Neurofeedback in attention-deficit/hyperactivity disorder - different models, different ways of application

Holger Gevensleben, Gunther H Moll, Aribert Rothenberger, Hartmut Heinrich, Holger Gevensleben, Gunther H Moll, Aribert Rothenberger, Hartmut Heinrich

Abstract

In children with attention-deficit/hyperactivity disorder (ADHD), different neurofeedback (NF) protocols have been applied, with the most prominent differentiation between EEG frequency-band (e.g., theta/beta) training and training of slow cortical potentials (SCPs). However, beyond distinctions between such basic NF variables, there are also competing assumptions about mechanisms of action (e.g., acquisition of regulation capability, generalization to daily life behavior). In the present article, we provide a framework for NF models and suppose two hypothetical models, which we call "conditioning-and-repairing model" and "skill-acquisition model," reflecting extreme poles within this framework. We argue that the underlying model has an impact not only on how NF is applied but also on the selection of evaluation strategies and suggest using evaluation strategies beyond beaten paths of pharmacological research. Reflecting available studies, we address to what extent different views are supported by empirical data. We hypothesize that different models may hold true depending on the processes and behaviors to be addressed by a certain NF protocol. For example, the skill-acquisition model is supported by recent findings as an adequate explanatory framework for the mechanisms of action of SCP training in ADHD. In conclusion, evaluation and interpretation of NF trials in ADHD should be based on the underlying model and the way training is applied, which, in turn, should be stated explicitly in study reports.

Keywords: application; attention-deficit/hyperactivity disorder (ADHD); evaluation; learning; model; neurofeedback.

References

    1. Alexander G. E., Delong M. R., Strick P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9 357–381. 10.1146/annurev.ne.09.030186.002041
    1. Anderson J. R. (1983). The Architecture of Cognition. Cambridge, MA: Harvard University Press
    1. Arnold L. E., Lofthouse N., Hersch S., Pan X., Hurt E., Bates B., et al. (2012). EEG neurofeedback for ADHD: double-blind sham-controlled randomized pilot feasibility trial. J. Atten. Disord. 17 410–419. 10.1177/1087054712446173
    1. Arns M., Conners C. K., Kraemer H. C. (2012). A decade of EEG Theta/Beta ratio research in ADHD: a meta-analysis. J. Atten. Disord. 17 374–383. 10.1177/1087054712460087
    1. Arns M., Heinrich H., Strehl U. (2014). Evaluation of neurofeedback in ADHD: the long and winding road. Biol. Psychol. 95 108–115. 10.1016/j.biopsycho.2013.11.013
    1. Arns M., Strehl U. (2013). Evidence for efficacy of neurofeedback in ADHD? Am. J. Psychiatry 170 799–800. 10.1176/appi.ajp.2013.13020208
    1. Bakhshayesh A. R., Hansch S., Wyschkon A., Rezai M. J., Esser G. (2011). Neurofeedback in ADHD: a single-blind randomized controlled trial. Eur. Child Adolesc. Psychiatry 20 481–491. 10.1007/s00787-011-0208-y
    1. Banaschewski T., Brandeis D. (2007). Annotation: what electrical brain activity tells us about brain function that other techniques cannot tell us – a child psychiatric perspective. J. Child Psychol. Psychiatry 48 415–435. 10.1111/j.1469-7610.2006.01681.x
    1. Banaschewski T., Brandeis D., Heinrich H., Albrecht B., Brunner E., Rothenberger A. (2003). Association of ADHD and conduct disorder–brain electrical evidence for the existence of a distinct subtype. J. Child Psychol. Psychiatry 44 356–376. 10.1111/1469-7610.00127
    1. Barry R. J., Clarke A. R., Johnstone S. J. (2003). A review of electrophysiology in attention-deficit/hyperactivity disorder: I. Qualitative and quantitative electroencephalography. Clin. Neurophysiol. 114 171–183. 10.1016/S1388-2457(02)00362-0
