Purpose: There is evidence that non-invasive brain stimulation transitorily modulates reading by facilitating the neural pathways underactive in individuals with dyslexia. The study aimed at investigating whether multiple sessions of transcranial direct current stimulation (tDCS) would enhance reading abilities of children and adolescents with dyslexia and whether the effect is long-lasting.
Methods: Eighteen children and adolescents with dyslexia received three 20-minute sessions a week for 6 weeks (18 sessions) of left anodal/right cathodal tDCS set at 1 mA over parieto-temporal regions combined with a cognitive training. The participants were randomly assigned to the active or the sham treatment; reading tasks (text, high and low frequency words, non-words) were used as outcome measures and collected before treatment, after treatment and one month after the end of treatment. The tolerability of tDCS was evaluated.
Results: The active group showed reduced low frequency word reading errors and non-word reading times. These positive effects were stable even one month after the end of treatment. None reported adverse effects.
Conclusions: The study shows preliminary evidence of tDCS feasibility and efficacy in improving non-words and low frequency words reading of children and adolescents with dyslexia and it opens new rehabilitative perspectives for the remediation of dyslexia.
American Psychiatric Association (2013). Diagnostic and Statistical Manual of Mental Disorders (Fifth ed.).Arlington, VA: American Psychiatric Publishing.
2.
AylwardE.H., RichardsT.L., BerningerV.W., NagyW.E., FieldK.M., GrimmeA.C., et al. (2003). Instructional treatment associated with changes in brain activation in children with dyslexia. Neurology, 61(2), 212–219.
3.
BakerJ.M., RordenC., & FridrikssonJ. (2010). Using transcranial direct current stimulation to treat stroke patients with aphasia. Stroke, 41(6), 1229–1236.
4.
BarcaL., BuraniC., & ArduinoL.S. (2002). Word naming times and psycholinguistic norms for Italian nouns. Behavior Research Methods, Instruments & Computers, 34(3), 424–434.
5.
BologniniN., Pascual-LeoneA., & FregniF. (2009). Using non-invasive brain stimulation to augment motor training-induced plasticity. Journal of NeuroEngineering and Rehabilitation, 6, 8. doi: 10.1186/1743-0003-6-8
6.
BologniniN., VallarG., CasatiC., LatifL.A., El-NazerR., WilliamsJ., & FregniF. (2011). Neurophysiological and Behavioral Effects of tDCS Combined With Constraint-Induced Movement Therapy in Poststroke Patients. Neurorehabilitation & Neural Repair, 25(9), 819–829. doi: 10.1177/1545968311411056
7.
BouhaliF., Thiebaut de SchottenM., PinelP., PouponC., ManginJ.F., DehaeneS., & CohenL. (2014). Anatomical connections of the visual word form area. The Journal of Neuroscience, 34(46), 15402–15414. doi: 10.1523/JNEUROSCI.4918-13.2014
8.
BrunoniA.R., AmaderaJ., BerbelB., VolzM.S., RizzerioB.G., & FregniF. (2011). A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. International Journal of Neuropsychopharmacology, 14(8), 1133–1145. doi: 10.1017/S1461145710001690
9.
CalvinoI. (1963), Mvaldo. Torino, Italy: Einaudi.
10.
Cohen KadoshR., SoskicS., IuculanoT., KanaiR., & WalshV. (2010). Modulating neuronal activity produces specific and long-lasting changes in numerical competence. Current Biology, 20(22), 2016–2020. doi: 10.1016/j.cub.2010.10.007
11.
ConnersC.K. (2007). Conners’ Rating Scales-Revised. Italian adaptation by M. Nobile, B. Alberti, & A. Zuddas. Firenze, Italy: Giunti OS.
12.
CornoldiC., & ColpoG. (2012). Nuove Prove di lettura MT per la Scuola Secondaria di I Grado.. Firenze, Italy: Giunti OS.
13.
CornoldiC., Pra BaldiA., FrisoG., GiacominA., GiofrèD., & ZaccariaS. (2010). Prove MT Avanzate di Lettura e Matematica 2 per il biennio della scuola superiore di II grado.Firenze, Italy: Giunti OS.
14.
CostanzoF., MenghiniD., CaltagironeC., OliveriM., & VicariS. (2013). How to improve reading skills in dyslexics: The effect of high frequency rTMS. Neuropsychologia, 51(14), 2953–2959. doi: 10.1016/j.neuropsychologia.2013.10.018
15.
