Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T17:35:40.915Z Has data issue: false hasContentIssue false

Diminished modulation of preparatory sensorimotor mu rhythm predicts attention-deficit/hyperactivity disorder severity

Published online by Cambridge University Press:  14 March 2017

N. ter Huurne*
Affiliation:
Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands
D. Lozano-Soldevilla
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
M. Onnink
Affiliation:
Department of Human Genetics, Radboudumc, Nijmegen, The Netherlands
C. Kan
Affiliation:
Department of Psychiatry, Radboudumc, Nijmegen, The Netherlands
J. Buitelaar
Affiliation:
Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands Department of Cognitive Neuroscience, Radboudumc, Nijmegen, The Netherlands
O. Jensen
Affiliation:
Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham, UK
*
*Address for correspondence: N. ter Huurne, Karakter Child and Adolescent Psychiatry University Centre, Reinier Postlaan 12, 6526 GC Nijmegen, The Netherlands. (Email: [email protected])

Abstract

Background

Attention-deficit/hyperactivity disorder (ADHD) is characterized by problems in regulating attention and in suppressing disruptive motor activity, i.e. hyperactivity and impulsivity. We recently found evidence that aberrant distribution of posterior α band oscillations (8–12 Hz) is associated with attentional problems in ADHD. The sensorimotor cortex also produces strong 8–12 Hz band oscillations, namely the μ rhythm, and is thought to have a similar inhibitory function. Here, we now investigate whether problems in distributing α band oscillations in ADHD generalize to the μ rhythm in the sensorimotor domain.

Method

In a group of adult ADHD (n = 17) and healthy control subjects (n = 18; aged 21–40 years) oscillatory brain activity was recorded using magnetoencephalography during a visuo-spatial attention task. Subjects had to anticipate a target with unpredictable timing and respond by pressing a button.

Results

Preparing a motor response, the ADHD group failed to increase hemispheric μ lateralization with relatively higher μ power in sensorimotor regions not engaged in the task, as the controls did (F1,33 = 8.70, p = 0.006). Moreover, the ADHD group pre-response μ lateralization not only correlated positively with accuracy (rs = 0.64, p = 0.0052) and negatively with intra-individual reaction time variability (rs = −0.52, p = 0.033), but it also correlated negatively with the score on an ADHD rating scale (rs = −0.53, p = 0.028).

Conclusions

We suggest that ADHD is associated with an inability to sufficiently inhibit task-irrelevant sensorimotor areas by means of modulating μ oscillatory activity. This could explain disruptive motor activity in ADHD. These results provide further evidence that impaired modulation of α band oscillations is involved in the pathogenesis of ADHD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, ZW, Derefinko, KJ, Milich, R, Fillmore, MT (2008). Inhibitory functioning across ADHD subtypes: recent findings, clinical implications, and future directions. Developmental Disabilities Research Reviews 14, 268275.Google Scholar
American Psychiatric Association (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, text rev. American Psychiatric Press: Washington, DC.Google Scholar
Aron, AR (2011). From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biological Psychiatry 69, e55e68.Google Scholar
Babiloni, C, Brancucci, A, Arendt-Nielsen, L, Babiloni, F, Capotosto, P, Carducci, F, Cincotti, F, Romano, L, Chen, AC, Rossini, PM (2004). Α event-related desynchronization preceding a go/no-go task: a high-resolution EEG study. Neuropsychology 18, 719728.Google Scholar
Barkley, RA (1997). Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychological Bulletin 121, 6594.Google Scholar
Bastiaansen, MC, Knosche, TR (2000). Tangential derivative mapping of axial MEG applied to event-related desynchronization research. Clinical Neurophysiology 111, 13001305.Google Scholar
Boonstra, AM, Kooij, JJ, Oosterlaan, J, Sergeant, JA, Buitelaar, JK (2010). To act or not to act, that's the problem: primarily inhibition difficulties in adult ADHD. Neuropsychology 24, 209221.Google Scholar
Brunia, CH (1999). Neural aspects of anticipatory behavior. Acta Psychologica 101, 213242.Google Scholar
Chambers, CD, Garavan, H, Bellgrove, MA (2009). Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neuroscience and Biobehavioral Reviews 33, 631646.Google Scholar
Clark, L, Blackwell, AD, Aron, AR, Turner, DC, Dowson, J, Robbins, TW, Sahakian, BJ (2007). Association between response inhibition and working memory in adult ADHD: a link to right frontal cortex pathology? Biological Psychiatry 61, 13951401.Google Scholar
Cubillo, A, Halari, R, Ecker, C, Giampietro, V, Taylor, E, Rubia, K (2010). Reduced activation and inter-regional functional connectivity of fronto-striatal networks in adults with childhood attention-deficit hyperactivity disorder (ADHD) and persisting symptoms during tasks of motor inhibition and cognitive switching. Journal of Psychiatric Research 44, 629639.Google Scholar
Devos, D, Szurhaj, W, Reyns, N, Labyt, E, Houdayer, E, Bourriez, JL, Cassim, F, Krystkowiak, P, Blond, S, Destee, A, Derambure, P, Defebvre, L (2006). Predominance of the contralateral movement-related activity in the subthalamo-cortical loop. Clinical Neurophysiology 117, 23152327.Google Scholar
Dockstader, C, Gaetz, W, Cheyne, D, Tannock, R (2009). Abnormal neural reactivity to unpredictable sensory events in attention-deficit/hyperactivity disorder. Biological Psychiatry 66, 376383.Google Scholar
DuPaul, GPT, Anastopoulos, A (1998). ADHD Rating Scale–IV: Checklists, Norms and Clinical Interpretation. Guilford Press: New York.Google Scholar
Fayyad, J, De Graaf, R, Kessler, R, Alonso, J, Angermeyer, M, Demyttenaere, K, De Girolamo, G, Haro, JM, Karam, EG, Lara, C, Lepine, JP, Ormel, J, Posada-Villa, J, Zaslavsky, AM, Jin, R (2007). Cross-national prevalence and correlates of adult attention-deficit hyperactivity disorder. British Journal of Psychiatry 190, 402409.Google Scholar
Foxe, JJ, Snyder, AC (2011). The role of α-band brain oscillations as a sensory suppression mechanism during selective attention. Frontiers in Psychology 2, 154.Google Scholar
Hoogman, M, Aarts, E, Zwiers, M, Slaats-Willemse, D, Naber, M, Onnink, M, Cools, R, Kan, C, Buitelaar, J, Franke, B (2011). Nitric oxide synthase genotype modulation of impulsivity and ventral striatal activity in adult ADHD patients and healthy comparison subjects. American Journal of Psychiatry 168, 10991106.Google Scholar
Hughes, SW, Crunelli, V (2005). Thalamic mechanisms of EEG α rhythms and their pathological implications. Neuroscientist 11, 357372.Google Scholar
Jensen, O, Mazaheri, A (2010). Shaping functional architecture by oscillatory α activity: gating by inhibition. Frontiers in Human Neuroscience 4, 186.Google Scholar
Jung, TP, Makeig, S, Humphries, C, Lee, TW, McKeown, MJ, Iragui, V, Sejnowski, TJ (2000). Removing electroencephalographic artifacts by blind source separation. Psychophysiology 37, 163178.Google Scholar
Klimesch, W, Sauseng, P, Hanslmayr, S (2007). EEG α oscillations: the inhibition-timing hypothesis. Brain Research Reviews 53, 6388.Google Scholar
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. Clinical Psychology Reviews 33, 795811.Google Scholar
Kooij, JFM (2007). Diagnostisch Interview voor ADHD (DIVA) bij volwassenen (Diagnostic Interview for ADHD (DIVA) in Adults). DIVA Foundation: the Hague, the Netherlands.Google Scholar
