EEG coherence in attention-deficit/hyperactivity disorder: a comparative study of two DSM-IV types

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Abstract

Objectives: This study investigated differences in intrahemispheric and interhemispheric electroencephalographic (EEG) coherences between attention-deficit/hyperactivity disorder (ADHD) and control children, and between children with the Combined (ADHDcom) and Inattentive (ADHDin) types of ADHD.

Methods: Three age- and sex-matched groups of 40 children, aged 8–12 years, diagnosed with ADHDcom, ADHDin, and normal control children, participated in this study. EEG was recorded from 21 sites during an eyes-closed resting condition and Fourier transformed. Wave-shape coherence was calculated for 8 intrahemispheric electrode pairs (4 in each hemisphere), and 8 interhemispheric electrode pairs, within each of the delta, theta, alpha and beta bands.

Results: At shorter inter-electrode distances, ADHD children had elevated intrahemispheric coherences in the theta band and reduced lateral differences in the theta and alpha bands. At longer inter-electrode distances, ADHD children had lower intrahemispheric alpha coherences than controls. Frontally, ADHD children had interhemispheric coherences elevated in the delta and theta bands, and reduced in the alpha band. An alpha coherence reduction in temporal regions, and a theta coherence enhancement in central/parietal/occipital regions, were also apparent. ADHDcom had greater intrahemispheric theta and beta coherences than ADHDin. Frontally, ADHDcom had higher levels of interhemispheric coherences than ADHDin for the delta and theta bands. In central/parietal/occipital regions, beta coherences were elevated in ADHDcom.

Conclusions: EEG coherences suggest reduced cortical differentiation and specialisation in ADHD, particularly in cortico-cortical circuits involving theta activity. Generally, ADHDcom children displayed greater anomalies than ADHDin children.

Introduction

Both cognition and behaviour depend on the integrated activity of different brain regions, and hence study of the coupling between regions would seem useful in understanding both normal brain function and the important processes involved in a range of brain dysfunctions. Most electroencephalographic (EEG) studies utilise power estimates within the traditional frequency bands, providing little information about the coupling of brain activity between different recording sites. The coherence of the EEG activity between two sites, conceptualised as the correlation in the time domain between two signals in a given frequency band (Shaw, 1981), provides just that information. Normal brain development from birth to the pre-adult years involves periods of both synaptic proliferation and pruning. These processes presumably underlie the observed systematic waxing and waning in coherence levels (e.g. Thatcher et al., 1987, Thatcher, 1994). From about 4 to 6 years, a growth spurt mainly involves increasing coherence in the frontal regions and left frontal–occipital coupling. From 8 to 10, another spurt involves fronto-temporal connections in the right hemisphere. Further spurts occur from about 11 to 14 years and from 15 years to adulthood, and are interpreted as reflecting the sequencing of development of different anatomical systems. This cyclic pattern complicates the interpretation of observed changes or differences in coherence.

Gasser et al. (1987) investigated coherence at rest and in a visual-matching task in normal and mildly retarded children aged 10–13 years. Coherences were generally higher and more variable in the mentally retarded group than in normal children. There were only slight age effects, with small increases in coherence with age in the normals. In younger (3 months to 7 years) mentally retarded children (mostly mildly and moderately retarded), Shibagaki et al. (1982) were unable to find evidence that coherence values were age-related. Marosi et al. (1995) examined EEG coherences in 3 groups of children differing on reading–writing ability. Generally, poor performance was associated with higher coherences in the delta, theta and beta bands, and reduced coherences in the alpha band. In older children, these differences were reduced, particularly in the theta, alpha and beta bands. In a follow-up study of these same children over a 2–3 year interval (Marosi et al., 1997), group differences remained, and a general increase in coherence was noted, except in the theta band, with most changes occurring in the alpha band.

Thatcher et al. (1986) advanced a two-process model of cortico-cortical associations in which short and long neuronal fibres contribute differentially to coherence as a function of inter-electrode distance. At longer distances, coherence is mainly dependent on the longer fibres alone, increases with their density/development, and falls off systematically with increasing inter-electrode distance. In contrast, increased density/development of short fibres in specialised neuronal populations reduces coherence by increasing the complexity and competition of interactions within the cell population. This two-compartment model appears to accommodate much of the existing coherence data, and has wide currency in the literature. For example, the increased coherence reported in children with intellectual impairment and reading disability (Gasser et al., 1987, Marosi et al., 1995), may be understood as reflecting decreased cortical differentiation compared with normal controls.

One of the most common disabilities of childhood listed in the DSM-IV (APA, 1994) is attention-deficit/hyperactivity disorder (ADHD). There are numerous EEG studies of ADHD using absolute and relative power estimates, mean frequencies from the traditional frequency bands, and power ratios (e.g. Dykman et al., 1982, Satterfield et al., 1972, Matousek et al., 1984, Lubar et al., 1985, Lubar, 1991, Mann et al., 1992, Janzen et al., 1995, Chabot and Serfontein, 1996, Lazzaro et al., 1998, Callaway et al., 1983). Work from our laboratory has confirmed that ADHD subjects have increased levels of absolute and relative theta, and a decrease in posterior relative beta and alpha (Bresnahan et al., 1999, Clarke et al., 1998, Clarke et al., 2001a, Clarke et al., 2001b). Children with ADHD were also found to have higher delta/theta, theta/alpha and theta/beta ratios, higher mean frequency in the delta band and lower mean frequencies in the alpha and beta bands (Clarke et al., 2001c). In our studies, children with the Inattentive type of ADHD (ADHDin) had some EEG abnormalities that were similar to those with the Combined type (ADHDcom), but less extreme, while topographic differences suggested that the Combined type had abnormalities in the frontal regions that were not present in the Inattentive type. Further investigation of maturational changes indicated that there was an EEG component associated with hyperactivity/impulsivity that matured with age and an inattentive component that was more pervasive (Clarke et al., 2001a).

In contrast to these studies, EEG coherence has not been investigated thoroughly in the ADHD context. An early study of hyperkinetic children by Montagu (1975) examined interhemispheric and intrahemispheric (right hemisphere only) coherences in 2 Hz bands (to 10 Hz) relative to normal children. Interhemispheric coherences were slightly (non-significantly) reduced in the hyperkinetic children, while intrahemispheric coherences were generally significantly elevated (the 10 Hz elevation was not significant). Chabot and Serfontein, 1996, Chabot et al., 1996 reported on a mixed group of attention disorder patients (43.9% ADHD, 40.5% ADD by DSM-III criteria, and 15.6% not meeting those criteria) aged 6–17 years, some of whom had learning disabilities. They found that attention disorders were associated with interhemispheric and intrahemispheric hypercoherence in frontal and central regions, based on comparisons with a normal control group from the John et al. (1980) database. There was also generally reduced coherence parietally. Chabot et al. (1999) reported pre-medication coherence data from a similar patient mix, using a subset of patients from their previous studies, and again noted increased frontal interhemispheric coherence, particularly in the theta and alpha bands, and increased intrahemispheric coherence bilaterally in fronto-temporal regions. Unfortunately, many of the coherence differences noted in these reports do not specify the frequency ranges involved.

This study examined interhemispheric and intrahemispheric coherences in the standard EEG frequency bands in two types of ADHD children, and age-matched normal controls. The aim was to investigate the usefulness of coherence measures in clarifying brain function in ADHD, and to examine the nature of the EEG differences between the two most common DSM-IV types of the disorder.

Section snippets

Subjects

Three groups of 40 children (32 boys and 8 girls, representing the approximate gender ratio in ADHD) participated. The EEG power data from these children were presented in Clarke et al. (2001c). All were aged 8–12 years, were right handed and footed, and had a full-scale WISC-III IQ score of 85 or higher. The groups used were children diagnosed with ADHDcom or ADHDin and a control group. Both clinical groups of children were drawn from new patients presenting at a Sydney-based paediatric

Results

As shown in Table 1, the groups did not differ on age. Across types, the ADHD children had a significantly lower mean IQ than the control group (F(1,118)=50.36, P<0.001), but the types did not differ on IQ.

The mean coherences from each pair of electrodes are shown in Table 2 for each group within each frequency band. These data were grouped into regions and analysed as outlined above.

Discussion

The intrahemispheric coherences from short-medium inter-electrode distances showed significant lateralisation, pointing to the existence of substantial hemispheric differentiation. The higher levels noted in all frequency bands in the left hemisphere suggests that general differentiation has progressed further in the right hemisphere than the left. Although this was not expected from previous suggestions of coherences being larger in the right than left hemisphere (e.g. Tucker et al., 1986,

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