Elsevier

Neuropsychologia

Volume 48, Issue 12, October 2010, Pages 3532-3539
Neuropsychologia

Atypical EEG beta asymmetry in adults with ADHD

https://doi.org/10.1016/j.neuropsychologia.2010.08.002Get rights and content

Abstract

Background

Abnormal brain laterality (ABL) is well established in ADHD. However, its clinical specificity and association to cognitive and clinical symptoms is not yet understood. Previous studies indicate increased right hemisphere (RH) contribution in both ADHD and reading impaired samples. The current study investigates whether this ABL characteristic occurs in adults with ADHD absent comorbid language impairment.

Methods

EEG beta asymmetry was compared in 35 adult ADHD subjects and 104 controls during rest and active cognition. Group differences in beta asymmetry were then further evaluated for association to linguistic and attentional abilities, as well as association to beta asymmetry measures across different brain regions.

Results

Adults with ADHD showed pronounced rightward beta asymmetry (p = .00001) in inferior parietal regions (P8-P7) during a continuous performance task (CPT) that could not be attributed to linguistic ability. Among ADHD subjects only, greater rightward beta asymmetry at this measure was correlated with better CPT performance. Furthermore, this measure showed a lack of normal association (i.e., observed in controls) to left-biased processing in temporal-parietal (TP8-TP7) brain regions important for higher order language functions.

Conclusion

Adult ADHD involves abnormally increased right-biased contribution to CPT processing that could not be attributed to poor language ability. This appears to also involve abnormal recruitment of LH linguistic processing regions and represents an alternative, albeit less effective, CPT processing strategy. These findings suggest different pathophysiologic mechanisms likely underlie RH biased processing in ADHD and reading impaired samples.

Introduction

To date, psychiatric research has been largely oriented toward trying to characterize disorder-specific impairment. However, mounting evidence of heterogeneity, comorbidity, and overlapping clinical and cognitive deficits suggests an additional approach is warranted whereby we also seek to characterize ‘what is common’ (i.e., shared neurobiological, affective, and cognitive features), and then in turn, try to understand how such general dysfunction gets uniquely expressed across disorders.

To this end, abnormal brain laterality (ABL) appears to be a highly convergent feature of psychiatric illness. It has been implicated in some form with most major disorders (e.g., ADHD, Dyslexia, autism, schizophrenia, bi-polar, anxiety, depression, etc.) (Annett, 1996, Asai et al., 2009, Baloch et al., 2009, Blumberg et al., 2003, Brambilla and Tansella, 2007, Downhill et al., 2000, Escalante-Mead et al., 2003, Hori et al., 2008, Kieseppa et al., 2010, Kleinhans et al., 2008, Monaghan and Shillcock, 2008, Morinaga et al., 2007, Robichon et al., 2000, Rotenberg, 2004, Schweiger et al., 1989, Stanfield et al., 2008, White et al., 2008), and may partly underlie noted overlap of affective and cognitive impairments among such disorders (e.g., impaired: linguistic processing, emotion/arousal regulation, working memory, attention, etc.) (Amir et al., 2009, Burdick et al., 2009, Calhoun and Mayes, 2005, Castaneda et al., 2008, Escalante-Mead et al., 2003, Hari and Renvall, 2001, Leung et al., 2009, Micco et al., 2009, Mur et al., 2007, Simonsen et al., 2009, Uekermann et al., 2008, Vaessen et al., 2009, Vasic et al., 2008). In short, normal integration of hemispherically specialized processing likely represents a key feature of the brain's basic operating system,1 and as such, ABL may be an inherent feature of psychiatric illness and contribute to similarly expressed clinical and cognitive impairments.

