lateralized attention bias. Cortex 69, 152–165. 10.1016/j.cortex.2015.05.007
    1. Berryhill M. E. (2017). Longitudinal tDCS: consistency across working memory training studies. AIMS Neurosci. 4, 71–86. 10.3934/neuroscience.2017.2.71
    1. Bestmann S., de Berker A. O., Bonaiuto J. (2015). Understanding the behavioural consequences of noninvasive brain stimulation. Trends Cogn. Sci. 19, 13–20. 10.1016/j.tics.2014.10.003
    1. Bikson M., Datta A., Elwassif M. (2009). Establishing safety limits for transcranial direct current stimulation. Clin. Neurophysiol. 120, 1033–1034. 10.1016/j.clinph.2009.03.018
    1. Bikson M., Name A., Rahman A. (2013). Origins of specificity during tDCS: anatomical, activity-selective, and input-bias mechanisms. Front. Hum. Neurosci. 7:688. 10.3389/fnhum.2013.00688
    1. Bitan T., Manor D., Morocz I. A., Karni A. (2005). Effects of alphabeticality, practice and type of instruction on reading an artificial script: an fMRI study. Cogn. Brain Res. 25, 90–106. 10.1016/j.cogbrainres.2005.04.014
    1. Blau V., Reithler J., van Atteveldt N., Seitz J., Gerretsen P., Goebel R., 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, 868–879. 10.1093/brain/awp308
    1. Blomert L. (2011). The neural signature of orthographic-phonological binding in successful and failing reading development. Neuroimage 57, 695–703. 10.1016/j.neuroimage.2010.11.003
    1. Bosse M.-L., Tainturier M. J., Valdois S. (2007). Developmental dyslexia: the visual attention span deficit hypothesis. Cognition 104, 198–230. 10.1016/j.cognition.2006.05.009
    1. Brennan C., Booth J. R. (2015). Large grain instruction and phonological awareness skill influence rime sensitivity, processing speed and early decoding skill in adult L2 learners. Read. Writ. 28, 917–938. 10.1007/s11145-015-9555-2
    1. Callan A. M., Callan D. E., Masaki S. (2005). When meaningless symbols become letters: neural activity change in learning new phonograms. Neuroimage 28, 553–562. 10.1016/j.neuroimage.2005.06.031
    1. Cao F., Rickles B., Vu M., Zhu Z., Chan D. H. L., Harris L. N., et al. . (2013). Early stage visual-orthographic processes predict long-term retention of word form and meaning: a visual encoding training study. J. Neurolinguistics 26, 440–461. 10.1016/j.jneuroling.2013.01.003
    1. Choe J., Coffman B. A., Bergstedt D. T., Ziegler M. D., Phillips M. E. (2016). Transcranial direct current stimulation modulates neuronal activity and learning in pilot training. Front. Hum. Neurosci. 10:34. 10.3389/fnhum.2016.00034
    1. Costanzo F., Varuzza C., Rossi S., Sdoia S., Varvara P., Oliveri M., et al. . (2016a). Reading changes in children and adolescents with dyslexia after transcranial direct current stimulation. Neuroreport 27, 295–300. 10.1097/WNR.0000000000000536
    1. Costanzo F., Varuzza C., Rossi S., Sdoia S., Varvara P., Oliveri M., et al. . (2016b). Evidence for reading improvement following tDCS treatment in children and adolescents with Dyslexia. Restor. Neurol. Neurosci. 34, 215–226. 10.3233/RNN-150561
    1. Deng Y., Booth J. R., Chou T.-L., Ding G.-S., Peng D.-L. (2008). Item-specific and generalization effects on brain activation when learning Chinese characters. Neuropsychologia 46, 1864–1876. 10.1016/j.neuropsychologia.2007.09.010
    1. Eden G. F., Jones K. M., Cappell K., Gareau L., Wood F. B., Zeffiro T. A., et al. . (2004). Neural changes following remediation in adult developmental dyslexia. Neuron 44, 411–422. 10.1016/j.neuron.2004.10.019
    1. Gabrieli J. D. E., Norton E. S. (2012). Reading abilities: importance of visual-spatial attention. Curr. Biol. 22, R298–R299. 10.1016/j.cub.2012.03.041
    1. Gerber P. J. (2012). The impact of learning disabilities on adulthood: a review of the evidenced-based literature for research and practice in adult education. J. Learn. Disabil. 45, 31–46. 10.1177/0022219411426858
    1. Gill J., Shah-Basak P. P., Hamilton R. (2015). It’s the thought that counts: examining the task-dependent effects of transcranial direct current stimulation on executive function. Brain Stimul. 8, 253–259. 10.1016/j.brs.2014.10.018
    1. Harm M. W., Seidenberg M. S. (1999). Phonology, reading acquisition, and dyslexia: insights from connectionist models. Psychol. Rev. 106, 491–528. 10.1037//0033-295x.106.3.491
    1. Harm M. W., Seidenberg M. S. (2004). Computing the meanings of words in reading: cooperative division of labor between visual and phonological processes. Psychol. Rev. 111, 662–720. 10.1037/0033-295x.111.3.662
    1. Hashimoto R., Sakai K. L. (2004). Learning letters in adulthood. Neuron 42, 311–322. 10.1016/s0896-6273(04)00196-5
    1. Heim S., Pape-Neumann J., van Ermingen-Marbach M., Brinkhaus M., Grande M. (2015). Shared vs. specific brain activation changes in dyslexia after training of phonology, attention, or reading. Brain Struct. Funct. 220, 2191–2207. 10.1007/s00429-014-0784-y
    1. Herwig U., Satrapi P., Schönfeldt-Lecuona C. (2003). Using the international 10–20 EEG system for positioning of transcranial magnetic stimulation. Brain Topogr. 16, 95–99. 10.1023/b:brat.0000006333.93597.9d
    1. Hill A. T., Fitzgerald P. B., Hoy K. E. (2016). Effects of anodal transcranial direct current stimulation on working memory: a systematic review and meta-analysis of Findings From Healthy and neuropsychiatric populations. Brain Stimul. 9, 197–208. 10.1016/j.brs.2015.10.006
    1. Hirshorn E. A., Wrencher A., Durisko C., Moore M. W., Fiez J. A. (2016). Fusiform gyrus laterality in writing systems with different mapping principles: an artificial orthography training study. J. Cogn. Neurosci. 28, 882–894. 10.1162/jocn_a_00940
    1. Hooper D., Coughlan J., Mullen M. (2008). Structural equation modelling: guidelines for determining model fit. Electron. J. Bus. Res. Methods 6, 53–60.
    1. Horvath J. C., Carter O., Forte J. D. (2016). No significant effect of transcranial direct current stimulation (tDCS) found on simple motor reaction time comparing 15 different simulation protocols. Neuropsychologia 91, 544–552. 10.1016/j.neuropsychologia.2016.09.017
    1. Horvath J. C., Forte J. D., Carter O. (2015). Quantitative review finds no evidence of cognitive effects in healthy populations from single-session transcranial direct current stimulation (tDCS). Brain Stimul. 8, 535–550. 10.1016/j.brs.2015.01.400
    1. Hsu T.-Y., Juan C.-H., Tseng P. (2016). Individual differences and state-dependent responses in transcranial direct current stimulation. Front. Hum. Neurosci. 10:643. 10.3389/fnhum.2016.00643
    1. Iyer M. B., Mattu U., Grafman J., Lomarev M., Sato S., Wassermann E. M. (2005). Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64, 872–875. 10.1212/01.WNL.0000152986.07469.e9
    1. Jacobson L., Koslowsky M., Lavidor M. (2012). tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp. Brain Res. 216, 1–10. 10.1007/s00221-011-2891-9
    1. Katz B., Au J., Buschkuehl M., Abagis T., Zabel C., Jaeggi S. M., et al. . (2017). Individual differences and long-term consequences of tDCS-augmented Cognitive Training. J. Cogn. Neurosci. 29, 1498–1508. 10.1162/jocn_a_01115
    1. Kenny D. A., Kaniskan B., McCoach D. B. (2015). The performance of RMSEA in models with small degrees of freedom. Soc. Methods Res. 44, 486–507. 10.1177/0049124114543236
    1. Levy J., Pernet C., Treserras S., Boulanouar K., Aubry F., Démonet J. F., et al. . (2009). Testing for the dual-route cascade reading model in the brain: an fMRI effective connectivity account of an efficient reading style. PLoS One 4:e6675. 10.1371/journal.pone.0006675
    1. López-Barroso D., Catani M., Ripollés P., Dell’Acqua F., Rodríguez-Fornells A., de Diego-Balaguer R. (2013). Word learning is mediated by the left arcuate fasciculus. Proc. Natl. Acad. Sci. U S A 110, 13168–13173. 10.1073/pnas.1301696110
    1. Martin D. M., Liu R., Alonzo A., Green M., Loo C. K. (2014). Use of transcranial direct current stimulation (tDCS) to enhance cognitive training: effect of timing of stimulation. Exp. Brain Res. 232, 3345–3351. 10.1007/s00221-014-4022-x
    1. McArdle J. J., Nesselroade J. R. (2003). “Growth curve analysis in contemporary psychological research,” in Handbook of Psychology, (Vol. 2) eds Schinka J., Velicer W. (Hoboken, NJ: John Wiley & Sons, Inc.), 447–480.
    1. Mei L., Xue G., Lu Z.-L., He Q., Zhang M., Wei M., et al. . (2014). Artificial language training reveals the neural substrates underlying addressed and assembled phonologies. PLoS One 9:e93548. 10.1371/journal.pone.0093548
    1. Minamoto T., Azuma M., Yaoi K., Ashizuka A., Mima T., Osaka M., et al. . (2014). The anodal tDCS over the left posterior parietal cortex enhances attention toward a focus word in a sentence. Front. Hum. Neurosci. 8:992. 10.3389/fnhum.2014.00992
    1. Möller A., Nemmi F., Karlsson K., Klingberg T. (2017). Transcranial electric stimulation can impair gains during working memory training and affects the resting state connectivity. Front. Hum. Neurosci. 11:364. 10.3389/fnhum.2017.00364
    1. Muthén L. K., Muthén B. O. (2012). Mplus User’s Guide. Los Angeles, CA: Muthén & Muthén.
    1. Nitsche M. A., Cohen L. G., Wassermann E. M., Priori A., Lang N., Antal A., et al. . (2008). Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 1, 206–223. 10.1016/j.brs.2008.06.004
    1. Nitsche M. A., Paulus W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 527, 633–639. 10.1111/j.1469-7793.2000.t01-1-00633.x
    1. Nitsche M. A., Paulus W. (2011). Transcranial direct current stimulation—update 2011. Restor. Neurol. Neurosci. 29, 463–492. 10.3233/RNN-2011-0618
    1. Odegard T. N., Ring J., Smith S., Biggan J., Black J. (2008). Differentiating the neural response to intervention in children with developmental dyslexia. Ann. Dyslexia 58, 1–14. 10.1007/s11881-008-0014-5
    1. Park C.-H., Chang W. H., Park J.-Y., Shin Y.-I., Kim S. T., Kim Y.-H. (2013). Transcranial direct current stimulation increases resting state interhemispheric connectivity. Neurosci. Lett. 539, 7–10. 10.1016/j.neulet.2013.01.047
    1. Pugh K. R., Mencl W. E., Jenner A. R., Katz L., Frost S. J., Lee J. R., et al. . (2001). Neurobiological studies of reading and reading disability. J. Commun. Disord. 34, 479–492. 10.1016/S0021-9924(01)00060-0
    1. Raschle N. M., Chang M., Gaab N. (2011). Structural brain alterations associated with dyslexia predate reading onset. Neuroimage 57, 742–749. 10.1016/j.neuroimage.2010.09.055
    1. Raschle N. M., Zuk J., Gaab N. (2012). Functional characteristics of developmental dyslexia in left-hemispheric posterior brain regions predate reading onset. Proc. Natl. Acad. Sci. U S A 109, 2156–2161. 10.1073/pnas.1107721109
    1. Reis J., Fischer J. T., Prichard G., Weiller C., Cohen L. G., Fritsch B. (2015). Time- but not sleep-dependent consolidation of tDCS-enhanced visuomotor skills. Cereb. Cortex 25, 109–117. 10.1093/cercor/bht208
    1. Reis J., Schambra H. M., Cohen L. G., Buch E. R., Fritsch B., Zarahn E., et al. . (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci. U S A 106, 1590–1595. 10.1073/pnas.0805413106
    1. Rezaie R., Simos P. G., Fletcher J. M., Cirino P. T., Vaughn S., Papanicolaou A. C. (2011a). Engagement of temporal lobe regions predicts response to educational interventions in adolescent struggling readers. Dev. Neuropsychol. 36, 869–888. 10.1080/87565641.2011.606404
    1. Rezaie R., Simos P. G., Fletcher J. M., Cirino P. T., Vaughn S., Papanicolaou A. C. (2011b). Temporo-parietal brain activity as a longitudinal predictor of response to educational interventions among middle school struggling readers. J. Int. Neuropsychol. Soc. 17, 875–885. 10.1017/s1355617711000890
    1. Richardson F. M., Thomas M. S. C., Filippi R., Harth H., Price C. J. (2010). Contrasting effects of vocabulary knowledge on temporal and parietal brain structure across lifespan. J. Cogn. Neurosci. 22, 943–954. 10.1162/jocn.2009.21238
    1. Richlan F. (2014). Functional neuroanatomy of developmental dyslexia: the role of orthographic depth. Front. Hum. Neurosci. 8:347. 10.3389/fnhum.2014.00347
    1. Richlan F., Kronbichler M., Wimmer H. (2011). Meta-analyzing brain dysfunctions in dyslexic children and adults. Neuroimage 56, 1735–1742. 10.1016/j.neuroimage.2011.02.040
    1. Sandrini M., Fertonani A., Cohen L. G., Miniussi C. (2012). Double dissociation of working memory load effects induced by bilateral parietal modulation. Neuropsychologia 50, 396–402. 10.1016/j.neuropsychologia.2011.12.011
    1. Schlaggar B. L., McCandliss B. D. (2007). Development of neural systems for reading. Annu. Rev. Neurosci. 30, 475–503. 10.1146/annurev.neuro.28.061604.135645
    1. Seidenberg M. S. (2005). Connectionist models of word reading. Curr. Dir. Psychol. Sci. 14, 238–242. 10.1111/j.0963-7214.2005.00372.x
    1. Shaywitz B. A., Shaywitz S. E., Blachman B. A., Pugh K. R., Fulbright R. K., Skudlarski P., et al. . (2004). Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention. Biol. Psychiatry 55, 926–933. 10.1016/j.biopsych.2003.12.019
    1. Shaywitz S. E., Shaywitz B. A. (2005). Dyslexia (specific reading disability). Biol. Psychiatry 57, 1301–1309. 10.1016/j.biopsych.2005.01.043
    1. Shaywitz S. E., Shaywitz B. A. (2008). Paying attention to reading: the neurobiology of reading and dyslexia. Dev. Psychopathol. 20, 1329–1349. 10.1017/S0954579408000631
    1. Shaywitz S. E., Shaywitz B. A., Fulbright R. K., Skudlarski P., Mencl W. E., Constable R. T., et al. . (2003). Neural systems for compensation and persistence: young adult outcome of childhood reading disability. Biol. Psychiatry 54, 25–33. 10.1016/s0006-3223(02)01836-x
    1. Siegel L. S. (2006). Perspectives on dyslexia. Paediatr. Child Health 11, 581–587. 10.1093/pch/11.9.581
    1. Simos P. G., Fletcher J. M., Bergman E., Breier J. I., Foorman B. R., Castillo E. M., et al. . (2002). Dyslexia-specific brain activation profile becomes normal following successful remedial training. Neurology 58, 1203–1213. 10.1212/WNL.58.8.1203
    1. Simos P. G., Fletcher J. M., Sarkari S., Billingsley R. L., Denton C., Papanicolaou A. C. (2007). Altering the brain circuits for reading through intervention: a magnetic source imaging study. Neuropsychology 21, 485–496. 10.1037/0894-4105.21.4.485
    1. Specht K., Hugdahl K., Ofte S., Nygård M., Bjørnerud A., Plante E., et al. . (2009). Brain activation on pre-reading tasks reveals at-risk status for dyslexia in 6-year-old children. Scand. J. Psychol. 50, 79–91. 10.1111/j.1467-9450.2008.00688.x
    1. Stagg C. J., Nitsche M. A. (2011). Physiological basis of transcranial direct current stimulation. Neuroscientist 17, 37–53. 10.1177/1073858410386614
    1. Takashima A., Wagensveld B., van Turennout M., Zwitserlood P., Hagoort P., Verhoeven L. (2014). Training-induced neural plasticity in visual-word decoding and the role of syllables. Neuropsychologia 61, 299–314. 10.1016/j.neuropsychologia.2014.06.017
    1. Taylor J. S. H., Davis M. H., Rastle K. (2017). Comparing and validating methods of reading instruction using behavioural and neural findings in an artificial orthography. J. Exp. Psychol. Gen. 146, 826–858. 10.1037/xge0000301
    1. Thomson J. M., Doruk D., Mascio B., Fregni F., Cerruti C. (2015). Transcranial direct current stimulation modulates efficiency of reading processes. Front. Hum. Neurosci. 9:114. 10.3389/fnhum.2015.00114
    1. Torgesen J., Wagner R., Rashotte C. (1999). Test of Word Reading Efficiency (TOWRE). Austin, TX: Pro-Ed.
    1. Trumbo M. C., Matzen L. E., Coffman B. A., Hunter M. A., Jones A. P., Robinson C. S. H., et al. . (2016). Enhanced working memory performance via transcranial direct current stimulation: the possibility of near and far transfer. Neuropsychologia 93, 85–96. 10.1016/j.neuropsychologia.2016.10.011
    1. Tseng P., Hsu T.-Y., Chang C.-F., Tzeng O. J. L., Hung D. L., Muggleton N. G., et al. . (2012). Unleashing potential: transcranial direct current stimulation over the right posterior parietal cortex improves change detection in low-performing individuals. J. Neurosci. 32, 10554–10561. 10.1523/JNEUROSCI.0362-12.2012
    1. Turi Z., Paulus W., Antal A. (2012). Functional neuroimaging and transcranial electrical stimulation. Clin. EEG Neurosci. 43, 200–208. 10.1177/1550059412444978
    1. Turkeltaub P. E., Benson J., Hamilton R. H., Datta A., Bikson M., Coslett H. B. (2012). Left lateralizing transcranial direct current stimulation improves reading efficiency. Brain Stimul. 5, 201–207. 10.1016/j.brs.2011.04.002
    1. Vandermosten M., Hoeft F., Norton E. S. (2016). How MRI brain imaging studies of pre-reading children inform theories of the etiology of developmental dyslexia and educational practice. Curr. Opin. Behav. Sci. 10, 155–161. 10.1016/j.cobeha.2016.06.007
    1. Vidyasagar T. R., Pammer K. (2010). Dyslexia: a deficit in visuo-spatial attention, not in phonological processing. Trends Cogn. Sci. 14, 57–63. 10.1016/j.tics.2009.12.003
    1. Wechsler D. (1999). Wechsler Adult Abbreviated Intelligence Scale-Fourth Edition (WAIS-IV). San Antonio, TX: NCS Pearson.
    1. Wechsler D. (2008). Wechsler Adult Intelligence Scale-Fourth Edition (WAIS-IV). San Antonio, TX: NCS Pearson.
    1. Westwood S. J., Romani C. (2017). Transcranial direct current stimulation (tDCS) modulation of picture naming and word reading: a meta-analysis of single session tDCS applied to healthy participants. Neuropsychologia 104, 234–249. 10.1016/j.neuropsychologia.2017.07.031
    1. Wiethoff S., Hamada M., Rothwell J. C. (2014). Variability in response to transcranial direct current stimulation of the motor cortex. Brain Stimul. 7, 468–475. 10.1016/j.brs.2014.02.003
    1. Wong P. C. M., Perrachione T. K., Parrish T. B. (2007). Neural characteristics of successful and less successful speech and word learning in adults. Hum. Brain Mapp. 28, 995–1006. 10.1002/hbm.20330
    1. Woodcock R., McGrew K., Schrank F., Mather N. (2007). Woodcock-Johnson III Normative Update. Rolling Meadows: Riverside.
    1. Xue G., Chen C., Jin Z., Dong Q. (2006). Cerebral asymmetry in the fusiform areas predicted the efficiency of learning a new writing system. J. Cogn. Neurosci. 18, 923–931. 10.1162/jocn.2006.18.6.923
    1. Yamada Y., Stevens C., Dow M., Harn B. A., Chard D. J., Neville H. J. (2011). Emergence of the neural network for reading in five-year-old beginning readers of different levels of pre-literacy abilities: an fMRI study. Neuroimage 57, 704–713. 10.1016/j.neuroimage.2010.10.057
    1. Yeatman J. D., Rauschecker A. M., Wandell B. A. (2013). Anatomy of the visual word form area: adjacent cortical circuits and long-range white matter connections. Brain Lang. 125, 146–155. 10.1016/j.bandl.2012.04.010
    1. Yoncheva Y. N., Blau V. C., Maurer U., McCandliss B. D. (2010). Attentional focus during learning impacts N170 ERP responses to an artificial script. Dev. Neuropsychol. 35, 423–445. 10.1080/87565641.2010.480918
    1. Yoncheva Y. N., Wise J., McCandliss B. (2015). Hemispheric specialization for visual words is shaped by attention to sublexical units during initial learning. Brain Lang. 145–146C, 23–33. 10.1016/j.bandl.2015.04.001
    1. Younger J. W., Randazzo Wagner M., Booth J. R. (2016). Weighing the cost and benefit of transcranial direct current stimulation on different reading subskills. Front. Neurosci. 10:262. 10.3389/fnins.2016.00262

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren