Effects of a short and intensive transcranial direct current stimulation treatment in children and adolescents with developmental dyslexia: A crossover clinical trial

Andrea Battisti, Giulia Lazzaro, Floriana Costanzo, Cristiana Varuzza, Serena Rossi, Stefano Vicari, Deny Menghini, Andrea Battisti, Giulia Lazzaro, Floriana Costanzo, Cristiana Varuzza, Serena Rossi, Stefano Vicari, Deny Menghini

Abstract

Developmental Dyslexia (DD) significantly interferes with children's academic, personal, social, and emotional functioning. Nevertheless, therapeutic options need to be further validated and tested in randomized controlled clinical trials. The use of transcranial direct current stimulation (tDCS) has been gaining ground in recent years as a new intervention option for DD. However, there are still open questions regarding the most suitable tDCS protocol for young people with DD. The current crossover study tested the effectiveness of a short and intensive tDCS protocol, including the long-term effects, as well as the influence of age and neuropsychological processes at baseline on reading improvements. Twenty-four children and adolescents with DD were randomly assigned to receive active tDCS during the first slot and sham tDCS during the second slot or vice versa. Five consecutive daily sessions of left anodal/right cathodal tDCS set at 1 mA for 20 min were administered over the parieto-occipital regions. Reading measures (text, high frequency word, low frequency word, and non-word lists) and neuropsychological measures (visual-spatial and verbal working memory, phoneme blending, and rapid automatized naming tasks) were collected before, immediately after, 1 week and 1 month later the treatment. Our results showed that only the active tDCS condition improved non-word reading speed immediately after and 1 month later the end of the treatment compared with baseline. In addition, the improvement in non-word reading speed was significantly correlated with age and with neuropsychological measures (verbal working memory and phoneme blending) at baseline but only in the active tDCS condition. The current crossover study contributed to enforce previous effects of tDCS, including long-term effects, on non-word reading speed and to understand the effect of age and neuropsychological processes on reading outcomes. Our findings showed that tDCS could be a low-cost and easy-to-implement treatment option with long-term effects for children and adolescents with DD.

Keywords: interventions; neuroplasticity; non-invasive brain stimulation; reading; specific learning disorders.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Battisti, Lazzaro, Costanzo, Varuzza, Rossi, Vicari and Menghini.

Figures

FIGURE 1
FIGURE 1
CONSORT flow diagram of the RCT.
FIGURE 2
FIGURE 2
The crossover design.