Given this generality, a key challenge of psychiatric brain laterality research is to try to elucidate shared versus unique aspects of ABL that might reflect general versus disorder-specific impairment (Crow et al., 1998, Smalley et al., 2005). We have addressed one small component of this challenge by first trying to characterize the nature of ABL in ADHD using behavioral laterality, EEG, and fMRI methodologies. This and other work has suggested a model that involves RH biased processing during early stages of information processing and/or simple forms of cognition, associated LH impairments, and abnormal interhemispheric interaction (Hale et al., 2007, Hale et al., 2009a, Hale et al., 2005, Hale et al., 2009b, Hale et al., 2009c, Hale et al., 2006). This pattern of ABL appears to contribute to ADHD deficits for more complex executive function (EF) operations dependent on normal LH functioning (Hale et al., 2007) and can be remediated via top-down attentional control (Hale et al., 2006). Moreover, it seems consistent with several ADHD characteristics such as: slow naming speed (Bedard et al., 2002, Brock and Christo, 2003, Nigg et al., 2002, Rucklidge and Tannock, 2002, Semrud-Clikeman et al., 2000, Tannock et al., 2000, van Mourik et al., 2005, Weiler et al., 2000, Willcutt et al., 2005b), increased left-handedness (Reid & Norvilitis, 2000), increased prevalence among males (Berry et al., 1985, Jones et al., 2003, Joseph, 2000), and increased novelty seeking (Cho et al., 2008, Goldberg et al., 1994, Lynn et al., 2005). Additionally, suspected low-dopamine and dysregulated noradrenergic function in ADHD (Pliszka, 2005) may also align with abnormal R > L contribution as these systems appear to exhibit some degree of left and right hemisphere specialization respectively (Tucker & Williamson, 1984).

An important outcome of this developing model is that ABL in ADHD appears to be highly similar to ABL reported in Dyslexia, which is a frequently comorbid disorder. ADHD–Dyslexia comorbidity has been estimated to range between 25% and 40% (Semrud-Clikeman, Biederman, & Sprich-Buchminster, 1992), and like ADHD, Dyslexia has been associated with RH biased processing during early stages of information processing (for review see: Pugh et al., 2000, Shaywitz and Shaywitz, 2008) and abnormal interhemispheric interaction (Dhar et al., 2010, Monaghan and Shillcock, 2008, Robichon et al., 2000). This pattern of ABL in Dyslexia also appears to be associated with abnormal brain-state orientation as it seems to be conditionally expressed (Ortiz et al., 1992, Pugh et al., 2000; and for review: Shaywitz & Shaywitz, 2008) and can be partly remediated through intensive training of LH encoding strategies (Penolazzi, Spironelli, Vio, & Angrilli, 2010). However, multiple factors indicate that there may be different pathophysiologic mechanisms underlying this shared pattern of ABL in ADHD and Dyslexic populations.

The posterior callosal region is abnormally small in ADHD (Seidman, Valera, & Makris, 2005), but appears to be abnormally large in Dyslexia (Monaghan & Shillcock, 2008). Moreover, event related potential (ERP) studies indicate opposite patterns of abnormal callosal transfer times. ADHD is associated with atypically fast left-to-right transfer in combined type, or atypically slow right-to-left transfer in inattentive type (Rolfe, Kirk, & Waldie, 2007), while Dyslexia shows the opposite pattern of abnormally fast right-to-left and slow left-to-right transfer (Davidson & Saron, 1992). Furthermore, Dyslexia shows abnormal structural asymmetries of the planum temporale that have not been identified in ADHD (Heim & Keil, 2004). Finally, our own behavioral laterality (Hale et al., 2009a, Hale et al., 2005, Hale et al., 2006) and imaging studies (Hale et al., 2007, Hale et al., 2009b, Hale et al., 2009c) have demonstrated that greater RH contribution in ADHD adults is not likely attributable to comorbid reading impairment. Still, additional research is needed to further substantiate whether increased RH contribution is an independent feature of ADHD, or reflects comorbid language impairment. The current study utilizes EEG beta spectral power (12–25 Hz) to address this matter.

There is ongoing debate about the nature of EEG beta, however, multiple studies have shown it to be associated with attention-directed early stage information processing (Bekisz and Wrobel, 2003, Deiber et al., 2007, Liang et al., 2002, Ray and Cole, 1985, Wrobel, 2000), and particularly so in the parietal regions (Barry et al., 2007, Ray and Cole, 1985, Schutter et al., 2001, Senkowski et al., 2006, Wrobel, 2000). More specifically, it is thought to be associated with mechanisms that potentiate early stage encoding of attentionally selected sensory information (for review see: Bekisz and Wrobel, 2003, Deiber et al., 2007, Wrobel, 2000). Consistent with this, EEG beta activation has been shown to track hemispherically specialized operations with leftward biased expression during verbal tasks and rightward biased expression for non-verbal tasks (Ray and Cole, 1985, Schutter et al., 2001). If ADHD and Dyslexia involve abnormal increased orientation toward RH biased processing, right-lateralized EEG beta activity should be evident in both groups. Moreover, if this is an independent feature of both disorders, it should be present in Dyslexia absent comorbid attention difficulties, and in ADHD absent comorbid reading difficulties.

To this end, multiple previous studies have shown increased RH parietal beta activity to be an independent feature of Dyslexia (i.e., without comorbid attention difficulties) (for review see: Rippon & Brunswick, 2000). Two studies have directly examined lateralized EEG beta activation in ADHD- one study of ADHD children with and without reading disorders (Clarke, Barry, McCarthy, & Selikowitz, 2002), and one in a reading impaired adult ADHD sample (Clarke et al., 2008). Both studies reported increased RH parietal beta activity in ADHD. The child study demonstrated this effect in ADHD children both with and without reading impairment. The adult ADHD study did not parse the effect of comorbid language impairment.

The current study extends this line of research by further examining whether increased RH EEG beta activity is evident among linguistically normal adults with ADHD (i.e., without comorbid language impairment). We do this during three conditions that place varying demands on attention-directed information processing (eyes closed, eyes open, Conner's Continuous Performance Test – CPT), and additionally examine the effects of language ability on all significant findings. Based on our own and others’ previous work indicating greater RH contribution in ADHD, and the previous report of increased RH beta activation in normal reading ADHD children, we hypothesized that increased RH EEG beta activity would be present in normal reading adults with ADHD.

Section snippets

Participants

The sample consisted of 139 adults (104 controls and 35 ADHD) recruited from an ongoing UCLA ADHD family genetics study (Smalley et al., 2000). Participation in this study required that families had at least 2 ADHD affected offspring. Thus, all subjects in the current study (cases and controls) were the biological parents of children with ADHD. After receiving verbal and written explanations of study requirements participants provided written informed consent approved by the UCLA Institutional

Step 1: beta asymmetry

One significant finding and one trend emerged. Both indicated increased rightward beta2 (16–21 Hz) asymmetry in adults with ADHD at the P8-P7 laterality index. The significant finding occurred during the CPT condition with controls (n = 84) showing leftward asymmetry (mean = −78.6, SE = 11.4) and ADHD subjects (n = 31) showing rightward asymmetry (mean = 26.8, SE = 19.3); [F(1,114) = 21.2, p = .00001]. The trend occurred during the eyes open condition with the same pattern [controls (n = 81): mean = −40, SE = 13.2;

Discussion

The current study uncovered a robust finding that showed adults with ADHD had abnormally increased rightward beta2 (16–21 Hz) asymmetry at P8-P7 electrodes (inferior parietal region) during the Conner's Continuous Performance Task (CPT). This could not be attributed to language ability as there were: (1) no group differences in vocabulary, phonologic, spelling, or reading abilities, (2) no significant correlations between the beta asymmetry measure of interest and any linguistic measure (with

References (104)

  • M. Dhar et al.

    Reduced interhemispheric coherence in dyslexic adults

    Cortex

    (2010)
  • J.E. Downhill et al.

    Shape and size of the corpus callosum in schizophrenia and schizotypal personality disorder

    Schizophrenia Research

    (2000)
  • C. Fassbender et al.

    Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature

    Clinical Psychology Review

    (2006)
  • I.I. Goncharova et al.

    EMG contamination of EEG: Spectral and topographical characteristics

    Clinical Neurophysiology

    (2003)
  • T.S. Hale et al.

    Impaired linguistic processing and atypical brain laterality in adults with ADHD

    Clinical Neuroscience Research

    (2005)
  • T.S. Hale et al.

    Atypical alpha asymmetry in adults with ADHD

    Neuropsychologia

    (2009)
  • T.S. Hale et al.

    Atypical brain laterality in adults with ADHD during dichotic listening for emotional intonation and words

    Neuropsychologia

    (2006)
  • R. Hari et al.

    Impaired processing of rapid stimulus sequences in dyslexia

    Trends in Cognitive Sciences

    (2001)
  • H. Hori et al.

    Functional near-infrared spectroscopy reveals altered hemispheric laterality in relation to schizotypy during verbal fluency task

    Progress in Neuro-Psychopharmacology and Biological Psychiatry

    (2008)
  • J. Kaufman et al.

    Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): Initial reliability and validity data

    Journal of the American Academy of Child and Adolescent Psychiatry

    (1997)
  • T. Kieseppa et al.

    Major depressive disorder and white matter abnormalities: A diffusion tensor imaging study with tract-based spatial statistics

    Journal of Affective Disorders

    (2010)
  • N.M. Kleinhans et al.

    Atypical functional lateralization of language in autism spectrum disorders

    Brain Research

    (2008)
  • K.-K. Leung et al.

    Selective attention biases of people with depression: Positive and negative priming of depression-related information

    Psychiatry Research

    (2009)
  • P. Monaghan et al.