CostanzoF., MenghiniD., CaltagironeC., OliveriM., & VicariS. (2012). High frequency rTMS over the left parietal lobule increases non-word reading accuracy. Neuropsychologia, 50(11), 2645–2651. doi: 10.1016/j.neuropsychologia.2012.07.017
16.
CotelliM., Manenti BrambillaM., PetesiM., RosiniS., FerrariC., & MiniussiC. (2014). Anodal tDCS during face-name associations memory training in Alzheimer’s patients. Frontiers in Aging Neuroscience, 6, 38. doi: 10.3389/fnagi.2014.00038
17.
DattaA., BakerJ.M., BiksonM., & FridrikssonJ. (2011). Individualized model predicts brain current flow during transcranial direct-current stimulation treatment in responsive stroke patient. Brain Stimuation, 4(3), 169–174. doi: 10.1016/j.brs.2010.11.001
18.
DehaeneS., & CohenL. (2011). The unique role of the visual word form area in reading. Trends in Cognitive Sciences, 15(6), 254–262.
19.
DehaeneS., CohenL., SigmanM., & VinckierF. (2005). The neural code for written words: A proposal. Trends in Cognitive Sciences, (7), 335–341.
20.
EckertM. (2004). Neuroanatomical markers for dyslexia: A review of dyslexia structural imaging studies. Neuroscientist, 10(4), 362–371.
21.
EdenG.F., JonesK.M., CappellK., GareauL., WoodF.B., & ZeffiroT.A., et al. (2004). Neural changes following remediation in adult developmental dyslexia. Neuron, 44(3), 411–422.
22.
ElmasryJ., LooC., & MartinD. (2015). A systematic review of transcranial electrical stimulation combined with cognitive training. Restorative Neurology and Neuroscience, 33(3), 263–278. doi: 10.3233/RNN-140473
23.
FerrerE., ShaywitzB.A., HolahanJ.M., MarchioneK., & ShaywitzS.E. (2010). Uncoupling of reading and IQ overtime: Empirical evidence for a definition of dyslexia. Psychological Science, 21(1), 93–101. doi: 10.1177/0956797609354084
FriedmanR.F., WeenJ.E., & AlbertM.L. (1993). Alexia. In HeilmanK.M. & ValensteinE. (eds), Clinical neuropsychology (pp. 37–62). New York, US: Oxford University Press.
26.
FryeR.E., RotenbergA., OusleyM., & Pascual-LeoneA. (2008). Transcranial magnetic stimulation in child neurology: Current and future directions. Journal of Child Neurology, 23(1), 79–96.
27.
GandigaP.C., HummelF.C., & CohenL.G. (2006). Transcranial DC stimulation (tDCS): A tool for doubleblind sham-controlled clinical studies in brain stimulation. Clinical Neuropsychology, 117(4), 845–850.
28.
GravesW., DesaiR., HumpriesC., SeidenbergM.S., & BinderJ.R. (2010). Neural systems for reading aloud: A multiparametric approach. Cerebral Cortex, 20(8), 1799–1815. doi: 10.1093/cercor/bhp245
29.
GreenwaldM. (2001). Acquired reading disorders. In BerndtR. S., GrafmanJ. &
BollerF. (eds.), Handbook of Neuropsychology: Language and Aphasia (pp. 205–220). Amsterdam, Netherlands: Elsevier.
30.
HeleniusP., SalmelinR., ServiceE., & ConnollyJ.F. (1998). Distinct time courses of word and context comprehension in the left temporal cortex. Brain, 121(Pt 6), 1133–1142.
31.
HethI., & LavidorM. (2015). Improved reading measures in adults with dyslexia following transcranial direct current stimulation treatment. Neuropsychologia, 70, 107–113. doi: 10.1016/j.neuropsychologia.2015.02.022.
32.
HoeftF., McCandlissB.D., BlackJ.M., GantmanA., ZakeraniN., HulmeC., et al. (2011). Neural systems predicting long-term outcome in dyslexia. PNAS, Proceedings of the National Academy of Sciences U S A, 108(1), 361–366. doi: 10.1073/pnas.1008950108.
33.
HoeftF., MeylerA., HernandezA., JuelC., Taylor-HillH., MartindaleJ.L., & GabrieliD.E. (2007). Functional and morphometric brain dissociation between dyslexia and reading ability. PNAS, Proceedings of the National Academy of Sciences, 104(10), 4234–4239.
34.
IuculanoT., & Cohen KadoshR. (2014). Preliminary evidence for performance enhancement following parietal lobe stimulation in Developmental Dyscalculia. Frontiers in Human Neuroscience, 8, 38. doi: 10.3389/fnhum.2014.00038
35.
