Weighing the Cost and Benefit of Transcranial Direct Current Stimulation on Different Reading Subskills

Jessica W Younger, Melissa Randazzo Wagner, James R Booth, Jessica W Younger, Melissa Randazzo Wagner, James R Booth

Abstract

Adults struggling with low reading skills are underserved by limited available treatments. While brain stimulation techniques such as transcranial direct current stimulation (tDCS) has the potential to improve a variety of cognitive functions, little work has been done examining its potential to treat reading disabilities. Research on the effects of tDCS on reading abilities has been somewhat inconsistent perhaps in part due to discrepancies between studies in the nature of the tasks. In the current study, we examined the effect of tDCS to the left inferior parietal lobe (L IPL) on two reading tasks in low-to-average readers. We compared performance on a sight word efficiency (SWE) task and a rhyme judgment task before and after either stimulation to the L IPL, right superior parietal lobe (R SPL), or sham stimulation. Readers who received stimulation to the L IPL showed greater improvements on the SWE task, but less improvement on the rhyme judgment task compared to the R SPL and sham groups. This study demonstrates for the first time both a positive and negative effect of stimulation under the same stimulation parameters within the same participants. The results highlight the need to consider multiple tasks when assessing the potential of using tDCS as a treatment.

Keywords: parietal lobes; reading intervention; rhyming; sight word efficiency; transcranial direct current stimulation.

Figures

Figure 1
Figure 1
Change in Single Word Reading Efficiency pre- and post-stimulation for each group. A significant Group × Time interaction indicates the L IPL group showed significantly greater improvement than the R SPL and Sham groups. Error bars indicate one standard deviation.
Figure 2
Figure 2
Change in Rhyme Judgment performance pre- and post-stimulation for each group. A significant Group × Time interaction indicates the Sham group showed significantly greater improvement than the L IPL and R SPL groups. Error bars indicate one standard deviation.

