Atypical EEG beta asymmetry in adults with ADHD☆
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
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2020, Clinical NeurophysiologyCitation Excerpt :The AD/HD group had elevated global absolute delta, elevated absolute and relative theta, and elevated absolute alpha and beta activity cf. controls. 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.
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2017, Neuroscience LettersCitation Excerpt :Many studies agree that, in various situations and conditions, beta waves significantly correlate with stimulatory and cognitive responses to external environments and mental states when awake, which vary among people according to individual differences and environmental factors [10–13]. For example, Hale [14] reported an abnormally increased rightward beta (16–21 Hz) asymmetry at the inferior parietal region in patients with attention deficit hyperactivity disorder performing continuous performance tasks. A study by Zaretskaya [15] analyzed the cognition and attention of participants and their correlation with beta waves when the patients viewed various rotational movement patterns of white and black dots.
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2016, NeuropsychologiaCitation Excerpt :Contrasting with the prevalent hypothesis of brain hypoarousal (Zentall and Zentall, 1983), increased cortical arousal was suggested in resting state and during sustained attention in adult ADHD cases with high intelligence functioning, possibly due to singular frontal neural organization (Loo et al., 2009). Moreover, increased rightward alpha and beta spectral power asymmetry at rest as well as in sustained attention and visuospatial cued tasks has been described in adult ADHD (Hale et al., 2009, 2010; ter Huurne et al., 2013), reinforcing the hypothesis of an abnormal brain laterality in this disorder (Stefanatos and Wasserstein, 2001). Unlike with these adult ADHD studies, the present work focused on short lasting attention task and analyzed the dynamics of event-locked oscillatory activity rather than time-independent gross spectral power.
Frontal brain asymmetry in adult attention-deficit/hyperactivity disorder (ADHD): Extending the motivational dysfunction hypothesis
2015, Clinical NeurophysiologyCitation Excerpt :Results from several studies suggest that these underpinnings may involve abnormal structural and functional hemispheric asymmetries (for reviews see: Konrad and Eickhoff, 2010; van Ewijk et al., 2012). In this context, a basic notion holds that undermined relative right-hemispheric functions involved in the regulation of attention and arousal may contribute to ADHD symptoms (Almeida et al., 2010; Fassbender and Schweitzer, 2006; Hale et al., 2009b, 2010b). Complementary notions highlight the importance of potentially disrupted interhemispheric connectivity (Hale et al., 2009a; Roessner et al., 2004).
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2014, Research in Developmental DisabilitiesCitation Excerpt :Although most studies on ADHD address sagittal topographical differences in EEG reactivity following eye opening, to our knowledge EEG differences between groups on the lateral plane (i.e., left hemisphere, midline and right hemisphere) have hardly been investigated. Yet, this may be important, since a few studies documented hemispherical divergence in EEG activity in ADHD (Hale et al., 2009; Hale, Smalley, Dang, et al., 2010; Hale, Smalley, Walshaw, et al., 2010; Keune et al., 2011). Therefore, in the present study, sagittal as well as lateral scalp regions were included, enabling a thorough investigation of possible topographical differences between groups and conditions.
Neurophysiologic predictors of response to atomoxetine in young adults with attention deficit hyperactivity disorder: A pilot project
2014, Journal of Psychiatric Research
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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).