    Hemispheric dissociation and dyslexia in a computational model of reading

    Brain and Language

    (2008)
  • K. Morinaga et al.

    Anticipatory anxiety-induced changes in human lateral prefrontal cortex activity

    Biological Psychology

    (2007)
  • J.T. Nigg et al.

    Neuropsychological executive functions and DSM-IV ADHD subtypes

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2002)
  • R.C. Oldfield

    Assessment and analysis of handedness: The Edinburgh Inventory

    Neuropsychologia

    (1971)
  • T. Ortiz et al.

    Brain mapping in dysphonemic dyslexia: In resting and phonemic discrimination conditions

    Brain and Language

    (1992)
  • B. Penolazzi et al.

    Brain plasticity in developmental dyslexia after phonological treatment: A beta EEG band study

    Behavioural Brain Research

    (2010)
  • S.R. Pliszka

    The neuropsychopharmacology of attention-deficit/hyperactivity disorder

    Biological Psychiatry

    (2005)
  • H.M. Reid et al.

    Evidence for anomalous laterlization across domain in ADHD children as well as adults identified with the Wender Utah rating scale

    Journal of Psychiatric Research

    (2000)
  • G. Rippon et al.

    Trait and state EEG indices of information processing in developmental dyslexia

    International Journal of Psychophysiology

    (2000)
  • V.S. Rotenberg

    The peculiarity of the right-hemisphere function in depression: Solving the paradoxes

    Progress in Neuro-Psychopharmacology and Biological Psychiatry

    (2004)
  • D.J. Schutter et al.

    Parietal electroencephalogram beta asymmetry and selective attention to angry facial expressions in healthy human subjects

    Neuroscience Letters

    (2001)
  • A. Schweiger et al.

    Right hemisphere contribution to lexical access in an aphasic with deep dyslexia

    Brain and Language

    (1989)
  • L.J. Seidman

    Neuropsychological functioning in people with ADHD across the lifespan

    Clinical Psychology Review

    (2006)
  • L.J. Seidman et al.

    Structural brain imaging of attention-deficit/hyperactivity disorder

    Biological Psychiatry

    (2005)
  • M. Semrud-Clikeman et al.

    Comorbidity between ADHD and learning disability: A review and report in a clinically referred sample

    Journal of the American Academy of Child and Adolescent Psychiatry

    (1992)
  • M. Semrud-Clikeman et al.

    Rapid naming deficits in children and adolescents with reading disabilities and attention deficit hyperactivity disorder

    Brain and Language

    (2000)
  • S.L. Smalley et al.

    Familial clustering of symptoms and disruptive behaviors in multiplex families with attention-deficit/hyperactivity disorder

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2000)
  • A.C. Stanfield et al.

    Towards a neuroanatomy of autism: A systematic review and meta-analysis of structural magnetic resonance imaging studies

    European Psychiatry

    (2008)
  • N.A. Taroyan et al.

    Behavioural and neurophysiological correlates of dyslexia in the continuous performance task

    Clinical Neurophysiology

    (2007)
  • L.Q. Uddin et al.

    Network homogeneity reveals decreased integrity of default-mode network in ADHD

    Journal of Neuroscience Methods

    (2008)
  • A. Vaessen et al.

    Naming problems do not reflect a second independent core deficit in dyslexia: Double deficits explored

    Journal of Experimental Child Psychology

    (2009)
  • N. Vasic et al.

    Neural correlates of working memory performance in adolescents and young adults with dyslexia

    Neuropsychologia

    (2008)
  • E.M. Whitham et al.

    Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20 Hz are contaminated by EMG

    Clinical Neurophysiology

    (2007)
  • N. Amir et al.

    Attention modification program in individuals with generalized anxiety disorder

    Journal of Abnormal Psychology

    (2009)
  • A. Baddeley et al.

    Working memory and the control of action: Evidence from task switching

    Journal of Experimental Psychology: General

    (2001)
  • H.A. Baloch et al.

    Corpus callosum abnormalities in pediatric bipolar disorder

    Expert Review of Neurotherapeutics

    (2009)
  • R.A. Barkley

    Behavioral inhibition, sustained attention, and executive functions: Construction a unifying theory of ADHD

    Psychological Bulletin

    (1997)
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    This work was funded in part by National Institute of Mental Health Grant MH058277 (Smalley), National Institute of Child Health and Human Development Grant HD40275 (Loo), National Institute of Neurological Disease and Stroke NS054124 (Loo), and by National Institute of Mental Health Grant MH082104 (Hale).

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