Kooij, JJ, Buitelaar, JK, van den Oord, EJ, Furer, JW, Rijnders, CA, Hodiamont, PP (2005). Internal and external validity of attention-deficit hyperactivity disorder in a population-based sample of adults. Psychological Medicine 35, 817827.Google Scholar
Majid, DS, Cai, W, Corey-Bloom, J, Aron, AR (2013). Proactive selective response suppression is implemented via the basal ganglia. Journal of Neuroscience 33, 1325913269.Google Scholar
Mazaheri, A, Coffey-Corina, S, Mangun, GR, Bekker, EM, Berry, AS, Corbett, BA (2010). Functional disconnection of frontal cortex and visual cortex in attention-deficit/hyperactivity disorder. Biological Psychiatry 67, 617623.Google Scholar
Mazaheri, A, Fassbender, C, Coffey-Corina, S, Hartanto, TA, Schweitzer, JB, Mangun, GR (2014). Differential oscillatory electroencephalogram between attention-deficit/hyperactivity disorder subtypes and typically developing adolescents. Biological Psychiatry 76, 422429.Google Scholar
Mazaheri, A, Nieuwenhuis, IL, van Dijk, H, Jensen, O (2009). Prestimulus α and μ activity predicts failure to inhibit motor responses. Human Brain Mapping 30, 17911800.Google Scholar
Muthukumaraswamy, SD, Johnson, BW, McNair, NA (2004). μ Rhythm modulation during observation of an object-directed grasp. Brain Research. Cognitive Brain Research 19, 195201.Google Scholar
Neuper, C, Wortz, M, Pfurtscheller, G (2006). ERD/ERS patterns reflecting sensorimotor activation and deactivation. Progress in Brain Research 159, 211222.Google Scholar
Nigg, JT (2005). Neuropsychologic theory and findings in attention-deficit/hyperactivity disorder: the state of the field and salient challenges for the coming decade. Biological Psychiatry 57, 14241435.Google Scholar
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97113.Google Scholar
Pfurtscheller, G, Brunner, C, Schlogl, A, Lopes da Silva, FH (2006). μ Rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks. NeuroImage 31, 153159.Google Scholar
Pfurtscheller, G, Neuper, C (1994). Event-related synchronization of μ rhythm in the EEG over the cortical hand area in man. Neuroscience Letters 174, 9396.Google Scholar
Pfurtscheller, G, Neuper, C (1997). Motor imagery activates primary sensorimotor area in humans. Neuroscience Letters 239, 6568.Google Scholar
Pfurtscheller, G, Neuper, C, Krausz, G (2000). Functional dissociation of lower and upper frequency μ rhythms in relation to voluntary limb movement. Clinical Neurophysiology 111, 18731879.Google Scholar
Pfurtscheller, G, Pregenzer, M, Neuper, C (1994). Visualization of sensorimotor areas involved in preparation for hand movement based on classification of μ and central β rhythms in single EEG trials in man. Neuroscience Letters 181, 4346.Google Scholar
Polanczyk, G, de Lima, MS, Horta, BL, Biederman, J, Rohde, LA (2007). The worldwide prevalence of ADHD: a systematic review and metaregression analysis. American Journal of Psychiatry 164, 942948.Google Scholar
Rubia, K, Overmeyer, S, Taylor, E, Brammer, M, Williams, SC, Simmons, A, Bullmore, ET (1999). Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. American Journal of Psychiatry 156, 891896.Google Scholar
Rubia, K, Taylor, E, Smith, AB, Oksanen, H, Overmeyer, S, Newman, S (2001). Neuropsychological analyses of impulsiveness in childhood hyperactivity. British Journal of Psychiatry 179, 138143.Google Scholar
Saalmann, YB, Pinsk, MA, Wang, L, Li, X, Kastner, S (2012). The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337, 753756.Google Scholar
Salmelin, R, Hari, R (1994). Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement. Neuroscience 60, 537550.Google Scholar
Sergeant, JA, Geurts, H, Huijbregts, S, Scheres, A, Oosterlaan, J (2003). The top and the bottom of ADHD: a neuropsychological perspective. Neuroscience and Biobehavioral Reviews 27, 583592.Google Scholar
Simon, V, Czobor, P, Balint, S, Meszaros, A, Bitter, I (2009). Prevalence and correlates of adult attention-deficit hyperactivity disorder: meta-analysis. British Journal of Psychiatry 194, 204211.Google Scholar
Stancak, A Jr., Pfurtscheller, G (1996). μ-Rhythm changes in brisk and slow self-paced finger movements. Neuroreport 7, 11611164.Google Scholar
Stolk, A, Todorovic, A, Schoffelen, JM, Oostenveld, R (2013). Online and offline tools for head movement compensation in MEG. NeuroImage 68, 3948.Google Scholar
Teicher, MH, Anderson, CM, Polcari, A, Glod, CA, Maas, LC, Renshaw, PF (2000). Functional deficits in basal ganglia of children with attention-deficit/hyperactivity disorder shown with functional magnetic resonance imaging relaxometry. Nature Medicine 6, 470473.Google Scholar
ter Huurne, N, Onnink, M, Kan, C, Franke, B, Buitelaar, J, Jensen, O (2013). Behavioral consequences of aberrant α lateralization in attention-deficit/hyperactivity disorder. Biological Psychiatry 74, 227233.Google Scholar
Wechsler, D (1997). Wechsler Adult Intelligence Scale, third edn. The Psychological Corporation: San Antonio, TX.Google Scholar
Yordanova, J, Kolev, V, Rothenberger, A (2013). Event-related oscillations reflect functional asymmetry in children with attention deficit/hyperactivity disorder. Supplements to Clinical Neurophysiology 62, 289301.Google Scholar