Development of Reading Abilities in Children with ADHD Following fNIRS-Neurofeedback or EMG-Biofeedback
Abstract
Abstract. Children with attention deficit/hyperactivity disorder (ADHD) show deficient reading skills, which, like ADHD symptoms, are associated with limitations in neurocognitive abilities. Neurofeedback (NF) aims to improve the latter, to alleviate ADHD symptoms, and to promote school and reading performances. Whether frontal lobe-NF based on functional near-infrared spectroscopy (fNIRS) and electromyogram (EMG)-biofeedback (BF), however, improve reading abilities of children with ADHD and whether these changes are associated with changes in neurocognitive abilities, has not yet been clarified. It was also unclear whether embedding trainings in virtual reality (VR) could increase their effectiveness. These questions were examined using data of 35 children with ADHD (6–11 years) who participated in 15 sessions of fNIRS-NF in VR, fNIRS-NF in 2D, or EMG-BF in VR. On average, children's reading performance improved in all training groups. Stronger improvements were found after VR trainings. Improvements in reading natural words were, on a trend level, accompanied by decreasing attention, while improvements in reading pseudowords were accompanied by improved sustained attention and response inhibition. The results suggest that fNIRS-NF and EMG-BF effectively improve reading abilities of children with ADHD, especially when training in VR.
Zusammenfassung. Kinder mit Aufmerksamkeitsdefizit-/Hyperaktivitätsstörung (ADHS) zeigen defizitäre Lesefähigkeiten, welche, wie ADHS-Symptome, mit Einschränkungen in neurokognitiven Fähigkeiten verbunden sind. Neurofeedback (NF) zielt darauf, diese Fähigkeiten zu verbessern und ADHS-Symptome zu mildern, sowie Schul- und Leseleistungen zu fördern. Ob NF basierend auf funktioneller Nahinfrarotspektroskopie (fNIRS) des Frontallappens und Elektromyogramm (EMG)-Biofeedback (BF) allerdings die Lesefähigkeit von Kindern mit ADHS verbessern und ob diese Veränderungen mit solchen in neurokognitiven Fähigkeiten einhergehen, war bislang unklar. Des Weiteren war unklar, ob die Einbettung von Trainings in virtuelle Realität (VR) deren Wirksamkeit steigern könnte. Diese Fragestellungen wurden anhand der Daten von 35 Kindern mit ADHS (6–11 Jahre alt), die an 15 Sitzungen eines fNIRS-NF in VR, fNIRS-NF in 2D oder EMG-BF in VR teilnahmen, untersucht. Die Leseleistung verbesserte sich im Mittel durch jedes Training. Stärkere Verbesserungen fanden sich nach Training in VR. Verbesserungen im Lesen natürlicher Wörter gingen mit einem Trend in der Abnahme der Aufmerksamkeit einher, während Verbesserungen im Lesen von Pseudowörtern von Verbesserungen in der Aufmerksamkeit und Impulskontrolle begleitet wurden. Die Ergebnisse legen die Wirksamkeit von fNIRS-NF und EMG-BF hinsichtlich der Verbesserung der Leseleistung von Kindern mit ADHS – vor allem bei Training in VR – nahe.
References
American Psychiatric Association (APA) . (2013). Diagnostic and statistical manual of mental disorders (DSM-5) (Fifth Vers.). Arlington: American Psychiatric Association Publishing.2015). Improved prefrontal activity in AD/HD children treated with atomoxetine: A NIRS study. Brain and Development, 37(1), 76–87. https://doi.org/10.1016/j.braindev.2014.03.011
(2014). Evaluation of neurofeedback in ADHD: The long and winding road. Biological Psychology, 95(0), 108–115. https://doi.org/10.1016/j.biopsycho.2013.11.013
(1997). Behavioral inhibition, sustained attention, and executive functions: Constructing a unifying theory of ADHD. Psychological Bulletin, 121(1), 65–94. https://doi.org/10.1037/0033-2909.121.1.65
(2005). Comparison of the DSM-IV combined and inattentive types of ADHD in a school-based sample of Latino/Hispanic children. Journal of Child Psychology and Psychiatry, 46(2), 166–179. https://doi.org/10.1111/j.1469-7610.2004.00343.x
. (2004). Impact of executive function deficits and attention-deficit/hyperactivity disorder (ADHD) on academic outcomes in children. Journal of Consulting and Clinical Psychology, 72(5), 757–766. https://doi.org/10.1037/0022-006X.72.5.757
(2019). Do students learn better when seated close to the teacher? A virtual classroom study considering individual levels of inattention and hyperactivity-impulsivity. Learning and Instruction, 61, 138–147. https://doi.org/10.1016/j.learninstruc.2018.10.004
(2017). NIRS-based neurofeedback training in a virtual reality classroom for children with attention-deficit/hyperactivity disorder: study protocol for a randomized controlled trial. Trials, 18, 41–57. https://doi.org/10.1186/s13063-016-1769-3
(2011). Virtual reality in neuroscience research and therapy. Nat Rev Neurosci, 12(12), 752–762. https://doi.org/http://dx.doi.org/10.1038/nrn3122
(2006). Fluency in Reading: Synchronization of Processes. Mahwah, N.J.: Routledge.
(2010). Attentional Control Activation Relates to Working Memory in Attention-Deficit/Hyperactivity Disorder. Biological Psychiatry, 67(7), 632–640. https://doi.org/10.1016/j.biopsych.2009.10.036
(2006). The design, development and evaluation of a virtual reality based learning environment. Australasian Journal of Educational Technology, 22(1), 39–63.
(2005).
(Modeling Reading: The Dual-Route Approach . In M. J. SnowlingC. Hulme (Eds.), The Science of Reading: A Handbook (pp. 6–23). Oxford: Blackwell Publishing.2011).
(Conners' Continuous Performance Test (CPT) . In DeLucaB. Caplan (Eds.), Encyclopedia of Clinical Neuropsychology SE - 1535 (pp. 681–683). Springer New York. https://doi.org/10.1007/978-0-387-79948-3_15351972). Human memory and the medial temporal region of the brain. Dissertation International, 34(2-B), 891.
(2016). Neurofeedback for Attention-Deficit/ Hyperactivity Disorder: Meta-analysis of clinical and neuropsychological outcomes from randomized controlled trials. Journal of the American Academy of Child & Adolescent Psychiatry, 55(6), 444–455. https://doi.org/10.1016/j.jaac.2016.03.007
(2011). A new method based on ICBM152 head surface for probe placement in multichannel fNIRS. NeuroImage, 54(2), 919–927. https://doi.org/10.1016/j.neuroimage.2010.09.030
(2010). ADHD and academic performance: why does ADHD impact on academic performance and what can be done to support ADHD children in the classroom? Child Care Health Dev, 36(4), 455–464. https://doi.org/10.1111/j.1365-2214.2009.01046.x
(2018). Sustained effects of neurofeedback in ADHD: a systematic review and meta-analysis. European Child & Adolescent Psychiatry. 28, 293–305, https://doi.org/10.1007/s00787-018-1121-4
(2008). Reduced lateral prefrontal activation in adult patients with attention-deficit/hyperactivity disorder (ADHD) during a working memory task: a functional near-infrared spectroscopy (fNIRS) study. Journal of Psychiatric Research, 42(13), 1060–1067. https://doi.org/10.1016/j.jpsychires.2007.11.011
(2008). Long term effects after feedback of slow cortical potentials and of theta-beta-amplitudes in children with attentiondeficit/hyperactivity disorder (ADHD). Int J Bioelectromagn, 10(4), 209–232.
(2017). Context-dependent learning and causal structure. Psychonomic Bulletin & Review, 24(2), 557–565. https://doi.org/10.3758/s13423-016-1110-x
(2014). Neurofeedback in attention-deficit/hyperactivity disorder – Different models, different ways of application. Frontiers in Human Neuroscience, 8. https://doi.org/10.3389/fnhum.2014.00846
(1997). The Strengths and Difficulties Questionnaire. A Research Note. Journal of Child Psychology and Psychiatry, 38, 581–586.
(2013). Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: Exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry, 70(2), 185–198. http://dx.doi.org/10.1001/jamapsychiatry.2013.277
(2018). Improving high school students' executive functions through digital game play. Computers & Education, 117, 50–58. https://doi.org/10.1016/J.COMPEDU.2017.09.011
(2011). Working memory influences processing speed and reading fluency in ADHD. Child Neuropsychology, 17(3), 209–224. https://doi.org/10.1080/09297049.2010.532204
(1958). Report of the committee on methods of clinical examination in electroencephalography. Electroencephalography and Clinical Neurophysiology., 10, 370–375.
(2013). Neurobiology of ADHD from childhood to adulthood. Journal of Attention Disorders, 19(11), 931–943. https://doi.org/10.1177/1087054713505322
(2014). Cognitive training in mental disorders: Update and future directions. American Journal of Psychiatry, 171(5), 510–522. https://doi.org/10.1176/appi.ajp.2013.13081075
(2008). Development of Word Reading Fluency and Spelling in a Consistent Orthography: An 8-Year Follow-Up. Journal of Educational Psychology, 100(1), 150–161. https://doi.org/10.1037/0022-0663.100.1.150
(2007). Neurofeedback for children with ADHD: A comparison of SCP and theta/beta protocols. Applied Psychophysiology and Biofeedback, 32(2), 73–88. https://doi.org/10.1007/s10484-007-9031-0
(2013). Conners Skalen zu Aufmerksamkeit und Verhalten-3. Deutschsprachige Adaption der Conners 3rd Edition von Keith Conners. [German translation of the Conners 3rd Edition]. Bern: Huber.
(2007). Academic and educational outcomes of children with ADHD. Journal of Pediatric Psychology, 32(6), 643–654. https://doi.org/10.1093/jpepsy/jsl054
(2015). Near-infrared spectroscopy (NIRS) neurofeedback as a treatment for children with attention deficit hyperactivity disorder (ADHD) – a pilot study. Frontiers in Human Neuroscience, 8. https://doi.org/10.3389/fnhum.2014.01038
(2015). Neurofeedback as a nonpharmacological treatment for adults with attention-deficit/hyperactivity disorder (ADHD): study protocol for a randomized controlled trial. Trials, 16(174). https://doi.org/10.1186/s13063-015-0683-4
(2014). Identifying a consistent pattern of neural function in attention deficit hyperactivity disorder: a meta-analysis. Psychological Medicine, 44(4), 869–880. https://doi.org/10.1017/S0033291713001037
(2014). Lese- und Rechtschreibtest (SLRT-II). Weiterentwicklung des Salzburger Lese- und Rechtschreibtests (SLRT) (2., korr. Aufl.). Bern: Verlag Hans Huber.
(2011). The PEBL Corsi Block Test.
(2014). The Psychology Experiment Building Language (PEBL) and PEBL Test Battery. Journal of Neuroscience Methods Methods. 222, 250–259.
(2000). Implementation of Virtual Reality in EEG Biofeedback. CyberPsychology & Behavior, 3(3), 415–420.
(2011). Wechsler Intelligence Scale for Children – Fourth Edition. Deutsche Bearbeitung (Pearson As). Frankfurt a.M.
(2019). The effect of adaptive difficulty adjustment on the effectiveness of a game to develop executive function skills for learners of different ages. Cognitive Development, 49, 56–67. https://doi.org/10.1016/J.COGDEV.2018.11.006
(R Core Team . (2020). R: A language and environment for statistical computing. Austria, Vienna: R Foundation for Statistical Computing.2005). Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI. NeuroImage, 27(4), 842–851. https://doi.org/10.1016/j.neuroimage.2005.05.019
(2017). Closed-loop brain training: the science of neurofeedback. Nature Reviews Neuroscience, 18, 86–101. ht tp://dx.doi.org/10.1038/nrn.2016.164
(2010). Beyond the dual pathway model: Evidence for the dissociation of timing, inhibitory, and delay-related impairments in attention-deficit/hyperactivity disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 49(4), 345–355. https://doi.org/10.1016/j.jaac.2009.12.018
(2013). Nonpharmacological interventions for ADHD: systematic review and meta-analyses of randomized controlled trials of dietary and psychological treatments. The American Journal of Psychiatry, 170(3), 275–289. https://doi.org/10.1176/appi.ajp.2012.12070991
(2002). Non-invasive neuroimaging using near-infrared light. Biological Psychiatry, 52(7), 679–693. https://doi.org/10.1016/S0006-3223(02)01550-0
(2017). Neurofeedback of Slow Cortical Potentials in children with Attention-Deficit/Hyperactivity Disorder (ADHD): a multicenter randomized trial controlling for unspecific effects. Frontiers in Human Neuroscience, 11, 135. https://doi.org/10.3389/FNHUM.2017.00135
(2006). Self-regulation of slow cortical potentials: A new treatment for children with Attention-Deficit/Hyperactivity Disorder. Pediatrics, 118(5), e1530–e1540. https://doi.org/10.1542/peds.2005-2478
(2014). Working memory and executive functions: effects of training on academic achievement. Psychological Research. Springer Verlag. https://doi.org/10.1007/s00426-013-0537-1
(2018). Sustained effects of neurofeedback in ADHD: a systematic review and meta-analysis. European Child & Adolescent Psychiatry, 28, 293–305. https://doi.org/10.1007/s00787-018-1121-4
(2013). CFT 1-R. Grundintelligenztest Skala 1 - Revision. Göttingen: Hogrefe Verlag.
(2006). CFT 20-R. Grundintelligenztest Skala 2 - Revision. Göttingen: Hogrefe Verlag.
(2005). Validity of the executive function theory of Attention-Deficit/Hyperactivity Disorder: A meta-analytic review. Biological Psychiatry, 57(11), 1336–1346. https://doi.org/10.1016/j.biopsych.2005.02.006
(2002). Paradoxical correlation between signal in functional magnetic resonance imaging and deoxygenated haemoglobin content in capillaries: a new theoretical explanation. Physics in Medicine and Biology, 47(7), 1121–1141. https://doi.org/10.1088/0031-9155/47/7/309
(