JacobsonL., GorenN., LavidorM., & LevyD.A. (2012). Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory. Brain Research, 23, 66–72. doi: 10.1016/j.brainres.2011.12.036
36.
JobardG., VigneauM., MazoyerB., & Tzourio-MazoyerN. (2007). Impact of modality and linguistic complexity during reading and listening tasks. Neuroimage, 34(2), 784–800.
37.
KrauseB., & Cohen KadoshR. (2013). Can transcranial electrical stimulation improve learning difficulties in atypical brain development? A future possibility for cognitive training. Developmental Cognitive Neuroscience, 6, 176–194. doi: 10.1016/j.dcn.2013.04.001
38.
LoganG.D. (1978). Attention in character classification: Evidence for the automaticity of component stages. Journal of Experimental Psychology: General, 107, 32–63.
39.
McArthurG., EveP.M., JonesK., BanalesE., KohnenS., AnandakumarT., & CastlesA. (2012). Phonics training for English-speaking poor readers. Cochrane Database of Systematic Reviews, 12, CD009115. doi: 10.1002/14651858. CD009115.pub2
40.
MeinzerM., JähnigenS., CoplandD.A., DarkowR., GrittnerU., AvirameK., & FlöelA. (2014). Transcranial direct current stimulation over multiple days improves learning and maintenance of a novel vocabulary. Cortex, 50, 137–147. doi: 10.1016/j.cortex.2013.07.013
41.
MinhasP., BiksonM., WoodsA.J., RosenA.R., & KesslerS.K. (2012). Transcranial direct current stimulation in pediatric brain: A computational modeling study. IEEE Engineering in Medicine and Biology Society Annual Conference, 2012, 859–862. doi: 10.1109/EMBC.2012.6346067
42.
MiniussiC., & RossiniP.M. (2011). Transcranial magnetic stimulation in cognitive rehabilitation. Neuropsychological Rehabilitation, 21(5), 579–601. doi: 10.1080/09602011.2011.562689
43.
OldfieldR.C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113.
44.
PhiliposeL.E., GottesmanR.F., NewhartM., KleinmanJ.T., HerskovitsE.H., PawlakM.A., et al. (2007). Neural regions essential for reading and spelling of words and pseudowords. Annals of Neurology, 62(5), 481–492.
45.
PriceC.J. (2000). The anatomy of language: Contributions from functional neuroimaging. Journal of Anatomy, 197(3), 335–359.
46.
PriceC.J., & MechelliA. (2005). Reading and reading disturbance. Current Opinion in Neurobiology, 15(2), 231–238.
47.
PughK.R., MenclW.E., JennerA.R., KatzL., FrostS.J., LeeJ.R., et al. (2000). Functional neuroimaging studies of reading and reading disability (developmental dyslexia. Mental Retardation and Developmental Disabilities Research Reviews, 6(3), 207–213.
48.
PughK.R., MenclW.E., JennerA.R., KatzL., FrostS.J., LeeJ.R., et al. (2001). Neurobiological studies of reading and reading disability. Journal of Communication Disorders, 34(6), 479–492.
49.
RavenJ.C. (2008a). Coloured progressive matrices. Italian standardization by C. Belacchi, T. C. Scalisi, E. Cannoni, & C. Cornoldi. Firenze, Italy: Giunti OS.
50.
RavenJ.C. (2008b). Standard Progressive Matrices. Firenze, Italy: Giunti OS.
51.
ReisJ., SchambraH.M., CohenL.G., BuchE.R., FritschB., ZarahnE., & KrakauercJ.W. (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. PNAS, Proceedings of the National Academy of Sciences U S A, 106(5), 1590–1595. doi: 10.1073/pnas.0805413106
52.
RichlanF. (2012). Developmental dyslexia: Dysfunction of a left hemisphere reading network. Frontiers in Human Neuroscience, 6, 120. doi: 10.3389/fnhum.2012.00120
53.
RichlanF. (2014). Functional neuroanatomy of developmental dyslexia: The role of orthographic depth. Frontiers in Human Neuroscience, 8, 347. doi: 10.3389/fnhum.2014.00347
54.
SartoriG., JobR., & TressoldiP.E. (2007), DDE-2 Batteria per la Valutazione della Dislessia e della Disortografia Evolutiva-2.
Firenze, Italy: Giunti OS.
55.
SchneiderW., & ShiffrinR.M. (1977). Controlled and automatic human information processing: Detection, search, and attention. Psychol Rev, 84, 1–66.
56.
ShaywitzB.A., ShaywitzS.E., BlachmanB.A., PughK.R., FulbrightR.K., SkudlarskiP., et al. (2004). Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention. Biological Psychiatry, 55(9), 926–933.
57.
ShaywitzB.A., ShaywitzS.E., PughK.R., MenclW.E., FulbrightR.K., SkudlarskiP., et al. (2002). Disruption of posterior brain systems for reading in children with developmental dyslexia. Biological Psychiatry, 52(2), 101–110.
58.
ShaywitzS.E. (1998). Functional disruption in the organization of the brain for reading in dyslexia. PNAS, Proceedings of the National Academy of Sciences U S A, 95(5), 2636–2641.
59.
ShaywitzS.E., & ShaywitzB.A. (2008). Paying attention to reading: The neurobiology of reading and dyslexia. Development and Psychopathology, 20(4), 1329–1349. doi: 10.1017/S0954579408000631
60.
SimosP.G., BreierJ.I., FletcherJ.M., FoormanB.R., CastilloE.M., & PapanicolaouA.C. (2002). Brain mechanisms for reading words and pseudowords: An integrated approach. Cerebral Cortex, 12(3), 297–305.
61.
StaggC.J., & NitscheM.A. (2011). Physiological basis of transcranial direct current stimulation. Neuroscientist, 17(1), 37–53. doi: 10.1177/1073858410386614
62.
StellaG., & TintoniC. (2007). Indagine e rilevazione sulle abilità di lettura nelle scuole secondarie di secondo grado. Dislessia, 4(3), 271–285.
63.
StussD.T. (2011). The future of cognitive neurorehabilitation. Neuropsychological Rehabilitation, 21(5), 755–768. doi: 10.1080/09602011.2011.605590
64.
TempleE., DeutschG.K., PoldrackR.A., MilleriS.L., TallaliP., & MerzenichiM.M., et al. (2003). Neural deficits in children with dyslexia ameliorated by behavioural remediation: Evidence from functional MRI. PNAS, Proceedings of the National Academy of Sciences U S A, 100(5), 2860–2865.
65.
TurkeltaubP.E., BensonJ., HamiltonR.H., DattaA., BiksonM., & CoslettH.B. (2012). Left lateralizing transcranial direct current stimulation improves reading efficiency. Brain Stimulation, 5(3), 201–207. doi: 10.1016/j.brs.2011.04.002
66.
TurkeltaubP.E., EdenG.F., JonesK.M., & ZeffiroT.A. (2002). Meta-analysis of the functional neuroanatomy of single-word reading: Method and validation. Neuroimage, 16(3), 765–780.
67.
TurkeltaubP.E., GareauL., FlowersD.L., ZeffiroT.A., & EdenG.F. (2003). Development of neural mechanisms for reading. Nature Neuroscience, 6(7), 767–773.
68.
ValdoisS., CarbonnelaS., JuphardaA., BaciuaM., AnsaB., & PeyrinaC., et al. (2006). Polysyllabic pseudo-word processing in reading and lexical decision: Converging evidence from behavioral data, connectionist simulations and functional MRI. Brain Research, 1085(1), 149–162.
69.
VicarioC.M., & NitscheM.A. (2013). Non-invasive brain stimulation for the treatment of brain diseases in childhood and adolescence: State of the art, current limits and future challenges. Frontiers in Systems Neuroscience, 7, 94. doi: 10.3389/fnsys.2013.00094
70.
VinckierF., DehaeneS., JobertA., DubusJ.P., SigmanM., & CohenL. (2007). Hierarchical coding of letter strings in the ventral stream: Dissecting the inner organization of the visual word-form system. Neuron, 55(1), 143–156.
71.
VinesB.W., NortonA.C., & SchlaugG. (2011). Non-invasive brain stimulation enhances the effects of melodic intonation therapy. Frontiers in Psychology, 2, 230. doi: 10.3389/fpsyg.2011.00230
72.
WagnerT., FregniF., FecteauS., GrodzinskyA., ZahnM., & Pascual-LeoneA. (2007). Transcranial direct current stimulation: A computer-based human model study. Neuroimage, 35(3), 1113–1124.
73.
YeatmanJ.D., DoughertyR.F., RykhlevskaiaE., SherbondyA.J., DeutschG.K., WandellB.A., & Ben-ShacharM. (2011). Anatomical properties of the arcuate fasciculus predict phonological and reading skills in children. Journal of Cognitive Neuroscience, 23(11), 3304–3317. doi: 10.1162/jocn_a_00061