References

    1. American Psychiatric Association [APA] (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th Edn. Washington, DC: American Psychiatric Association.
    1. Aro T., Eklund K., Eloranta A.-K., Närhi V., Korhonen E., Ahonen T. (2019). Associations between childhood learning disabilities and adult-age mental health problems, lack of education, and unemployment. J. Learn. Disabil. 52 71–83. 10.1177/0022219418775118
    1. Bandeira I. D., Lins-Silva D. H., Barouh J. L., Faria-Guimarães D., Dorea-Bandeira I., Souza L. S., et al. (2021). Neuroplasticity and non-invasive brain stimulation in the developing brain. Prog. Brain Res. 264 57–89. 10.1016/bs.pbr.2021.04.003
    1. Beneventi H., Tønnessen F. E., Ersland L., Hugdahl K. (2010). Executive working memory processes in dyslexia: Behavioral and fMRI evidence: Working memory deficit in dyslexia. Scand. J. Psychol. 51 192–202. 10.1111/j.1467-9450.2010.00808.x
    1. Boets B., Vandermosten M., Cornelissen P., Wouters J., Ghesquière P. (2011). Coherent motion sensitivity and reading development in the transition from prereading to reading stage: coherent motion sensitivity and Dyslexia. Child Dev. 82 854–869. 10.1111/j.1467-8624.2010.01527.x
    1. Borghini G., Candini M., Filannino C., Hussain M., Walsh V., Romei V., et al. (2018). Alpha oscillations are causally linked to inhibitory abilities in ageing. J. Neurosci. 38 4418–4429. 10.1523/JNEUROSCI.1285-17.2018
    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. Buchanan D., Bogdanowicz T., Khanna N., Lockman-Dufour G., Robaey P., D’Angiulli A. (2021). Systematic review on the safety and tolerability of transcranial direct current stimulation in children and adolescents. Brain Sci. 11:212. 10.3390/brainsci11020212
    1. Cancer A., Antonietti A. (2018). tDCS modulatory effect on reading processes: a review of studies on typical readers and individuals with Dyslexia. Front. Behav. Neurosci. 12:162. 10.3389/fnbeh.2018.00162
    1. Carroll J. M., Maughan B., Goodman R., Meltzer H. (2005). Literacy difficulties and psychiatric disorders: evidence for comorbidity. J. Child Psychol. Psychiat. 46 524–532. 10.1111/j.1469-7610.2004.00366.x
    1. Chow S.-C., Liu J. (2009). Design and Analysis of Bioavailability and Bioequivalence Studies, 3rd ed. Chapman & Hall/CRC biostatistics series. Boca Raton, FL: CRC Press.
    1. Cornoldi C., Candela M. (2015). MT 16-19. Trento: Centro Studi Erickson.
    1. Cornoldi C., Colpo G. (2012). Nuove Prove di lettura MT per la Scuola Secondaria di I Grado. Firenze: Giunti OS.
    1. Cornoldi C., Pra Baldi A., Friso G., Giacomin A., Giofre D., Zaccaria S. (2010). Prove MT Avanzate di Lettura e Matematica 2 per il Biennio Della Scuola Superiore di II Grado. Firenze: Giunti OS.
    1. Costanzo F., Rossi S., Varuzza C., Varvara P., Vicari S., Menghini D. (2019). Long-lasting improvement following tDCS treatment combined with a training for reading in children and adolescents with dyslexia. Neuropsychologia 130 38–43. 10.1016/j.neuropsychologia.2018.03.016
    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. RNN 34 215–226. 10.3233/RNN-150561
    1. de Lima R. F., Salgado-Azoni C. A., Dell’Agli B. A. V., Baptista M. N., Ciasca S. M. (2020). Behavior problems and depressive symptoms in developmental dyslexia: risk assessment in Brazilian students. Clin. Neuropsychiatry 17 141–148. 10.36131/cnfioritieditore20200301
    1. Facoetti A., Trussardi A. N., Ruffino M., Lorusso M. L., Cattaneo C., Galli R., et al. (2010). Multisensory spatial attention deficits are predictive of phonological decoding skills in developmental Dyslexia. J. Cogn. Neurosci. 22 1011–1025. 10.1162/jocn.2009.21232
    1. Finisguerra A., Borgatti R., Urgesi C. (2019). Non-invasive brain stimulation for the rehabilitation of children and adolescents with neurodevelopmental disorders: a systematic review. Front. Psychol. 10:135. 10.3389/fpsyg.2019.00135