    1. Barry R. J., Clarke A. R., Johnstone S. J., Mccarthy R., Selikowitz M. (2009). Electroencephalogram theta/beta ratio and arousal in attention-deficit/hyperactivity disorder: evidence of independent processes. Biol. Psychiatry 66 398–401. 10.1016/j.biopsych.2009.04.027
    1. Birbaumer N., Ruiz S., Sitaram R. (2013). Learned regulation of brain metabolism. Trends Cogn. Sci. 17 295–302. 10.1016/j.tics.2013.04.009
    1. Borkovec T. D., Sibrava N. J. (2005). Problems with the use of placebo conditions in psychotherapy research, suggested alternatives, and some strategies for the pursuit of the placebo phenomenon. J. Clin. Psychol. 61 805–818. 10.1002/jclp.20127
    1. Bruckmann S., Hauk D., Roessner V., Resch F., Freitag C. M., Kammer T., et al. (2012). Cortical inhibition in attention deficit hyperactivity disorder: new insights from the electroencephalographic response to transcranial magnetic stimulation. Brain 135 2215–2230. 10.1093/brain/aws071
    1. Daum I., Rockstroh B., Birbaumer N., Elbert T., Canavan A., Lutzenberger W. (1993). Behavioural treatment of slow cortical potentials in intractable epilepsy: neuropsychological predictors of outcome. J. Neurol. Neurosurg. Psychiatry 56 94–97. 10.1136/jnnp.56.1.94
    1. Doehnert M., Brandeis D., Straub M., Steinhausen H. C., Drechsler R. (2008). Slow cortical potential neurofeedback in attention deficit hyperactivity disorder: is there neurophysiological evidence for specific effects? J. Neural Transm. 115 1445–1456. 10.1007/s00702-008-0104-x
    1. Doppelmayr M., Weber E., Hoedlmoser K., Klimesch W. (2009). Effects of SMR feedback on the EEG amplitude. Hum. Cogn. Neurophysiol. 2 21–32
    1. Drechsler R., Straub M., Doehnert M., Heinrich H., Steinhausen H. C., Brandeis D. (2007). Controlled evaluation of a neurofeedback training of slow cortical potentials in children with Attention Deficit/Hyperactivity Disorder (ADHD). Behav. Brain Funct. 3 35. 10.1186/1744-9081-3-35
    1. Duric N. S., Assmus J., Gundersen D., Elgen I. B. (2012). Neurofeedback for the treatment of children and adolescents with ADHD: a randomized and controlled clinical trial using parental reports. BMC Psychiatry 12:107. 10.1186/1471-244X-12-107
    1. Egner T., Gruzelier J. H. (2003). Ecological validity of neurofeedback: modulation of slow wave EEG enhances musical performance. Neuroreport 14 1221–1224. 10.1097/00001756-200307010-00006
    1. Egner T., Zech T. F., Gruzelier J. H. (2004). The effects of neurofeedback training on the spectral topography of the electroencephalogram. Clin. Neurophysiol. 115 2452–2460. 10.1016/j.clinph.2004.05.033
    1. Gevensleben H., Holl B., Albrecht B., Schlamp D., Kratz O., Studer P., et al. (2010). Neurofeedback training in children with ADHD: 6-month follow-up of a randomised controlled trial. Eur. Child Adolesc. Psychiatry 19 715–724. 10.1007/s00787-010-0109-105.
    1. Gevensleben H., Holl B., Albrecht B., Vogel C., Schlamp D., Kratz O., et al. (2009a). Is neurofeedback an efficacious treatment for ADHD? A randomised controlled clinical trial. J. Child Psychol. Psychiatry 50 780–789. 10.1111/j.1469-7610.2008.02033.x
    1. Gevensleben H., Holl B., Albrecht B., Schlamp D., Kratz O., Studer P., et al. (2009b). Distinct EEG effects related to neurofeedback training in children with ADHD: a randomized controlled trial. Int. J. Psychophysiol. 74 149–157. 10.1016/j.ijpsycho.2009.08.005
    1. Gevensleben H., Kleemeyer M., Studer P., Flaig-Röhr A., Moll G. H., Rothenberger A., et al. (2014). Neurofeedback in ADHD: further pieces of the puzzle. Brain Topogr. 27 20–32. 10.1007/s10548-013-0285-y
    1. Gevensleben H., Rothenberger A., Moll G. H., Heinrich H. (2012). Neurofeedback in children with ADHD: validation and challenges. Exp. Rev. Neurother. 12 447–460. 10.1586/ern.12.22
    1. Goldberg J., Weller L., Blittner M. (1982). Cognitive self-control factors in EMG biofeedback. Biofeedback Self Regul. 7 545–551. 10.1007/BF00998893
    1. Goujon A., Didierjean A., Poulet S. (2014). The emergence of explicit knowledge from implicit learning. Mem. Cogn. 42 225–236. 10.3758/s13421-013-0355-0
    1. Gruzelier J. H. (2014a). EEG-neurofeedback for optimising performance. I: a review of cognitive and affective outcome in healthy participants. Neurosci. Biobehav. Rev. 44 124–141. 10.1016/j.neubiorev.2013.09.015
    1. Gruzelier J. H. (2014b). EEG-neurofeedback for optimising performance. II: creativity, the performing arts and ecological validity. Neurosci. Biobehav. Rev. 44 142–158. 10.1016/j.neubiorev.2013.11.004
    1. Gruzelier J. H. (2014c). EEG-neurofeedback for optimising performance III: a review of methodological and theoretical considerations. Neurosci. Biobehav. Rev. 44 159–182. 10.1016/j.neubiorev.2014.03.015
    1. Hardman E., Gruzelier J., Cheesman K., Jones C., Liddiard D., Schleichert H., et al. (1997). Frontal interhemispheric asymmetry: self regulation and individual differences in humans. Neurosci. Lett. 221 117–120. 10.1016/S0304-3940(96)13303-6
    1. Heinrich H., Busch K., Studer P., Erben K., Moll G. H., Kratz O. (2014). EEG spectral analysis of attention in ADHD: implications for neurofeedback training? Front. Hum. Neurosci. 8:611. 10.3389/fnhum.2014.00611
    1. Heinrich H., Gevensleben H., Freisleder F. J., Moll G. H., Rothenberger A. (2004). Training of slow cortical potentials in attention-deficit/hyperactivity disorder: evidence for positive behavioral and neurophysiological effects. Biol. Psychiatry 55 772–775. 10.1016/j.biopsych.2003.11.013
    1. Heinrich H., Gevensleben H., Strehl U. (2007). Annotation: neurofeedback – train your brain to train behaviour. J. Child Psychol. Psychiatry 48 3–16. 10.1111/j.1469-7610.2006.01665.x
    1. Hinterberger T., Veit R., Wilhelm B., Weiskopf N., Vatine J. J., Birbaumer N. (2005). Neuronal mechanisms underlying control of a brain-computer interface. Eur. J. Neurosci. 21 3169–3181. 10.1111/j.1460-9568.2005.04092.x
    1. Hoedlmoser K., Pecherstorfer T., Gruber G., Anderer P., Doppelmayr M., Klimesch W., et al. (2008). Instrumental conditioning of human sensorimotor rhythm (12-15 Hz) and its impact on sleep as well as declarative learning. Sleep 31 1401–1408
    1. Holtmann M., Pniewski B., Wachtlin D., Wörz S., Strehl U. (2014). Neurofeedback in children with attention-deficit/hyperactivity disorder (ADHD) – a controlled multicenter study of a non-pharmacological treatment approach. BMC Pediatr. 14:202. 10.1186/1471-2431-14-202
    1. Holroyd K. A., Penzien D. B., Hursey K. G., Tobin D. L., Rogers L., Holm J. E., et al. (1984). Change mechanisms in EMG biofeedback training: cognitive changes underlying improvements in tension headache. J. Consult. Clin. Psychol. 52 1039–1053. 10.1037/0022-006X.52.6.1039
    1. Johnson K. A., Hartwell K., Lematty T., Borckardt J., Morgan P. S., Govindarajan K., et al. (2012). Intermittent “real-time” fMRI feedback is superior to continuous presentation for a motor imagery task: a pilot study. J. Neuroimaging 22 58–66. 10.1111/j.1552-6569.2010.00529.x
    1. Kathner I., Ruf C. A., Pasqualotto E., Braun C., Birbaumer N., Halder S. (2013). A portable auditory P300 brain-computer interface with directional cues. Clin. Neurophysiol. 124 327–338. 10.1016/j.clinph.2012.08.006
    1. Kerson C. Collaborative Neurofeedback Group. (2013). A proposed multisite double-blind randomized clinical trial of neurofeedback for ADHD: need, rationale, and strategy. J. Atten. Disord. 17 420–436. 10.1177/1087054713482580
    1. Koralek A. C., Jin X., Long J. D., II, Costa R. M., Carmena J. M. (2012). Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills. Nature 483 331–335. 10.1038/nature10845
    1. Kotchoubey B., Strehl U., Uhlmann C., Holzapfel S., Konig M., Froscher W., et al. (2001). Modification of slow cortical potentials in patients with refractory epilepsy: a controlled outcome study. Epilepsia 42 406–416. 10.1046/j.1528-1157.2001.22200.x
    1. Kratz O., Studer P., Malcherek S., Erbe K., Moll G. H., Heinrich H. (2011). Attentional processes in children with ADHD: an event-related potential study using the attention network test. Int. J. Psychophysiol. 81 82–90. 10.1016/j.ijpsycho.2011.05.008
    1. Kübler A., Birbaumer N. (2008). Brain-computer interfaces and communication in paralysis: extinction of goal directed thinking in completely paralysed patients? Clin. Neurophysiol. 119 2658–2666. 10.1016/j.clinph.2008.06.019
    1. Landers D. M., Petruzzello S. J., Salazar W., Crews D. J., Kubitz K. A., Gannon T. L., et al. (1991). The influence of electrocortical biofeedback on performance in pre-elite archers. Med. Sci. Sports Exerc. 23 123–129. 10.1249/00005768-199101000-00018
    1. Leins U., Hinterberger T., Kaller S., Schober F., Weber C., Strehl U. (2006). [Neurofeedback for children with ADHD: a comparison of SCP- and theta/beta-protocols]. Prax. Kinderpsychol. Kinderpsychiatr. 55 384–407
    1. Liechti M. D., Valko L., Muller U. C., Dohnert M., Drechsler R., Steinhausen H. C., et al. (2012). Diagnostic value of resting electroencephalogram in attention-deficit/hyperactivity disorder across the lifespan. Brain Topogr. 26 135–151. 10.1007/s10548-012-0258-6
    1. Logemann H. N., Lansbergen M. M., Van Os T. W., Bocker K. B., Kenemans J. L. (2010). The effectiveness of EEG-feedback on attention, impulsivity and EEG: a sham feedback controlled study. Neurosci. Lett. 479 49–53. 10.1016/j.neulet.2010.05.026
    1. Lubar J. F., Shouse M. N. (1976). EEG and behavioral changes in a hyperkinetic child concurrent with training of the sensorimotor rhythm (SMR): a preliminary report. Biofeedback Self Regul. 1 293–306. 10.1007/BF01001170
    1. Lutz A., Greischar L., Rawlings N., Davidson R. J. (2004). Long-term meditators self- induce high-amplitude gamma synchrony during mental practice. Proc. Natl. Acad. Sci. U.S.A. 101 16369–16373. 10.1073/pnas.0407401101
    1. Maurizio S., Liechti M. D., Heinrich H., Jancke L., Steinhausen H. C., Walitza S., et al. (2014). Comparing tomographic EEG neurofeedback and EMG biofeedback in children with attention-deficit/hyperactivity disorder. Biol. Psychol. 95 31–44. 10.1016/j.biopsycho.2013.10.008
    1. Meichenbaum D. (1976). Cognitive factors in biofeedback therapy. Biofeedback Self Regul. 1 201–216. 10.1007/BF00998587
    1. Monastra V. J., Monastra D. M., George S. (2002). The effects of stimulant therapy, EEG biofeedback, and parenting style on the primary symptoms of attention-deficit/hyperactivity disorder. Appl. Psychophysiol. Biofeedback 27 231–249. 10.1023/A:1021018700609
    1. Ninaus M., Kober S. E., Witte M., Koschutnig K., Stangl M., Neuper C., et al. (2013). Neural substrates of cognitive control under the belief of getting neurofeedback training. Front. Hum. Neurosci. 7:914. 10.3389/fnhum.2013.00914
    1. Pascual-Leone A., Amedi A., Fregni F., Merabet L. B. (2005). The plastic human brain cortex. Annu. Rev. Neurosci. 28 377–401. 10.1146/annurev.neuro.27.070203.144216
    1. Philippens I. H., Vanwersch R. A. (2010). Neurofeedback training on sensorimotor rhythm in marmoset monkeys. Neuroreport 21 328–332. 10.1097/WNR.0b013e3283360ba8
    1. Reber A. S. (1993). Implicit Learning and Tacit Knowledge: An Essay on the Cognitive Unconscious. New York: Oxford University Press
    1. Ros T., Munneke M. A., Parkinson L. A., Gruzelier J. H. (2014). Neurofeedback facilitation of implicit motor learning. Biol. Psychol. 95 54–58. 10.1016/j.biopsycho.2013.04.013
    1. Ros T., Theberge J., Frewen P. A., Kluetsch R., Densmore M., Calhoun V. D., et al. (2013). Mind over chatter: plastic up-regulation of the fMRI salience network directly after EEG neurofeedback. Neuroimage 65 324–335. 10.1016/j.neuroimage.2012.09.046
    1. Schabus M., Heib D. P., Lechinger J., Griessenberger H., Klimesch W., Pawlizki A., et al. (2014). Enhancing sleep quality and memory in insomnia using instrumental sensorimotor rhythm conditioning. Biol. Psychol. 95 126–134. 10.1016/j.biopsycho.2013.02.020
    1. Schafer R. J., Moore T. (2011). Selective attention from voluntary control of neurons in prefrontal cortex. Science 332 1568–1571. 10.1126/science.1199892
    1. Shebilske W., Goettl B., Regian J. W. (1999). “Executive control and automatic processes as complex skills develop in laboratory and applied settings,” in Attention and Performance XVII: Cognitive Regulation of Performance: Interaction of Theory and Application eds Gopher D., Koriat A. (Cambridge, MA: MIT Press; ) 401–432
    1. Sherlin L. A., Arns M., Lubar J., Heinrich H., Kersoni C., Strehl U., et al. (2011). Neurofeedback and basic learning theory: implications for research and practice. Neurotherapy 15 292–304. 10.1080/10874208.2011.623089
    1. Snyder S. M., Hall J. R. (2006). A meta-analysis of quantitative EEG power associated with attention-deficit hyperactivity disorder. J. Clin. Neurophysiol. 23 440–455. 10.1097/01.wnp.0000221363.12503.78
    1. Sonuga-Barke E., Brandeis D., Cortese S., Daley D., Danckaerts M., Döpfner M., et al. (2013). Response to Chronis-Tuscano et al and Arns and Strehl. Am. J. Psychiatry 170 800–802. 10.1176/appi.ajp.2013.13020208r
    1. Steinberg M., Othmer S. (2004). ADD: The 20-Hour Solution. Bandon, OR: Robert Reed Publishers
    1. Strehl U., Leins U., Goth G., Klinger C., Hinterberger T., Birbaumer N. (2006). Self-regulation of slow cortical potentials: a new treatment for children with attention-deficit/hyperactivity disorder. Pediatrics 118 e1530–e1540. 10.1542/peds.2005-2478
    1. Sun R., Slusarz P., Terry C. (2005). The interaction of the explicit and the implicit in skill learning: a dual-process approach. Psychol. Rev. 112 159–192. 10.1037/0033-295X.112.1.159
    1. van Dongen-Boomsma M., Vollebregt M. A., Slaats-Willemse D., Buitelaar J. K. (2013). A randomized placebo-controlled trial of electroencephalographic (EEG) neurofeedback in children with attention-deficit/hyperactivity disorder. J. Clin. Psychiatry 74 821–827. 10.4088/JCP.12m08321
    1. Vollebregt M. A., Van Dongen-Boomsma M., Buitelaar J. K., Slaats-Willemse D. (2014a). Does EEG-neurofeedback improve neurocognitive functioning in children with attention-deficit/hyperactivity disorder? A systematic review and a double-blind placebo-controlled study. J. Child Psychol. Psychiatry 55 460–472. 10.1111/jcpp.12143
    1. Vollebregt M. A., Van Dongen-Boomsma M., Slaats-Willemse D., Buitelaar J. K. (2014b). What future research should bring to help resolving the debate about the efficacy of EEG-neurofeedback in children with ADHD. Front. Hum. Neurosci. 8:321. 10.3389/fnhum.2014.00321
    1. Wangler S., Gevensleben H., Albrecht B., Studer P., Rothenberger A., Moll G. H., et al. (2011). Neurofeedback in children with ADHD: specific event-related potential findings of a randomized controlled trial. Clin. Neurophysiol. 122 942–950. 10.1016/j.clinph.2010.06.036
    1. Witte M., Kober S. E., Ninaus M., Neuper C., Wood G. (2013). Control beliefs can predict the ability to up-regulate sensorimotor rhythm during neurofeedback training. Front. Hum. Neurosci. 7:478. 10.3389/fnhum.2013.00478

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner