Prefrontal oxygenation during working memory in ADHD

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Abstract

Objectives

Deficits in working memory have been repeatedly found on a behavioural level in children with attention-deficit/hyperactivity disorder (ADHD). Functional brain imaging studies have revealed evidence for alterations in the prefrontal cortex associated with working memory. So far it remains unresolved whether object (OWM) and spatial visual working memory (SWM) are distinctly impaired in ADHD. We investigated this issue with the fist multi-channel functional near-infrared spectroscopy study of children with ADHD.

Method

We investigated 19 children with ADHD combined type (DSM-IV) and 19 controls matched for age (8–15 years), sex, handedness, and intelligence during a working memory task assessing OWM and SWM separately, and a control condition (CON). Prefrontal brain activity was measured by concentration changes of oxygenated haemoglobin.

Results

Working memory performance showed significant differences for conditions (OWM > SWM > CON), but no differences between groups. Cortical prefrontal activation was significantly higher for OWM and SWM in contrast to CON, again with no differences between groups.

Conclusions

We found no indication for an altered prefrontal processing during OWM and SWM tasks in ADHD children compared to controls. Reviewing the existing imaging literature on working memory in ADHD and considering the present data, we discuss possible confounding factors relevant for brain activity in previous, the current, and future investigations. Thus, it is of high importance to capture developmental trajectories, task specific discrepancies, and effects of permanent medication intake in future studies.

Introduction

According to the theoretical concept of Baddeley, 2003, Baddeley, 2001 working memory (WM) consists of manipulation, maintenance, and storage of different types of material. In the following, the notation of “WM component” is indicated by the material (verbal, object or spatial visual) that subjects are required to manipulate. “WM process” mirrors the cognitive activity, i.e. the manipulation (e.g. mental rotation), storage, or simple repetition (rehearsal) of material. WM is a function assumed to be mainly processed in the prefrontal cortex, but also in parietal areas and the cerebellum (Owen et al., 2005, Vance et al., 2007).

Meta-analyses indicate neuropsychological WM performance deficits in children and adolescents (Martinussen et al., 2005, Willcutt et al., 2005), and adults with attention-deficit/hyperactivity disorder (ADHD) (Boonstra et al., 2005, Hervey et al., 2004, Schoechlin and Engel, 2005, Woods et al., 2002). Functional and anatomical alterations are well established in the frontal cortex in ADHD (Durston, 2003, Ehlis et al., 2008, Schneider et al., 2006). Various functional imaging investigations on WM (compare Table 1) affirm these findings both in children and adolescents (Kobel et al., 2008, Sheridan et al., 2007, Silk et al., 2005, Vance et al., 2007), and in adults with ADHD (Ehlis et al., 2008, Hale et al., 2007, Schweitzer et al., 2006, Valera et al., 2005, Wolf et al., 2008). In six of these nine studies, patients showed altered brain activation in the prefrontal cortex (compare Table 1).

However, so far neither above mentioned meta-analyses nor recent studies (Clark et al., 2007, Schweitzer et al., 2006) found a specific WM component or process to be associated with ADHD. The reason for this might be the fact that different components or processes were rarely tested in one sample at the same time. To our knowledge only one study simultaneously investigated spatial, object, and verbal WM revealing group differences for the latter two tasks (Pasini et al., 2007).

Thus, in the current study prefrontal oxygenation changes were investigated by functional near-infrared spectroscopy (fNIRS) in children with ADHD combined type and matched healthy controls. Our investigation is the first study applying multi-channel fNIRS in a relevantly sized sample of children with ADHD. Only three fNIRS investigations on samples sized 10–12 have previously been performed in children with ADHD applying an unspecific psychomotor test in two investigations with two fNIRS channels and a Stroop task with four channels in the other study (Weber et al., 2005, Weber et al., 2007, Moser et al., 2009). Our investigation is the first study assessing specific working memory functions, i.e. object (OWM) and spatial visual working memory (SWM) as well as processes of the slave systems (storage and rehearsal) and the central executive (matching of stimuli held in short term memory). We expected diminished performance and altered brain activity in patients with ADHD in contrast to comparable controls in several prefrontal cortical areas, possibly accentuated for object working memory (Pasini et al., 2007).

Section snippets

Subjects

We examined a total of 38 individuals, 19 out-patient children with ADHD combined type (DSM-IV, American Psychiatric Association) and 19 healthy control children. Patients were recruited and diagnosed within the framework of a nationally funded research project (Deutsche Forschungsgemeinschaft, KFO 125-1) ensuring a qualitatively high diagnostic standard. All ADHD patients were evaluated by a semi-structured interview (Kiddie-Sads – Present and Lifetime Version, German Version; Kaufman et al.,

Results

For behavioural data (Fig. 2) we found main effects of task condition (correct responses: F = 91.2; df = 2,72; p < 0.001; η2 = 0.717; reaction time: F = 360.8; df = 2,72; p < 0.001; η2 = 0.909) and no main effects of group (correct responses: F = 0.6; df = 1,36; p = 0.463; η2 = 0.015; reaction time: F = 0.3; df = 1,36; p = 0.614; d = 0.007) or condition by group interaction effects (correct responses: F = 1.1; df = 2,72; p = 0.335; η2 = 0.030; reaction time: F < 0.1; df = 2,72; p = 0.999; η2 < 0.001). Subjects had inferior performance for

Discussion

We investigated children with ADHD combined type and matched healthy controls during an fNIRS task differentiating face object (OWM) and spatial visual working memory (SWM) and furthermore differentiating a storage (memorizing of three stimuli) and a matching component. The storage and matching component correspond to processes of the slave systems or the central executive, respectively, in Baddeley’s model of working memory (Baddeley, 2003, Baddeley, 2001). Performance differences between the

Contributors

Authors Martin Schecklmann and Marcel Romanos designed the study, managed the literature searches and analyses, and wrote the first draft of the manuscript. Franziska Bretscher undertook the biggest part of the measurements. Martin Schecklmann and Michael Plichta undertook the statistical analyses. Andreas Warnke and Andreas Fallgatter supervised the study. All authors contributed to and have approved the final manuscript.

Role of the founding source

The study was supported by the Deutsche Forschungsgemeinschaft, KFO 125-1, i.e. the appointment of Martin Schecklmann and Michael Plichta, and the compensation for participation of the subjects (cinema coupons) was funded. The KFO 125-1 had no role in the study design, the collection, analyses, and interpretation of the data, the writing of the manuscript, and the decision to submit the paper for publication.

Conflict of interest

The authors report no conflicts of interest.

Acknowledgements

The authors would like to thank Hitachi Medical Corporation for the ETG-4000 equipment and Renate Huttner for the language proofreading. The study was supported by the Deutsche Forschungsgemeinschaft, KFO 125-1.

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