    1. Franceschini S., Gori S., Ruffino M., Pedrolli K., Facoetti A. (2012). A causal link between visual spatial attention and reading acquisition. Curr. Biol. 22 814–819. 10.1016/j.cub.2012.03.013
    1. Freitas C., Farzan F., Pascual-Leone A. (2013). Assessing brain plasticity across the lifespan with transcranial magnetic stimulation: why, how, and what is the ultimate goal? Front. Neurosci. 7:42. 10.3389/fnins.2013.00042
    1. Gabrieli J. D. (2009). Dyslexia: a new synergy between education and cognitive neuroscience. Science 325 280–283. 10.1126/science.1171999
    1. Galaburda A., Livingstone M. (1993). Evidence for a magnocellular defect in developmental Dyslexia. Ann. NY Acad. Sci. 682 70–82. 10.1111/j.1749-6632.1993.tb22960.x
    1. Galuschka K., Ise E., Krick K., Schulte-Körne G. (2014). Effectiveness of treatment approaches for children and adolescents with reading disabilities: a meta-analysis of randomized controlled trials. PLoS One 9:e89900. 10.1371/journal.pone.0089900
    1. Gathercole S. E., Alloway T. P., Willis C., Adams A.-M. (2006). Working memory in children with reading disabilities. J. Exp. Child Psychol. 93 265–281. 10.1016/j.jecp.2005.08.003
    1. Gori S., Cecchini P., Bigoni A., Molteni M., Facoetti A. (2014). Magnocellular-dorsal pathway and sub-lexical route in developmental dyslexia. Front. Hum. Neurosci. 8:460. 10.3389/fnhum.2014.00460
    1. Graves W. W., Grabowski T. J., Mehta S., Gupta P. (2008). The left posterior superior temporal Gyrus participates specifically in accessing lexical phonology. J. Cogn. Neurosci. 20 1698–1710. 10.1162/jocn.2008.20113
    1. Hari R., Renvall H. (2001). Impaired processing of rapid stimulus sequences in dyslexia. Trends Cogn. Sci. 5 525–532. 10.1016/S1364-6613(00)01801-5
    1. Hendren R. L., Haft S. L., Black J. M., White N. C., Hoeft F. (2018). Recognizing psychiatric comorbidity with reading disorders. Front. Psychiatry 9:101. 10.3389/fpsyt.2018.00101
    1. Jobard G., Vigneau M., Mazoyer B., Tzourio-Mazoyer N. (2007). Impact of modality and linguistic complexity during reading and listening tasks. NeuroImage 34 784–800. 10.1016/j.neuroimage.2006.06.067
    1. Jones B., Kenward M. G. (2014). Design and Analysis of Cross-Over Trials, Chapman & Hall/CRC Monographs on Statistics and Applied Probability. Boca Raton, FL: CRC Press/Taylor & Francis.
    1. Kevan A., Pammer K. (2008). Visual deficits in pre-readers at familial risk for dyslexia. Vis. Res. 48 2835–2839. 10.1016/j.visres.2008.09.022
    1. Kevan A., Pammer K. (2009). Predicting early reading skills from pre-reading measures of dorsal stream functioning. Neuropsychologia 47 3174–3181. 10.1016/j.neuropsychologia.2009.07.016
    1. Lallier M., Tainturier M.-J., Dering B., Donnadieu S., Valdois S., Thierry G. (2010). Behavioral and ERP evidence for amodal sluggish attentional shifting in developmental dyslexia. Neuropsychologia 48 4125–4135. 10.1016/j.neuropsychologia.2010.09.027
    1. Lazzaro G., Bertoni S., Menghini D., Costanzo F., Franceschini S., Varuzza C., et al. (2021a). Beyond reading modulation: Temporo-Parietal tDCS alters Visuo-Spatial attention and motion perception in Dyslexia. Brain Sci. 11:263. 10.3390/brainsci11020263
    1. Lazzaro G., Costanzo F., Varuzza C., Rossi S., Vicari S., Menghini D. (2021b). Effects of a short, intensive, multi-session tDCS treatment in developmental dyslexia: Preliminary results of a sham-controlled randomized clinical trial. Prog. Brain Res. 264 191–210. 10.1016/bs.pbr.2021.01.015
    1. Lazzaro G., Costanzo F., Varuzza C., Rossi S., De Matteis M. E., Vicari S., et al. (2021c). Individual differences modulate the effects of tDCS on reading in children and adolescents with Dyslexia. Sci. Stud. Read. 25 470–485. 10.1080/10888438.2020.1842413
