Top

ADHD Attention Deficit and Hyperactivity Disorders

Published in:

01-03-2019 | Original Article

The impact of successful learning of self-regulation on reward processing in children with ADHD using fMRI

Authors: Sarah Baumeister, Isabella Wolf, Sarah Hohmann, Nathalie Holz, Regina Boecker-Schlier, Tobias Banaschewski, Daniel Brandeis

Published in: ADHD Attention Deficit and Hyperactivity Disorders | Issue 1/2019

Abstract

Neurofeedback (NF) is a non-pharmacological treatment for attention-deficit/hyperactivity disorder (ADHD) that is targeting self-regulation, is efficacious when standard protocols are used and induces partly specific neurophysiological changes in the inhibitory network. However, its effects on reward processing, which is also considered an important aspect of ADHD and has been linked to neurophysiological deficits, remain unknown. Children with ADHD (N = 15, mean age 11.8, SD 1.52) were randomly assigned to either slow cortical potential NF (n = 8) or EMG biofeedback control training (n = 7) and received 20 sessions of training under comparable conditions. Learning was defined as the slope of successful training runs across all transfer sessions. Whole brain analysis, region-of-interest analysis of anticipatory ventral striatal (VS) activation, and analysis of behavioral data were performed. Clinically, the NF group improved more than the EMG group. Whole brain analysis indicated increased activation in the left superior frontal gyrus in the control group only, and in medial prefrontal cortex and dorsolateral prefrontal gyrus (DLPFC) after treatment across all groups. Only successful learners of self-regulation (n = 8) showed increased left inferior frontal gyrus and DLPFC activation after treatment. Left VS activation was increased after treatment and showed a significant time*medication-status interaction. Specific treatment effects were found in left frontal regions for the control treatment and successful learners. Also, unmedicated participants, irrespective of treatment type or successful learning, showed treatment-induced improvement in reward processing. The results suggest no prominent specific effect of NF on reward processing. However, cautious interpretation is warranted due to the small sample.

Aarts E et al (2015) Reward modulation of cognitive function in adult attention-deficit/hyperactivity disorder: a pilot study on the role of striatal dopamine. Behav Pharmacol 26:227–240. https://doi.org/10.1097/FBP.0000000000000116 CrossRefPubMedPubMedCentral

Alegria AA et al (2017) Real-time fMRI neurofeedback in adolescents with attention deficit hyperactivity disorder. Hum Brain Mapp 38:3190–3209. https://doi.org/10.1002/hbm.23584 CrossRefPubMedPubMedCentral

Arns M, de Ridder S, Strehl U, Breteler M, Coenen A (2009) Efficacy of neurofeedback treatment in ADHD: the effects on inattention, impulsivity and hyperactivity: a meta-analysis. Clin EEG Neurosci 40:180–189. https://doi.org/10.1177/155005940904000311 CrossRefPubMed

Balodis IM, Kober H, Worhunsky PD, Stevens MC, Pearlson GD, Carroll KM, Potenza MN (2016) Neurofunctional reward processing changes in cocaine dependence during recovery. Neuropsychopharmacology 41:2112–2121. https://doi.org/10.1038/npp.2016.11 CrossRefPubMedPubMedCentral

Banaschewski T, Hollis C, Oosterlaan J, Roeyers H, Rubia K, Willcutt E, Taylor E (2005) Towards an understanding of unique and shared pathways in the psychopathophysiology of ADHD. Dev Sci 8:132–140. https://doi.org/10.1111/j.1467-7687.2005.00400.x CrossRefPubMed

Baumeister S et al (2018) Neurofeedback training effects on inhibitory brain activation in ADHD: a matter of learning? Neuroscience 378:89–99. https://doi.org/10.1016/j.neuroscience.2016.09.025 CrossRefPubMed

Beauregard M, Levesque J (2006) Functional magnetic resonance imaging investigation of the effects of neurofeedback training on the neural bases of selective attention and response inhibition in children with attention-deficit/hyperactivity disorder. Appl Psychophysiol Biofeedback 31:3–20. https://doi.org/10.1007/s10484-006-9001-y CrossRefPubMed

Becker A, Gerchen MF, Kirsch M, Hoffmann S, Kiefer F, Kirsch P (2018) Striatal reward sensitivity predicts therapy-related neural changes in alcohol addiction. Eur Arch Psychiatry Clin Neurosci 268:231–242. https://doi.org/10.1007/s00406-017-0805-y CrossRefPubMed

Boecker R et al (2014) Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years. PLoS ONE 9:e104185. https://doi.org/10.1371/journal.pone.0104185 CrossRefPubMedPubMedCentral

Chantiluke K et al (2014) Disorder-specific functional abnormalities during temporal discounting in youth with attention deficit hyperactivity disorder (ADHD), autism and comorbid ADHD and autism. Psychiatry Res 223:113–120. https://doi.org/10.1016/j.pscychresns.2014.04.006 CrossRefPubMed

Coenen VA et al (2018) The anatomy of the human medial forebrain bundle: ventral tegmental area connections to reward-associated subcortical and frontal lobe regions. NeuroImage Clin 18:770–783. https://doi.org/10.1016/j.nicl.2018.03.019 CrossRefPubMedPubMedCentral

Cohen J (1969) Statistical power analysis for the behavioral sciences. Academic Press, New York

Cortese S et al (2016) Neurofeedback for attention-deficit/hyperactivity disorder: meta-analysis of clinical and neuropsychological outcomes from randomized controlled trials. J Am Acad Child Adolesc Psychiatry 55:444–455. https://doi.org/10.1016/j.jaac.2016.03.007 CrossRefPubMed

Delmo C, Weiffenbach O, Gabriel M, Stadler C, Poustka F (2000) 3. Auflage der Forschungsversion des K-SADS-PL, erweitert um ICD-10-Diagnostik. Huber, Bern

Demurie E, Roeyers H, Baeyens D, Sonuga-Barke E (2011) Common alterations in sensitivity to type but not amount of reward in ADHD and autism spectrum disorders. J Child Psychol Psychiatry 52:1164–1173. https://doi.org/10.1111/j.1469-7610.2010.02374.x CrossRefPubMed

Doehnert M, Brandeis D, Straub M, Steinhausen HC, 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. https://doi.org/10.1007/s00702-008-0104-x CrossRefPubMed

Dong G, Hu Y, Lin X (2013) Reward/punishment sensitivities among internet addicts: implications for their addictive behaviors. Prog Neuropsychopharmacol Biol Psychiatry 46:139–145. https://doi.org/10.1016/j.pnpbp.2013.07.007 CrossRefPubMed

Döpfner M, Götz-Dorten A, Lehmkuhl G, Breuer D, Goletz H (2008) Diagnostik-system für psychische Störungen im Kindes- und Jugendalter nach DSM-IV und ICD-10—II (DISYPS-II). Huber, Bern

Gevensleben H et al (2009) Distinct EEG effects related to neurofeedback training in children with ADHD: a randomized controlled trial. Int J Psychophysiol 74:149–157. https://doi.org/10.1016/j.ijpsycho.2009.08.005 CrossRefPubMed

Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35:4–26. https://doi.org/10.1038/npp.2009.129 CrossRefPubMed

Hauser TU, Iannaccone R, Ball J, Mathys C, Brandeis D, Walitza S, Brem S (2014) Role of the medial prefrontal cortex in impaired decision making in juvenile attention-deficit/hyperactivity disorder. JAMA Psychiatry 71:1165–1173. https://doi.org/10.1001/jamapsychiatry.2014.1093 CrossRefPubMed

Hayes DJ, Duncan NW, Xu J, Northoff G (2014) A comparison of neural responses to appetitive and aversive stimuli in humans and other mammals. Neurosci Biobehav Rev 45:350–368. https://doi.org/10.1016/j.neubiorev.2014.06.018 CrossRefPubMed

Holtmann M et al (2009) Spezifische Wirksamkeit von neurofeedback auf die impulsivität bei ADHS. Kindheit und Entwicklung 18:95–104CrossRef

Holtmann M, Pniewski B, Wachtlin D, Worz S, Strehl U (2014a) Neurofeedback in children with attention-deficit/hyperactivity disorder (ADHD): a controlled multicenter study of a non-pharmacological treatment approach. BMC Pediatr 14:202. https://doi.org/10.1186/1471-2431-14-202 CrossRefPubMedPubMedCentral

Holtmann M, Sonuga-Barke E, Cortese S, Brandeis D (2014b) Neurofeedback for ADHD: a review of current evidence. Child Adolesc Psychiatr Clin 23:789–806. https://doi.org/10.1016/j.chc.2014.05.006 CrossRef

Kirsch P et al (2003) Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. NeuroImage 20:1086–1095. https://doi.org/10.1016/S1053-8119(03)00381-1 CrossRefPubMed

Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159CrossRefPubMed

Kofler MJ, Rapport MD, Sarver DE, Raiker JS, Orban SA, Friedman LM, Kolomeyer EG (2013) Reaction time variability in ADHD: a meta-analytic review of 319 studies. Clin Psychol Rev 33:795–811. https://doi.org/10.1016/j.cpr.2013.06.001 CrossRefPubMed

Kohls G, Thonessen H, Bartley GK, Grossheinrich N, Fink GR, Herpertz-Dahlmann B, Konrad K (2014) Differentiating neural reward responsiveness in autism versus ADHD. Dev Cognit Neurosci 10:104–116. https://doi.org/10.1016/j.dcn.2014.08.003 CrossRef

Luking KR, Nelson BD, Infantolino ZP, Sauder CL, Hajcak G (2017) Internal consistency of functional magnetic resonance imaging and electroencephalography measures of reward in late childhood and early adolescence. Biol Psychiatry Cognit Neurosci Neuroimaging 2:289–297. https://doi.org/10.1016/j.bpsc.2016.12.004 CrossRef

Luman M, Oosterlaan J, Sergeant JA (2005) The impact of reinforcement contingencies on AD/HD: a review and theoretical appraisal. Clin Psychol Rev 25:183–213. https://doi.org/10.1016/j.cpr.2004.11.001 CrossRefPubMed

Metin B, Tas ZC, Cebi M, Buyukaslan A, Soysal A, Hatiloglu D, Tarhan N (2018) Reward processing deficits during a spatial attention task in patients with ADHD: an fMRI study. J Atten Disord 22:694–702. https://doi.org/10.1177/1087054717703188 CrossRefPubMed

Micoulaud-Franchi JA, Geoffroy PA, Fond G, Lopez R, Bioulac S, Philip P (2014) EEG neurofeedback treatments in children with ADHD: an updated meta-analysis of randomized controlled trials. Front Hum Neurosci 8:906. https://doi.org/10.3389/fnhum.2014.00906 CrossRefPubMedPubMedCentral

Muller VI, Hohner Y, Eickhoff SB (2018) Influence of task instructions and stimuli on the neural network of face processing: an ALE meta-analysis. Cortex 103:240–255. https://doi.org/10.1016/j.cortex.2018.03.011 CrossRefPubMedPubMedCentral

Mullinger KJ, Yan WX, Bowtell R (2011) Reducing the gradient artefact in simultaneous EEG-fMRI by adjusting the subject’s axial position. NeuroImage 54:1942–1950. https://doi.org/10.1016/j.neuroimage.2010.09.079 CrossRefPubMed

Norman LJ et al (2018) Frontostriatal dysfunction during decision making in attention-deficit/hyperactivity disorder and obsessive-compulsive disorder. Biol Psychiatry Cognit Neurosci Neuroimaging. https://doi.org/10.1016/j.bpsc.2018.03.009 CrossRef

Oldham S, Murawski C, Fornito A, Youssef G, Yucel M, Lorenzetti V (2018) The anticipation and outcome phases of reward and loss processing: a neuroimaging meta-analysis of the monetary incentive delay task. Hum Brain Mapp. https://doi.org/10.1002/hbm.24184 CrossRefPubMedPubMedCentral

Paloyelis Y, Mehta MA, Faraone SV, Asherson P, Kuntsi J (2012) Striatal sensitivity during reward processing in attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 51(722–732):e729. https://doi.org/10.1016/j.jaac.2012.05.006 CrossRef

Plichta MM, Scheres A (2014) Ventral-striatal responsiveness during reward anticipation in ADHD and its relation to trait impulsivity in the healthy population: a meta-analytic review of the fMRI literature. Neurosci Biobehav Rev 38:125–134. https://doi.org/10.1016/j.neubiorev.2013.07.012 CrossRefPubMed

Plichta MM, Scheres A (2015) Measuring the neural basis of reward anticipation and reward receipt in attention-deficit/hyperactivity disorder: the importance of task design. J Am Acad Child Adolesc Psychiatry 54:685–686. https://doi.org/10.1016/j.jaac.2015.05.012 CrossRefPubMed

Plichta MM et al (2012) Test-retest reliability of evoked BOLD signals from a cognitive-emotive fMRI test battery. NeuroImage 60:1746–1758. https://doi.org/10.1016/j.neuroimage.2012.01.129 CrossRefPubMed

Plichta MM et al (2013) Simultaneous EEG and fMRI reveals a causally connected subcortical-cortical network during reward anticipation. J Neurosci 33:14526–14533. https://doi.org/10.1523/JNEUROSCI.0631-13.2013 CrossRefPubMedPubMedCentral

Richardson JTE (2011) Eta squared and partial eta squared as measures of effect size in educational research. Educ Res Rev 6:135–147. https://doi.org/10.1016/j.edurev.2010.12.001 CrossRef

Rubia K, Halari R, Cubillo A, Mohammad AM, Brammer M, Taylor E (2009a) Methylphenidate normalises activation and functional connectivity deficits in attention and motivation networks in medication-naive children with ADHD during a rewarded continuous performance task. Neuropharmacology 57:640–652. https://doi.org/10.1016/j.neuropharm.2009.08.013 CrossRefPubMed

Rubia K, Smith AB, Halari R, Matsukura F, Mohammad M, Taylor E, Brammer MJ (2009b) Disorder-specific dissociation of orbitofrontal dysfunction in boys with pure conduct disorder during reward and ventrolateral prefrontal dysfunction in boys with pure ADHD during sustained attention. Am J Psychiatry 166:83–94. https://doi.org/10.1176/appi.ajp.2008.08020212 CrossRefPubMed

Sagvolden T, Johansen EB, Aase H, Russell VA (2005) A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav Brain Sci 28:397–419. https://doi.org/10.1017/S0140525X05000075 (discussion 419–368) CrossRefPubMed

Scheres A, Milham MP, Knutson B, Castellanos FX (2007) Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder. Biol Psychiatry 61:720–724. https://doi.org/10.1016/j.biopsych.2006.04.042 CrossRefPubMed

Schweren LJS et al (2017) Stimulant treatment trajectories are associated with neural reward processing in attention-deficit/hyperactivity disorder. J Clin Psychiatry 78:e790–e796. https://doi.org/10.4088/JCP.15m10624 CrossRefPubMed

Singh-Curry V, Husain M (2009) The functional role of the inferior parietal lobe in the dorsal and ventral stream dichotomy. Neuropsychologia 47:1434–1448. https://doi.org/10.1016/j.neuropsychologia.2008.11.033 CrossRefPubMedPubMedCentral

Sjowall D, Roth L, Lindqvist S, Thorell LB (2013) Multiple deficits in ADHD: executive dysfunction, delay aversion, reaction time variability, and emotional deficits. J Child Psychol Psychiatry 54:619–627. https://doi.org/10.1111/jcpp.12006 CrossRefPubMed

Sonuga-Barke EJ (2011) Editorial: ADHD as a reinforcement disorder—moving from general effects to identifying (six) specific models to test. J Child Psychol Psychiatry 52:917–918. https://doi.org/10.1111/j.1469-7610.2011.02444.x CrossRefPubMed

Sonuga-Barke EJ et al (2013) Nonpharmacological interventions for ADHD: systematic review and meta-analyses of randomized controlled trials of dietary and psychological treatments. Am J Psychiatry 170:275–289. https://doi.org/10.1176/appi.ajp.2012.12070991 CrossRefPubMed

Stoy M et al (2011) Reward processing in male adults with childhood ADHD–a comparison between drug-naive and methylphenidate-treated subjects. Psychopharmacology 215:467–481. https://doi.org/10.1007/s00213-011-2166-y CrossRefPubMed

Strehl U et al (2017) Neurofeedback of slow cortical potentials in children with attention-deficit/hyperactivity disorder: a multicenter randomized trial controlling for unspecific effects. Front Hum Neurosci 11:135. https://doi.org/10.3389/fnhum.2017.00135 CrossRefPubMedPubMedCentral

Strohle A et al (2008) Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder. NeuroImage 39:966–972. https://doi.org/10.1016/j.neuroimage.2007.09.044 CrossRefPubMed

Uebel H et al (2010) Performance variability, impulsivity errors and the impact of incentives as gender-independent endophenotypes for ADHD. J Child Psychol Psychiatry 51:210–218. https://doi.org/10.1111/j.1469-7610.2009.02139.x CrossRefPubMed

van Dongen EV et al (2015) Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study. Mol Autism 6:48. https://doi.org/10.1186/s13229-015-0043-y CrossRefPubMedPubMedCentral

von Rhein D et al (2015) Increased neural responses to reward in adolescents and young adults with attention-deficit/hyperactivity disorder and their unaffected siblings. J Am Acad Child Adolesc Psychiatry 54:394–402. https://doi.org/10.1016/j.jaac.2015.02.012 CrossRef

Wangler S, Gevensleben H, Albrecht B, Studer P, Rothenberger A, Moll GH, Heinrich H (2011) Neurofeedback in children with ADHD: specific event-related potential findings of a randomized controlled trial. Clin Neurophysiol 122:942–950. https://doi.org/10.1016/j.clinph.2010.06.036 CrossRefPubMed

Title: The impact of successful learning of self-regulation on reward processing in children with ADHD using fMRI
Authors: Sarah Baumeister
Isabella Wolf
Sarah Hohmann
Nathalie Holz
Regina Boecker-Schlier
Tobias Banaschewski
Daniel Brandeis
Publication date: 01-03-2019
Publisher: Springer Vienna
Published in: ADHD Attention Deficit and Hyperactivity Disorders / Issue 1/2019
Print ISSN: 1866-6116
Electronic ISSN: 1866-6647
DOI: https://doi.org/10.1007/s12402-018-0269-6

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

The impact of successful learning of self-regulation on reward processing in children with ADHD using fMRI

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2019

Special edition on the occasion of Jan K. Buitelaar’s 65th anniversary

ADHD: a hidden comorbidity in adult psychiatric patients

Effect of disease-associated SLC9A9 mutations on protein–protein interaction networks: implications for molecular mechanisms for ADHD and autism

Reaction time variability and attention-deficit/hyperactivity disorder: is increased reaction time variability specific to attention-deficit/hyperactivity disorder? Testing predictions from the default-mode interference hypothesis

Apparent lack of practice effects in the Test of Variables of Attention (TOVA) in adult ADHD

Social-communicative and attention problems in infancy and toddlerhood as precursors of preschool autistic traits