References

    1. Adlof S. M., Catts H. W., Little T. D. (2006). Should the simple view of reading include a fluency component? Read. Writ. 19, 933–958. 10.1007/s11145-006-9024-z
    1. Ashmore R. A., Farrier M. J., Paulson L. H., Chu X. (2002). The Effects of Phonemic Awareness Drills on Phonological Awareness and Word Reading Performance in a Later Learned Alphabetic Script. Available online at: (Accessed November 12, 2015).
    1. Balota D. A., Yap M. J., Hutchison K. A., Cortese M. J., Kessler B., Loftis B., et al. . (2007). The english lexicon project. Behav. Res. Methods 39, 445–459. 10.3758/BF03193014
    1. Barth A. E., Catts H. W., Anthony J. L. (2009). The component skills underlying reading fluency in adolescent readers: a latent variable analysis. Read. Writ. 22, 567–590. 10.1007/s11145-008-9125-y
    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. Bitan T., Burman D. D., Chou T.-L., Lu D., Cone N. E., Cao F., et al. . (2007a). The interaction between orthographic and phonological information in children: an fMRI study. Hum. Brain Mapp. 28, 880–891. 10.1002/hbm.20313
    1. Bitan T., Cheon J., Lu D., Burman D. D., Gitelman D. R., Mesulam M.-M., et al. . (2007b). Developmental changes in activation and effective connectivity in phonological processing. Neuroimage 38, 564–575. 10.1016/j.neuroimage.2007.07.048
    1. Booth J. R., Burman D. D., Meyer J. R., Gitelman D. R., Parrish T. B., Mesulam M. M. (2003). Relation between brain activation and lexical performance. Hum. Brain Mapp. 19, 155–169. 10.1002/hbm.10111
    1. Booth J. R., Mehdiratta N., Burman D. D., Bitan T. (2008). Developmental increases in effective connectivity to brain regions involved in phonological processing during tasks with orthographic demands. Brain Res. 1189, 78–89. 10.1016/j.brainres.2007.10.080
    1. Cao F., Bitan T., Booth J. R. (2008). Effective brain connectivity in children with reading difficulties during phonological processing. Brain Lang. 107, 91–101. 10.1016/j.bandl.2007.12.009
    1. Cao F., Bitan T., Chou T.-L., Burman D. D., Booth J. R. (2006). Deficient orthographic and phonological representations in children with dyslexia revealed by brain activation patterns. J. Child Psychol. Psychiatry 47, 1041–1050. 10.1111/j.1469-7610.2006.01684.x
    1. Cao F., Brennan C., Booth J. R. (2015). The brain adapts to orthography with experience: evidence from English and Chinese. Dev. Sci. 18, 785–798. 10.1111/desc.12245
    1. Cohen Kadosh R., Dowker A., Heine A., Kaufmann L., Kucian K. (2013). Interventions for improving numerical abilities: present and future. Trends Neurosci. Educ. 2, 85–93. 10.1016/j.tine.2013.04.001
    1. Costanzo F., Menghini D., Caltagirone C., Oliveri M., Vicari S. (2012). High frequency rTMS over the left parietal lobule increases non-word reading accuracy. Neuropsychologia 50, 2645–2651. 10.1016/j.neuropsychologia.2012.07.017
    1. Costanzo F., Menghini D., Caltagirone C., Oliveri M., Vicari S. (2013). How to improve reading skills in dyslexics: the effect of high frequency rTMS. Neuropsychologia 51, 2953–2959. 10.1016/j.neuropsychologia.2013.10.018
    1. De Berker A. O., Bikson M., Bestmann S. (2013). Predicting the behavioral impact of transcranial direct current stimulation: issues and limitations. Front. Hum. Neurosci. 7:613. 10.3389/fnhum.2013.00613
    1. Dubljević V., Saigle V., Racine E. (2014). The rising tide of tDCS in the media and academic literature. Neuron 82, 731–736. 10.1016/j.neuron.2014.05.003
    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. Finn E. S., Shen X., Holahan J. M., Scheinost D., Lacadie C., Papademetris X., et al. . (2014). Disruption of functional networks in dyslexia: a whole-brain, data-driven analysis of connectivity. Biol. Psychiatry 76, 397–404. 10.1016/j.biopsych.2013.08.031
    1. Fregni F., Pascual-Leone A. (2007). Technology insight: noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat. Clin. Pract. Neurol. 3, 383–393. 10.1038/ncpneuro0530
    1. Hashimoto R., Sakai K. L. (2004). Learning letters in adulthood. Neuron 42, 311–322. 10.1016/S0896-6273(04)00196-5
    1. He Q., Xue G., Chen C., Chen C., Lu Z.-L., Dong Q. (2013). Decoding the neuroanatomical basis of reading ability: a multivoxel morphometric study. J. Neurosci. 33, 12835–12843. 10.1523/JNEUROSCI.0449-13.2013
    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. Heth I., Lavidor M. (2015). Improved reading measures in adults with dyslexia following transcranial direct current stimulation treatment. Neuropsychologia 70, 107–113. 10.1016/j.neuropsychologia.2015.02.022
    1. Hoeft F., Hernandez A., McMillon G., Taylor-Hill H., Martindale J. L., Meyler A., et al. . (2006). Neural basis of dyslexia: a comparison between dyslexic and nondyslexic children equated for reading ability. J. Neurosci. 26, 10700–10708. 10.1523/JNEUROSCI.4931-05.2006
    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. Horwitz B., Rumsey J. M., Donohue B. C. (1998). Functional connectivity of the angular gyrus in normal reading and dyslexia. Proc. Natl. Acad. Sci. U.S.A. 95, 8939–8944.
    1. Illingworth S., Bishop D. V. M. (2009). Atypical cerebral lateralisation in adults with compensated developmental dyslexia demonstrated using functional transcranial Doppler ultrasound. Brain Lang. 111, 61–65. 10.1016/j.bandl.2009.05.002
    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. Jobard G., Crivello F., Tzourio-Mazoyer N. (2003). Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. Neuroimage 20, 693–712. 10.1016/S1053-8119(03)00343-4
    1. Johnson M. H. (2001). Functional brain development in humans. Nat. Rev. Neurosci. 2, 475–483. 10.1038/35081509
    1. Jones K. T., Berryhill M. E. (2012). Parietal contributions to visual working memory depend on task difficulty. Front. psychiatry 3:81. 10.3389/fpsyt.2012.00081
    1. Kovelman I., Norton E. S., Christodoulou J. A., Gaab N., Lieberman D. A., Triantafyllou C., et al. . (2012). Brain basis of phonological awareness for spoken language in children and its disruption in dyslexia. Cereb. Cortex 22, 754–764. 10.1093/cercor/bhr094
    1. Koyama M. S., Di Martino A., Zuo X.-N., Kelly C., Mennes M., Jutagir D. R., et al. . (2011). Resting-state functional connectivity indexes reading competence in children and adults. J. Neurosci. 31, 8617–8624. 10.1523/JNEUROSCI.4865-10.2011
    1. Krause B., Cohen Kadosh R. (2013). Can transcranial electrical stimulation improve learning difficulties in atypical brain development? A future possibility for cognitive training. Dev. Cogn. Neurosci. 6, 176–194. 10.1016/j.dcn.2013.04.001
    1. Krause B., Cohen Kadosh R. (2014). Not all brains are created equal: the relevance of individual differences in responsiveness to transcranial electrical stimulation. Front. Syst. Neurosci. 8:25. 10.3389/fnsys.2014.00025
    1. Kucian K., von Aster M. (2015). Developmental dyscalculia. Eur. J. Pediatr. 174, 1–13. 10.1007/s00431-014-2455-7
    1. Maclean M., Bryant P., Bradley L. (1987). Rhymes, nursery rhymes, and reading in early childhood. Merril-Palmer Q. 33, 255–281.
    1. 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, 1963–1981. 10.1002/hbm.22749
    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. Meyler A., Keller T. A., Cherkassky V. L., Gabrieli J. D. E., Just M. A. (2008). Modifying the brain activation of poor readers during sentence comprehension with extended remedial instruction: a longitudinal study of neuroplasticity. Neuropsychologia 46, 2580–2592. 10.1016/j.neuropsychologia.2008.03.012
    1. Milne R. D., Syngeniotis A., Jackson G., Corballis M. C. (2002). Mixed lateralization of phonological assembly in developmental dyslexia. Neurocase 8, 205–209. 10.1093/neucas/8.3.205
    1. Miniussi C., Cappa S. F., Cohen L. G., Floel A., Fregni F., Nitsche M. A., et al. . (2008). Efficacy of repetitive transcranial magnetic stimulation/transcranial direct current stimulation in cognitive neurorehabilitation. Brain Stimul. 1, 326–336. 10.1016/j.brs.2008.07.002
    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. Norton E. S., Beach S. D., de Gabrieli J. (2014). Neurobiology of dyslexia. Curr. Opin. Neurobiol. 30C, 73–78. 10.1016/j.conb.2014.09.007
    1. Park H.-J., Friston K. (2013). Structural and functional brain networks: from connections to cognition. Science 342:1238411. 10.1126/science.1238411
    1. Price A. R., McAdams H., Grossman M., Hamilton R. H. (2015). A meta-analysis of transcranial direct current stimulation studies examining the reliability of effects on language measures. Brain Stimul. 8, 1093–1100. 10.1016/j.brs.2015.06.013
    1. Price C. J., Devlin J. T. (2011). The interactive account of ventral occipitotemporal contributions to reading. Trends Cogn. Sci. 15, 246–253. 10.1016/j.tics.2011.04.001
    1. Price G. R., Ansari D. (2013). Dyscalculia : characteristics, causes, and treatments. Numeracy 6, 1–18. 10.5038/1936-4660.6.1.2
    1. Priori A., Hallett M., Rothwell J. C. (2009). Repetitive transcranial magnetic stimulation or transcranial direct current stimulation? Brain Stimul. 2, 241–245. 10.1016/j.brs.2009.02.004
    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. Pugh K. R., Mencl W. E., Shaywitz B. A., Shaywitz S. E., Fulbright R. K., Constable R., et al. . (2000). The angular gyrus in developmental dyslexia: task-specific differences in functional connectivity within posterior cortex. Psychol. Sci. 11, 51–56. 10.1111/1467-9280.00214
    1. Quaglino V., Bourdin B., Czternasty G., Vrignaud P., Fall S., Meyer M. E., et al. . (2008). Differences in effective connectivity between dyslexic children and normal readers during a pseudoword reading task: an fMRI study. Neurophysiol. Clin. 38, 73–82. 10.1016/j.neucli.2007.12.007
    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. Richlan F., Kronbichler M., Wimmer H. (2009). Functional abnormalities in the dyslexic brain: a quantitative meta-analysis of neuroimaging studies. Hum. Brain Mapp. 30, 3299–3308. 10.1002/hbm.20752
    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. Ridding M. C., Rothwell J. C. (2007). Is there a future for therapeutic use of transcranial magnetic stimulation? Nat. Rev. Neurosci. 8, 559–567. 10.1038/nrn2169
    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. 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. Simon G., Lanoë C., Poirel N., Rossi S., Lubin A., Pineau A., et al. . (2013). Dynamics of the anatomical changes that occur in the brains of schoolchildren as they learn to read. PLoS ONE 8:e81789. 10.1371/journal.pone.0081789
    1. Simos P. G., Breier J. I., Jack M. (2001). Age-related changes in regional brain activation during phonological decoding and printed word recognition. Dev. Neuropsychol. 19, 37–41. 10.1207/S15326942DN1902
    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. Sparing R., Thimm M., Hesse M. D., Küst J., Karbe H., Fink G. R. (2009). Bidirectional alterations of interhemispheric parietal balance by non-invasive cortical stimulation. Brain 132, 3011–3020. 10.1093/brain/awp154
    1. Temple E., Deutsch G. K., Poldrack R. A., Miller S. L., Tallal P., Merzenich M. M., et al. . (2003). Neural deficits in children with dyslexia ameliorated by behavioral remediation: evidence from functional MRI. Proc. Natl. Acad. Sci. U.S.A. 100, 2860–2865. 10.1073/pnas.0030098100
    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). TOWRE–2 Test of Word Reading Efficiency. Austin, TX: Pro-Ed. Available online at: (Accessed January 15, 2016).
    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. Turkeltaub P. E., Gareau L., Flowers D. L., Zeffiro T. A., Eden G. F. (2003). Development of neural mechanisms for reading. Nat. Neurosci. 6, 767–773. 10.1038/nn1065
    1. van der Mark S., Klaver P., Bucher K., Maurer U., Schulz E., Brem S., et al. . (2011). The left occipitotemporal system in reading: disruption of focal fMRI connectivity to left inferior frontal and inferior parietal language areas in children with dyslexia. Neuroimage 54, 2426–2436. 10.1016/j.neuroimage.2010.10.002
    1. Vellutino F. R., Tunmer W. E., Jaccard J. J., Chen R. (2007). Components of reading ability: multivariate evidence for a convergent skills model of reading development. Sci. Stud. Read. 11, 3–32. 10.1080/10888430709336632
    1. Vicario C. M., Nitsche M. A. (2013). Transcranial direct current stimulation: a remediation tool for the treatment of childhood congenital dyslexia? Front. Hum. Neurosci. 7:139. 10.3389/fnhum.2013.00139
    1. Wechsler D. (2008). Wechsler Adult Intelligence Scale–Fourth Edition (WAIS–IV). San Antonio, TX: NCS Pearson; Available : (Accessed January 15, 2016).
    1. Williams J. A., Imamura M., Fregni F. (2009). Updates on the use of non-invasive brain stimulation in physical and rehabilitation medicine. J. Rehabil. Med. 41, 305–311. 10.2340/16501977-0356
    1. Wong I. S. Y., Tsang H. W. H. (2013). A review on the effectiveness of repetitive transcranial magnetic stimulation (rTMS) on post-stroke aphasia. Rev. Neurosci. 24, 105–114. 10.1515/revneuro-2012-0072
    1. Xu M., Yang J., Siok W. T., Tan L. H. (2015). Atypical lateralization of phonological working memory in developmental dyslexia. J. Neurolinguist. 33, 67–77. 10.1016/j.jneuroling.2014.07.004
    1. Zeno S. (1995). The Educator's Word Frequency Guide. Touchstone Applied Science Associates. Available online at: (Accessed January 15, 2016).
    1. Ziegler J. C., Goswami U. (2005). Reading acquisition, developmental dyslexia, and skilled reading across languages: a psycholinguistic grain size theory. Psychol. Bull. 131, 3–29. 10.1037/0033-2909.131.1.3

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