    1. Lim C.-Y., In J. (2021). Considerations for crossover design in clinical study. Korean J. Anesthesiol. 74 293–299. 10.4097/kja.21165
    1. McArthur G., Sheehan Y., Badcock N. A., Francis D. A., Wang H. C., Kohnen S., et al. (2018). Phonics training for English-speaking poor readers. Cochrane Database Syst. Rev. 11:CD009115. 10.1002/14651858.CD009115.pub3
    1. Mee Bell S., McCallum R. S., Cox E. A. (2003). Toward a research-based assessment of Dyslexia: Using cognitive measures to identify reading disabilities. J. Learn. Disabil. 36 505–516. 10.1177/00222194030360060201
    1. Melby-Lervåg M., Lyster S. A., Hulme C. (2012). Phonological skills and their role in learning to read: a meta-analytic review. Psychol. Bull. 138 322–352. 10.1037/a0026744
    1. Menghini D., Finzi A., Benassi M., Bolzani R., Facoetti A., Giovagnoli S., et al. (2010). Different underlying neurocognitive deficits in developmental dyslexia: A comparative study. Neuropsychologia 48 863–872. 10.1016/j.neuropsychologia.2009.11.003
    1. Menghini D., Finzi A., Carlesimo G. A., Vicari S. (2011). Working memory impairment in children with developmental Dyslexia: Is it just a phonological Deficity? Dev. Neuropsychol. 36 199–213. 10.1080/87565641.2010.549868
    1. Menghini D., Hagberg G. E., Caltagirone C., Petrosini L., Vicari S. (2006). Implicit learning deficits in dyslexic adults: An fMRI study. NeuroImage 33 1218–1226. 10.1016/j.neuroimage.2006.08.024
    1. Mirahadi S. S., Nitsche M. A., Pahlavanzadeh B., Mohamadi R., Ashayeri H., Abolghasemi J. (2022). Reading and phonological awareness improvement accomplished by transcranial direct current stimulation combined with phonological awareness training: A randomized controlled trial. Appl. Neuropsychol. Child 2022:2051144. 10.1080/21622965.2022.2051144
    1. Nicolson R. I., Fawcett A. J. (1990). Automaticity: A new framework for dyslexia research? Cognition 35 159–182.
    1. Nicolson R. I., Fawcett A. J., Dean P. (2001). Developmental dyslexia: The cerebellar deficit hypothesis. Trends Neurosci. 24 508–511.
    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. Peterson R. L., Pennington B. F. (2012). Developmental dyslexia. Lancet 379 1997–2007. 10.1016/S0140-6736(12)60198-6
    1. Raven J. (2008). Coloured Progressive Matrices (CPM). Firenze: Giunti OS.
    1. Raven J. (2009). Standard Progressive Matrices (SPM). Firenze: Giunti OS.
    1. Richlan F. (2020). The functional neuroanatomy of developmental dyslexia across languages and writing systems. Front. Psychol. 11:155. 10.3389/fpsyg.2020.00155
    1. Ridding M. C., Ziemann U. (2010). Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J. Physiol. 588(Pt 13), 2291–2304. 10.1113/jphysiol.2010.190314
    1. Rios D. M., Correia Rios M., Bandeira I. D., Queiros Campbell F., de Carvalho Vaz D., Lucena R. (2018). Impact of transcranial direct current stimulation on reading skills of children and adolescents with Dyslexia. Child Neurol. Open 5:2329048X1879825. 10.1177/2329048X18798255
    1. Roach N. W., Hogben J. H. (2007). Impaired filtering of behaviourally irrelevant visual information in dyslexia. Brain 130 771–785. 10.1093/brain/awl353
    1. Santarnecchi E., Polizzotto N. R., Godone M., Giovannelli F., Feurra M., Matzen L., et al. (2013). Frequency-dependent enhancement of fluid intelligence induced by transcranial oscillatory potentials. Curr. Biol. 23 1449–1453. 10.1016/j.cub.2013.06.022
    1. Sartori G., Job R., Tressoldi P. E. (2007). DDE–2 Batteria per la Valutazione della Dislessia e della Disortografia Evolutiva–2. Firenze: Giunti OS.
    1. Senn S. (2002). “Cross-over trials in clinical research,” in Statistics in practice, 2nd Edn, eds Machin D., Day S., Green S. (New York, NY: Wiley; ).
    1. Shanahan M. A., Pennington B. F., Yerys B. E., Scott A., Boada R., Willcutt E. G., et al. (2006). Processing speed deficits in attention Deficit/Hyperactivity disorder and reading disability. J. Abnorm. Child Psychol. 34 584–601. 10.1007/s10802-006-9037-8
    1. Shaywitz S. E., Gruen J. R., Shaywitz B. A. (2007). Management of Dyslexia, its rationale, and underlying neurobiology. Pediatr. Clin. North Am. 54 609–623. 10.1016/j.pcl.2007.02.013
    1. Stella G., Tintoni C. (2007). Indagine e rilevazione sulle abilità di lettura nelle scuole secondarie di secondo grado. Dislessia 4 271–285.
    1. Toffalini E., Giofrè D., Pastore M., Carretti B., Fraccadori F., Szűcs D. (2021). Dyslexia treatment studies: A systematic review and suggestions on testing treatment efficacy with small effects and small samples. Behav. Res. Methods 53 1954–1972. 10.3758/s13428-021-01549-x
    1. Turker S., Hartwigsen G. (2022). The use of noninvasive brain stimulation techniques to improve reading difficulties in dyslexia: A systematic review. Hum. Brain Mapp. 43 1157–1173. 10.1002/hbm.25700
    1. Varvara P., Varuzza C., Sorrentino A. C. P., Vicari S., Menghini D. (2014). Executive functions in developmental dyslexia. Front. Hum. Neurosci. 8:120. 10.3389/fnhum.2014.00120
    1. Vergallito A., Feroldi S., Pisoni A., Romero Lauro L. J. (2022). Inter-individual variability in tDCS effects: A narrative review on the contribution of stable, variable, and contextual factors. Brain Sci. 12:522. 10.3390/brainsci12050522
    1. Vicari S., Marotta L., Menghini D., Molinari M., Petrosini L. (2003). Implicit learning deficit in children with developmental dyslexia. Neuropsychologia 41 108–114. 10.1016/S0028-3932(02)00082-9
    1. Wang L. (2021). Anxiety and depression among Chinese children with and without reading disabilities. Dyslexia 27 355–372. 10.1002/dys.1691
    1. Wanzek J., Stevens E. A., Williams K. J., Scammacca N., Vaughn S., Sargent K. (2018). Current evidence on the effects of intensive early reading interventions. J. Learn. Disabil. 51 612–624. 10.1177/0022219418775110
    1. Wellek S., Blettner M. (2012). On the proper use of the crossover design in clinical trials. Dtsch. Ärztebl. Int. 109 276–281. 10.3238/arztebl.2012.0276
    1. Willcutt E. G., Pennington B. F., Olson R. K., Chhabildas N., Hulslander J. (2005). Neuropsychological analyses of comorbidity between reading disability and attention deficit Hyperactivity disorder: In search of the common deficit. Dev. Neuropsychol. 27 35–78. 10.1207/s15326942dn2701_3
    1. Wolf R. C., Sambataro F., Lohr C., Steinbrink C., Martin C., Vasic N. (2010). Functional brain network abnormalities during verbal working memory performance in adolescents and young adults with dyslexia. Neuropsychologia 48 309–318. 10.1016/j.neuropsychologia.2009.09.020
    1. Woods A. J., Antal A., Bikson M., Boggio P. S., Brunoni A. R., Celnik P., et al. (2016). A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin. Neurophysiol. 127 1031–1048. 10.1016/j.clinph.2015.11.012
    1. Xiao P., Zhu K., Liu Q., Xie X., Jiang Q., Feng Y., et al. (2022). Association between developmental dyslexia and anxiety/depressive symptoms among children in China: The chain mediating of time spent on homework and stress. J. Affect. Disord. 297 495–501. 10.1016/j.jad.2021.10.120
    1. Yang L., Li C., Li X., Zhai M., An Q., Zhang Y., et al. (2022). Prevalence of developmental Dyslexia in primary school children: A systematic review and meta-analysis. Brain Sci. 12:240. 10.3390/brainsci12020240
    1. Zorzi M., Barbiero C., Facoetti A., Lonciari I., Carrozzi M., Montico M., et al. (2012). Extra-large letter spacing improves reading in dyslexia. Proc. Natl. Acad. Sci. U.S.A. 109 11455–11459. 10.1073/pnas.1205566109
    1. Zweig E., Pylkkänen L. (2009). A visual M170 effect of morphological complexity. Lang. Cogn. Proc. 24 412–439. 10.1080/01690960802180420

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe