Atypical alpha asymmetry in adults with ADHD

Abstract

Introduction

A growing body of literature suggests atypical cerebral asymmetry and interhemispheric interaction in ADHD. 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). Increased rightward alpha asymmetry has been associated with ADHD-like traits such as reduced reward responsiveness, a lack of inhibition toward aversive experience, and increased approach behaviors, and previous work has indicated increased rightward alpha asymmetry in children with ADHD. The current study explores whether increased rightward alpha asymmetry is also evident in adults with ADHD.

Method

We assessed low (8–10 Hz) and high (10–12 Hz) alpha asymmetry in adults with ADHD (n = 29) versus controls (n = 62) during baseline and cognitive activation conditions for nine homologous electrode pairs along the anterior–posterior axis. Result: Seven results emerged (p < .05) showing increased rightward alpha asymmetry in adults with ADHD. This occurred in three specific electrode pairs across two testing conditions, and five of six results occurred in the lower alpha band. Finally, post hoc analysis indicated that increased rightward alpha asymmetry was generally associated with greater numbers of ADHD symptoms—with a possible parietal association for inattentive and a fronto-temporal association for hyperactivity symptoms.

Conclusions

Increased rightward alpha asymmetry previously observed in children with ADHD appears to be a developmentally persistent feature of 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).