Atypical alpha asymmetry in adults with ADHD☆
Introduction
Attention deficit hyperactivity disorder (ADHD) is thought to represent an extreme on a normal continuum of liability with multiple genetic and environmental influences implicated as etiologic factors. A growing body of research suggests that atypical brain laterality (ABL) may be a common trait influencing ADHD risk along this continuum (Fassbender and Schweitzer, 2006, Hale et al., 2007, Hale et al., 2005, Hale et al., 2006, Smalley et al., 2005, Stefanatos and Wasserstein, 2001). ABL was first suggested by the observation that ADHD-like symptoms occurred in some patients with right-sided brain damage (Heilman, Voeller, & Nadeau, 1991) and by the observation that brain systems important for attention and arousal regulation, implicated in ADHD pathology, seemed to be right-lateralized (Aston-Jones et al., 1984, Corbetta et al., 1993, Pardo and Raichle, 1991). From this, a ‘right hemisphere’ (RH) deficit model in ADHD has been considered (for review see Stefanatos & Wasserstein, 2001).
Subsequent neurocognitive and brain-imaging studies have supported abnormal RH contribution, however, the nature of this abnormality has not yet been characterized. Impoverished RH function is sometimes assumed due to the association of ADHD-like symptoms with right-sided brain damage or abnormal brain structure, but it is also possible that such circumstance could lead to a loss of inhibition and dysregulated and/or increased RH activation (for review see Mesulam, 1988). Likewise, reports of ADHD deficits on tasks thought to tap RH specialized functions (for review see Stefanatos & Wasserstein, 2001) cannot by themselves rule out whether poor LH function also contributed to poor task performance. Finally, brain-imaging studies of ADHD have clearly demonstrated abnormal structure and function in both hemispheres (for review see Durston, 2003, Giedd et al., 2001, Seidman et al., 2005, Valera et al., 2006), as well as smaller corpus callosum volumes and abnormal left–right EEG coherence (Barry et al., 2005, Chabot and Serfontein, 1996, Clarke et al., 2007). In short, the nature of putative abnormal RH function in ADHD remains unclear, and the notion of a strictly lateralized deficit does not account for additional suggested abnormalities of both LH and interhemispheric function. Thus, characterization of putative ABL in ADHD requires continued research.
A common means of assessing lateralized brain function in clinical populations has been to examine the relative proportion of EEG alpha activity (8–12 Hz) in each hemisphere (i.e., alpha asymmetry). Alpha asymmetry appears to be a relatively stable trait with good internal consistency and test–re-test reliability (Tomarken, Davidson, Wheeler, & Kinney, 1992). Approximately 60% of variance is estimated to reflect a trait component, and 40% a state component (Hagemann, Naumann, Thayer, & Bartussek, 2002). Moreover, abnormalities in alpha asymmetry have been demonstrated with multiple forms of psychopathology such as depression (Bruder et al., 1997), anxiety (Bruder et al., 1997), bipolar disorder (Harmon-Jones et al., 2008), schizophrenia (Strelets, Garakh, Novototskii-Vlasov, & Magomedov, 2006), and autism (Stroganova et al., 2007) highlighting its importance for clinical research and demonstrating that ABL may be a shared feature of brain dysfunction impacting multiple psychiatric disorders (Smalley et al., 2005).
EEG studies of ADHD have consistently demonstrated anomalous alpha activity (for review see Barry, Clarke, & Johnstone, 2003), while medication studies have shown that increased alpha activity may be an important feature of ADHD methylphenidate response (Loo et al., 2004, Song et al., 2005). Also, increased rightward alpha asymmetry has been generally associated with ADHD-like traits such as reduced reward responsiveness, a lack of inhibition toward aversive experience, and increased approach behaviors (Davidson, 1992). Yet to our knowledge, only two studies have directly examined alpha asymmetry in ADHD. Baving, Laucht, and Schmidt (1999) reported increased rightward alpha asymmetry in 4–8-year-old boys with ADHD during an eyes-open resting condition. (Chabot and Serfontein, 1996) also reported increased rightward alpha asymmetry in large sample of 6–16-year-old ADHD male and female children during an eyes-closed resting condition.
The current study is the first to explore the hypothesis that increased rightward alpha asymmetry is also present in adults with ADHD. To do this, we assess alpha asymmetry in adults with ADHD versus healthy controls during two baseline conditions and one cognitive activation condition. Additionally, in our asymmetry analysis we examine upper (10–12 Hz) and lower (8–10 Hz) aspects of the alpha frequency band. Low alpha has been postulated to reflect diffuse attentional and brain-state phenomenon, while high alpha is postulated to reflect more localized and task-specific cognition (for review see Klimesch, 1999, Pfurtscheller et al., 2000).
Section snippets
Participants
The sample consisted of 91 adults (62 controls and 29 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
Results
Seven group differences emerged, all of which indicated increased rightward alpha asymmetry in adults with ADHD. These results occurred only during the CPT and EC conditions, and only in three laterality indices (F8-F7, FT8-FT7, P4-P3). Moreover, five of seven group differences occurred in low alpha. Medication status (entered as a covariate along with age and sex) did not approach significance in any analysis (for example, p-values for the covariate ‘medication status’ in the seven reported
Discussion
This study sought to determine whether rightward alpha asymmetry previously observed in child ADHD samples was also present in adults with ADHD. We compared EEG alpha asymmetry of adults with ADHD to controls during baseline (EC, EO) and cognitive challenge (CPT) conditions. Group differences were assessed with nine homologous electrode pairs for low (8–10 Hz) and high (10–12 Hz) alpha frequency bands. Seven results emerged all demonstrating increased rightward alpha asymmetry in adults with
Limitations
The issue of multiple comparisons is particularly difficult with EEG research as there are multiple sources of measurement (i.e., electrodes), each producing multiple data components (i.e., multi-hertz signal). Adding to this, state-influenced variability in EEG signal can diminish important trait characteristics that are thus less likely to survive corrections for multiple testing. EEG researchers often address this issue by averaging data across electrodes and/or using repeated measures ANOVA
References (72)
- et al.
A review of electrophysiology in attention-deficit/hyperactivity disorder: I. Qualitative and quantitative electroencephalography
Clinical Neurophysiology
(2003) - et al.
EEG coherence adjusted for inter-electrode distance in children with attention-deficit/hyperactivity disorder
International Journal of Psychophysiology
(2005) - et al.
Atypical frontal brain activation in ADHD: Preschool and elementary school boys and girls
Journal of the American Academy of Child and Adolescent Psychiatry
(1999) - et al.
Regional brain asymmetries in major depression with or without an anxiety disorder: A quantitative electroencephalographic study
Biological Psychiatry
(1997) - et al.
Electroencephalographic alpha measures predict therapeutic response to a selective serotonin reuptake inhibitor antidepressant: Pre- and post-treatment findings
Biological Psychiatry
(2008) - et al.
Functional neuroimaging of attention-deficit/hyperactivity disorder: A review and suggested future directions
Biological Psychiatry
(2005) - et al.
Quantitative electroencephalographic profiles of children with attention deficit disorder
Biological Psychiatry
(1996) - et al.
Coherence in children with attention-deficit/hyperactivity disorder and excess beta activity in their EEG
Clinical Neurophysiology
(2007) - et al.
Paradox lost? Exploring the role of alpha oscillations during externally vs. internally directed attention and the implications for idling and inhibition hypotheses
International Journal of Psychophysiology
(2003) Anterior cerebral asymmetry and the nature of emotion
Brain and Cognition
(1992)
Molecular genetics of attention-deficit/hyperactivity disorder
Biological Psychiatry
Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature
Clinical Psychology Review
Impaired linguistic processing and atypical brain laterality in adults with ADHD
Clinical Neuroscience Research
Aytpical Brain laterality in adults with ADHD during dichotic listening for emotional intonation and words
Neuropsychologia
Effect of bipolar disorder on left frontal cortical responses to goals differing in valence and task difficulty
Biological Psychiatry
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
Intra-subject variability in attention-deficit hyperactivity disorder
Biological Psychiatry
EEG alpha and theta oscillations reflect cognitive and memory performance: A review and analysis
Brain Research. Brain Research Reviews
EEG alpha oscillations: The inhibition-timing hypothesis
Brain Research Review
Concurrent EEG/fMRI analysis by multiway Partial Least Squares
Neuroimage
Assessment and analysis of handedness: The Edinburgh Inventory
Neuropsychologia
New vistas for alpha-frequency band oscillations
Trends in Neurosciences
Functional dissociation of lower and upper frequency mu rhythms in relation to voluntary limb movement
Clinical Neurophysiology
The thalamus as the generator and modulator of EEG alpha rhythm: A combined PET/EEG study with lorazepam challenge in humans
Neuroimage
Structural brain imaging of attention-deficit/hyperactivity disorder
Biological Psychiatry
Rapid naming deficits in children and adolescents with reading disabilities and attention deficit hyperactivity disorder
Brain and Language
Intention as a component of the alpha-rhythm response to mental activity
International Journal of Psychophysiology
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
Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis
Neuroscience and Biobehavioral Review
Abnormal EEG lateralization in boys with autism
Clinical Neurophysiology
EEG differences in ADHD-combined type during baseline and cognitive tasks
Pediatric Neurology
Validity of the executive function theory of attention-deficit/hyperactivity disorder: A meta-analytic review
Biological Psychiatry
Anatomy and physiology of locus coeruleus neurons: Functional implication
Frontiers of Clinical Neuroscience
Patterns of psychiatric comorbidity, cognition, and psychosocial functioning in adults with attention deficit hyperactivity disorder
The American Journal of Psychiatry
Digit naming speed performance among children with attention-deficit/hyperactivity disorder
California School Psychologist
Methylphenidate slows right hemisphere processing in children with attention-deficit/hyperactivity disorder
Journal of Child and Adolescent Psychopharmacology
Cited by (63)
The effectiveness of emotion cognitive reappraisal as measured by self-reported response and its link to EEG alpha asymmetry
2021, Behavioural Brain ResearchResting state EEG power research in Attention-Deficit/Hyperactivity Disorder: A review update
2020, Clinical NeurophysiologyCitation Excerpt :In two separate papers, alpha asymmetries (Hale et al., 2009) and beta asymmetries (Hale et al., 2010b) were investigated. Hale et al. (2009) reported alpha asymmetries during an eyes-open study, with adults with AD/HD showing increased rightward alpha asymmetry for low alpha at FT8-FT7 and P4-P3, and for high alpha at P4-P3. Hale et al. (2010b) found only significant right greater than left beta asymmetry for the P8-P7 pair during a continuous performance task.
- ☆
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), and National Institute of Mental Health Grant 1K99MH082104 (Hale).