RESEARCH ARTICLE
A Study of Null Effects for the Use of Transcranial
Direct Current Stimulation (tDCS) in Adults With
and Without Reading Impairment
a n o p e n a c c e s s
j o u r n a l
Jacqueline Cummine1,2, Miya Villarena2, Taylor Onysyk1
, and Joseph T. Devlin3
1Communication Sciences and Disorders, University of Alberta, Edmonton, Canada
2Neuroscience and Mental Health Institute, University of Alberta, Edmonton, Canada
3Experimental Psychology, University College London, London, UK
Keywords: brain modulation, reading, dyslexia, tDCS
ABSTRACT
There is evidence to support the hypothesis that the delivery of anodal transcranial direct current
stimulation (tDCS) to the left temporoparietal junction can enhance performance on reading
speed and reading accuracy (Costanzo et al., 2016B; Heth & Lavidor, 2015). Here, we explored
whether we could demonstrate similar effects in adults with and without reading impairments.
Method: Adults with (N = 33) and without (N = 29) reading impairment were randomly assigned
to anodal or sham stimulation conditions. All individuals underwent a battery of reading
assessments pre and post stimulation. The stimulation session involved 15 min of anodal/sham
stimulation over the left temporoparietal junction while concurrently completing a
computerized nonword segmentation task known to activate the temporoparietal junction.
Results: There were no conclusive findings that anodal stimulation impacted reading
performance for skilled or impaired readers. Conclusions: While tDCS may provide useful
gains on reading performance in the paediatric population, much more work is needed to
establish the parameters under which such findings would transfer to adult populations. IL
documentation, reporting, and interpreting of null effects of tDCS are immensely important to
a field that is growing exponentially with much uncertainty.
INTRODUCTION
Literacy skills are characterized by performance in reading, spelling, and/or related tasks
(Peterson & Pennington, 2015; Tunmer & Greaney, 2010; Eden & Zeffiro, 1998). Literacy impair-
ment (per esempio., developmental dyslexia) can have a profound impact on an individuals’ academic
achievement, career opportunities, mental well-being, and social life, particularly in today’s
society where social media platforms are extensive and rely heavily on written communication
(per esempio., e-mail, Facebook, Twitter, eccetera.). Individuals with impaired literacy skills experience
decreased opportunities for employment, overall lower paying jobs, decreased success in
educational environments, and increased mental health issues (cioè., depression and anxiety), just
per dirne alcuni. To make matters worse, there are no cures for literacy-based learning disabilities.
Many remediation approaches have been proposed that target specific skill-based training (cioè.,
letter-to-sound mapping, phonemic decoding, fluency); Tuttavia, these are best implemented in
childhood when the skills are still developing. They are not always effective, with vast variability
in literacy profiles, responders -versus non-responders, and often, these children continue to have
persistent literacy difficulties through adulthood. Overall, these findings underscore the need to
Citation: Cummine, J., Villarena, M.,
Onysyk, T., & Devlin, J. T. (2020). UN
study of null effects for the use of
transcranial direct current stimulation
(tDCS) in adults with and without
reading impairment. Neurobiology of
Language, 1(4), 434–451. https://doi.org/
10.1162/nol_a_00020
DOI:
https://doi.org/10.1162/nol_a_00020
Supporting Information:
https://doi.org/10.1162/nol_a_00020
Received: 28 ottobre 2019
Accepted: 19 Luglio 2020
Competing Interests: The authors have
declared that no competing interests
exist.
Corresponding Author:
Jacqueline Cummine
jcummine@ualberta.ca
Handling Editor:
Kate Watkins
Copyright: © 2020 Massachusetts
Institute of Technology. Pubblicato
under a Creative Commons Attribution
4.0 Internazionale (CC BY 4.0) licenza.
The MIT Press
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Null effects of tDCS in adult readers
explore novel approaches, such as neuromodulation, to remediating reading difficulties in
adulthood.
Neuromodulation
Transcranial direct current stimulation (tDCS) is a noninvasive neurostimulation technique that
involves direct current delivery to the level of the scalp (Filmer, Dux, & Mattingley, 2014; Monti
et al., 2013; Stagg & Nitsche, 2011). Negative cathodal stimulation hyperpolarizes neurons
whereas positive anodal stimulation depolarizes neurons (Thair, Holloway, Newport, & Smith,
2017). Placement of the positive and negative electrodes into various montages is purposeful to
upregulate and/or downregulate activity in specific brain regions. The recommended current
delivery range is between 1–2 mA, with no adverse or harmful effects being documented except
for mild itching or tingling sensations (Brunoni et al., 2012; Nitsche et al., 2004). Direct current
delivery (which varies in current strength, measured in milli-amperes, mA) can be described in
terms of charge density (C/cm2) and duration of current application, both of which elicit changes
during and after stimulation (Stagg & Nitsche, 2011). The changes during stimulation are a result
of subthreshold alterations in neuron resting membrane potential; a dose of anodal stimulation
elevates the resting membrane potential, causing neurons to be more easily excited, whereas
cathodal stimulation brings the neurons to a more negative resting potential, increasing the
difficulty for excitation (Filmer et al., 2014; Nitsche & Paulus, 2001; Thair et al., 2017). IL
evidence for this comes from combined tDCS plus transcranial magnetic stimulation studies that
measure induced motor evoked potentials (Nitsche & Paulus, 2001) and pharmacological exper-
iments. Per esempio, Nitsche et al. (2003) showed that blocking calcium and sodium ion chan-
nels with flunarizine and carbamezipine was able to attenuate the effects of anodal stimulation,
highlighting the importance of ion channels in the elevation of the resting membrane potential
and subsequent anodal effects.
Neuromodulation and Reading
Within the paediatric literature, a handful of researchers have provided supportive findings for the
use of tDCS in the remediation of reading difficulties (Costanzo et al., 2016UN, 2016B, 2019;
Rahimi et al., 2019; Rios et al., 2018). Per esempio, Costanzo et al. (2016B) tested the effects
of single session tDCS (20 min, 0.04 mA/cm2 current density) on reading performance with
different montages: concurrent anodal left temporoparietal junction stimulation with right
homologue cathodal stimulation, as well as the reverse (cathodal left hemisphere, anodal right).
Overall, they found a reduction in reading errors on a 400-word Italian text during left anodal/
right cathodal stimulation, but diminished accuracy when the right anodal/ left cathodal
condition was administered. Such effects have also been reported for nonword and word accu-
racy (Rios et al., 2018), and auditory processing speed (Rahimi et al., 2019) with single anodal
stimulation conditions over the left temporal region.
While adult reading studies with tDCS are often varied and conflicting (Heth & Lavidor, 2015;
Thomson, Doruk, Mascio, Fregni, & Cerruti, 2015; Turkeltaub et al., 2012; Younger, Randazzo
Wagner, & Booth, 2016; see also Minarik et al., 2016, for a discussion of how power in tDCS
studies translates to mixed findings), the significant effects associated with stimulation warrant
further investigation. Per esempio, Turkeltaub et al.’s (2012) study on left lateralization of reading
efficiency reported that delivering anodal stimulation (via 5 × 5 cm positive electrode at 1.5 mA,
20-min stimulation) to the left temporoparietal junction and cathodal stimulation to the right
homologue was able to improve performance on reading both words and nonwords. In contrasto,
Neurobiology of Language
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Null effects of tDCS in adult readers
it appears that right and not left temporoparietal junction stimulation improves letter-to-sound
mapping in adults (Thomson et al., 2015). To further complicate matters, it appears that left
hemisphere stimulation can be detrimental to performance in some cases. For instance,
Younger et al. (2016) reported anodal stimulation of the left inferior parietal lobule (via 5 ×
5 cm positive electrode at 1.5 mA, 20-min stimulation) enhanced single word reading efficiency
but impaired rhyme judgment. As such, additional work is still needed—particularly approaches
that take into account the recommendations outlined in Minarik et al. (2016) with respect to
power and sample size—to answer the question: Does anodal tDCS over the left temporoparietal
junction enhance reading performance in adults?
Given the promising effects of neuromodulation on reading performance in the paediatric
population, perhaps the mixed findings in the adult population are due to a reduced capacity
for neural plasticity (see Cancer & Antonietti, 2018, for a review of nine papers that explore
tDCS effects on reading performance). As noted in several papers (Costanzo et al., 2016UN,
2019; see also Younger & Booth, 2018, for an example of neuromodulation plus reading training
in adults), one possible way of boosting the effects of neuromodulation is to apply simultaneous
stimulation, whereby the stimulation is paired with a task that utilizes the same brain region that is
being targeted for stimulation and the subsequent behavioural performance. From neuroimaging,
we have evidence that the temporoparietal junction (consisting of the posterior superior temporal
gyrus, the inferior supramarginal gyrus, and the angular gyrus) is particularly sensitive to letter-to-
sound mapping, among other things (Ramus, 2004). For individuals with reading impairments,
the temporoparietal junction has been identified as underactivated by fMRI (Eden et al., 2004;
Richlan, Kronbichler, & Wimmer, 2009; Shaywitz et al., 2002; Eden & Zeffiro, 1998), positron
emission tomography (Rumsey et al., 1992), and MEG (Breier et al., 2003). On a structural level
(cioè., diffusion tensor imaging), it has been reported that white matter tracts underlying the
left temporoparietal junction have decreased structural integrity compared to typical readers
(Klingberg et al., 2000; Deutsch et al., 2005; Hoeft et al., 2011; Rimrodt, Peterson, Denckla,
Kaufmann, & Cutting, 2010; Niogi & McCandliss, 2006).
In the paediatric literature, we know that individuals with reading impairments often have
deficits in letter-to-sound mapping (Navas, Ferraz, & Borges, 2014; Ramus, 2014; Snowling,
1981) and manipulation of the small sound units that comprise a word (per esempio., phonemic aware-
ness, reading of nonwords such as “yeighb”; Kochnower, Richardson, & DiBenedetto, 1983;
Rack, Snowling, & Olson, 1992; Snowling, 1981). Previous research has shown that training
for certain aspects of reading by segmenting words into small units of sound can improve future
reading performance (Alexander & Slinger-Constant, 2004; Eden et al., 2004; Younger & Booth,
2018). The joint effects of neuromodulation plus skill-based reading training was recently
explored by Costanzo et al., (2016UN, 2019) in children with the following protocol: 3 sessions
per week for 6 weeks, at 20 min per session, with anode on left parietotemporal and cathode
on right parietotemporal regions, and current density 0.04mA/cm2. In this work, the authors
showed that sessions of cognitive behavioural training, which included overt reading speed and
covert phonics, alongside anodal stimulation were able to improve nonword reading speed and
low-frequency word accuracy in Italian children with and without reading impairment. Those
administered the sham condition saw no improvement overall, whereas those who received
the anodal condition displayed improvements at both 1-month and 6-month timepoints, impli-
cating a lasting beneficial effect of tDCS delivery alongside training. The lasting after-effects of
tDCS have been documented (Brunoni et al., 2012; Monte-Silva et al., 2013; Nitsche & Paulus,
2001; Bindman, Lippold, & Redfearn, 1964) and are attributed to mechanisms of synaptic plasticity
similar to long-term potentiation (see Bear & Malenka, 1994; Bliss & Lømo, 1973; Liebetanz,
Nitsche, Tergau, & Paulus, 2002; Monte-Silva et al., 2013; Nitsche et al., 2003; Stagg & Nitsche,
Neurobiology of Language
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Null effects of tDCS in adult readers
2011, for discussions on molecular changes via NMDA receptor antagonist dextromethropane,
agonist d-cycloserine, and Ca2+).
In a recent study by Younger and Booth (2018), adults underwent training to learn a new
orthography and either had anodal stimulation over the left temporoparietal junction (5 cm ×
5 cm, 1.5 mA, 20-min, 3 sessions) or sham stimulation. Similar to previous work, the authors
found that stimulation benefitted adults with lower reading skills to a greater degree than adults
with higher reading skills. Notably, Younger and Booth (2018) did not deliver stimulation at the
same time as training, and thus it remains unknown the extent to which there are potential benefits
of simultaneous neuromodulation and training in adults with and without reading difficulties.
The Current Study
There is some evidence to support the hypothesis that (1) the delivery of tDCS to the left temporo-
parietal junction can enhance performance on reading speed and reading accuracy (Costanzo
et al., 2016B; Heth & Lavidor, 2015) E (2) simultaneous tDCS and training can improve reading
performance (Costanzo et al., 2016UN, 2019; Alexander & Slinger-Constant, 2004; Eden et al., 2004).
Here, we aim to explore the impact of simultaneous neuromodulation and training on reading
performance in adults with and without reading impairments. Based on the recent review by
Cancer and Antonietti (2018), we anticipate that the training, in general, would enhance reading
performance (cioè., accuracy and reading speed) for individuals with impaired reading ability. Noi
further anticipate that stimulation plus training would improve reading speed in both groups.
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MATERIALS AND METHODS
Participants
Adults (N = 62; age >18) were recruited to take part in the study. Individuals were classified as
having a reading impairment based on the following criteria: (1) they self-identified as having
previous reading and learning difficulties and (2) at least one overt reading score (using the
Word Identification and Word Attack standardized reading tests; Woodcock & Johnson, 1989)
that falls 2 SD below the mean of the skilled adult readers. The subjects that were recruited were
all over 18 (M = 22.125; SD = 3.442; 5 females), had no previous history of stroke, migraines,
seizures, and epilepsy, and had no existing comorbidities with attention deficit hyperactive
disorder. All subjects were right-handed, had normal or corrected normal vision, and were
proficient in English. Two participants were removed due to equipment failure (cioè., NO
dependent measures recorded). The final groups were Impaired (N = 32; Females = 29) E
Skilled (N = 28; Females = 20; Vedi la tabella 1 Descriptive Statistics). Consent was obtained
according to the Declaration of Helsinki (2013, https://www.wma.net/policies-post/wma-
declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjects/)
and the experiment was performed in compliance with the relevant laws and institutional
Tavolo 1. Descriptive statistics
Skilled
Age
23.1 (4.4)
Mean school years
16.29 (2.4)
Word identification
102.75 (1.3)
Word attack
43.52 (1.4)
Reading history questionnaire
0.16 (0.17)
Impaired
22.2 (4.1)
15.55 (2.4)
98.85 (2.2)
41.09 (2.5)
0.28 (0.16)
p value
0.413
0.243
*<0.001
*<0.001
*0.007
Note. Mean (SD) and group differences. *Significant difference ( p < 0.05) between groups using an independent samples t test.
Neurobiology of Language
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Null effects of tDCS in adult readers
guidelines and was approved by the Health Research Ethics Board at the University of Alberta.
All participants were paid a small honorarium.
Materials
Several tasks were chosen based on previous work on tDCS plus reading (Cancer & Antonietti,
2018; Turkeltaub et al., 2012; Younger et al., 2016; Younger & Booth, 2018). Specifically, reading
efficiency (i.e., timed tasks that require participants to overtly generate single words/nonwords as
quickly and accurately as possible) have been shown to be positively impacted by tDCS in adults
(Turkeltaub et al., 2012; Younger et al., 2016). In addition, given the single session, single montage
nature of the current study, we also opted to include an additional efficiency task that removed the
reading component and just measured fluency (i.e., timed tasks that require participants to overtly
generate single letters/digits as quickly and accurately as possible; Younger et al., 2016). Notably,
the latter task is highly related to and predictive of reading ability and disability and may also be
susceptible to training and/or stimulation changes in a single session.
Overt reading task
Two lists (40 words in each) for each stimulus type (regular words, nonwords, and pseudohomo-
phones) were prepared and randomized for each participant, with one as the pre-stimulation task
and the other as the post-stimulation task. Words were taken from the English Lexicon Project
(Balota et al., 2007; mean length = 4.2, mean log frequency HAL = 8.3; mean orthographic neigh-
borhood = 8.4; mean phonological neighborhood = 17.4; mean number of phonemes = 3.5; mean
bigram = 1,420), while nonwords (mean length = 5.3; mean orthographic neighborhood = 1.6;
mean bigram = 1,211) and pseudohomophones (mean length = 5.2; mean orthographic neigh-
bourhood = 1.8; mean bigram = 1,287) were selected from the ARC nonword database (Rastle,
Harrington, & Coltheart, 2002). The order of presentation of pre-stimulus tasks (words, nonwords,
pseudohomophones) was randomized for each participant. The stimuli in the pre- and post-tasks
were also counter-balanced across participants. Each list contained 40 letter strings, for a total of
240 letter strings (see Appendix A in online supporting information located at https://www.
mitpressjournals.org/doi/suppl/10.1162/nol_a_00020).
Rapid naming task
A standard 4 × 9 array of letters (i.e., c, n, s, a, k, t) and digits (i.e., 2, 3, 4, 5, 7, 8) as per the
Comprehensive Test of Phonological Processing (CTOPP; Wagner, Torgesen, Rashotte, &
00
00
Pearson, 1999) was used. The following procedure was used to create the 4 × 9 array: a 6
× 8
grid was created that was partitioned into 36 cells. The six letters were randomly inserted into the
array with the following restrictions: (1) no letter/digit was presented more than two times in a row,
and (2) no letter/digit was presented twice in sequence (including controlling for a letter presented at
the end of a row and the beginning of the next row). The letters/digits were presented in Calibri
68 pt. font on a Dell Vostro laptop, running Windows 7, with a screen resolution of 1366 × 768.
Following this procedure, five unique arrays of letters and digits were created. Wagner et al.
(1999) reported test–retest reliability for letters and digits in adults to be 0.86 and 0.90, respectively.
Procedure
Upon arrival at the testing area, individuals were provided with a verbal explanation of the study,
requested to read the terms of the study (with assistance if necessary), ask any questions, and sign
the consent form. After consenting to the experiment, they were asked to complete a reading
history questionnaire (Adult Reading History Questionnaire; see Parrila, Georgiou, & Corkett,
Neurobiology of Language
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Null effects of tDCS in adult readers
2007, for details) and a health evaluation form for screening. Participants then completed both the
Word Identification and Word Attack tests (Woodcock & Johnson, 1989) to further characterize
their overall reading abilities.
Pre-stimulation testing
Participants were seated in front of a monitor in the testing room for the administration of the pre-
stimulus tests. One microphone was affixed between the eyebrow region with the microphone
surface directed downwards and placed 10 cm away from the mouth, and a second free-standing
microphone was placed directly in front of the mouth to record participant onset response time.
The pre-stimulus tasks (the same as for post) included a fluency measure (rapid automatized
naming (RAN) of digits and letters) and a reading measure (overt word naming of real words, non-
words, and pseudohomophones). The order of task presentation was randomized for each partic-
ipant. All tasks were programmed in, and delivered through, E-Prime 3.0 software (Psychology
Software Tools, Pittsburgh, PA, USA) using a standard Dell computer with a secondary monitor
extension to avoid distracting the participant during the coding process. Participants were told that
they would see some familiar and unfamiliar words on the screen, and their goal was to read aloud
the words as quickly and accurately as possible as they appeared in the centre of the screen one by
one. Halfway through the task, participants were offered a break, which typically lasted <1 min.
The examiner coded for accuracy of the responses by button-presses on laptop (1 =correct
pronunciation; 2 = incorrect; 3 = spoil). Voice recordings participants during word
reading task were collected via program TF32, and stored as WAV>
