Neurophysiological Correlates of Attentional Fluctuation in Attention-Deficit/Hyperactivity Disorder

Celeste H M Cheung,Jonna Kuntsi,Daniel Brandeis,Philip Asherson,Gráinne Mcloughlin,Tobias Banaschewski

doi:10.1007/s10548-017-0554-2

Abstract

Cognitive performance in attention-deficit/hyperactivity disorder (ADHD) is characterised, in part, by frequent fluctuations in response speed, resulting in high reaction time variability (RTV). RTV captures a large proportion of the genetic risk in ADHD but, importantly, is malleable, improving significantly in a fast-paced, rewarded task condition. Using the temporal precision offered by event-related potentials (ERPs), we aimed to examine the neurophysiological measures of attention allocation (P3 amplitudes) and preparation (contingent negative variation, CNV), and their associations with the fluctuating RT performance and its improvement in ADHD. 93 participants with ADHD and 174 controls completed the baseline and fast-incentive conditions of a four-choice reaction time task, while EEG was simultaneously recorded. Compared to controls, individuals with ADHD showed both increased RTV and reduced P3 amplitudes during performance on the RT task. In the participants with ADHD, attenuated P3 amplitudes were significantly associated with high RTV, and the increase in P3 amplitudes from a slow baseline to a fast-paced, rewarded condition was significantly associated with the RTV decrease. Yet, the individuals with ADHD did not show the same increase in CNV from baseline to fast-incentive condition as observed in controls. ADHD is associated both with a neurophysiological impairment of attention allocation (P3 amplitudes) and an inability to adjust the preparatory state (CNV) in a changed context. Our findings suggest that both neurophysiological and cognitive performance measures of attention are malleable in ADHD, which are potential targets for non-pharmacological interventions.

Highlights

Inconsistent performance on reaction time tasks is one of the most prominent features of cognitive performance in attention-deficit/ hyperactivity disorder (ADHD) (Kofler et al 2013; Tamm et al 2012)
In the participants with ADHD, attenuated P3 amplitudes were significantly associated with high reaction time variability (RTV), and the increase in P3 amplitudes from a slow baseline to a fast-paced, rewarded condition was significantly associated with the RTV decrease
First, that ADHD is associated with attenuated P3 amplitudes during performance on an RT task, indicating difficulties with attentional resource allocation

Summary

Introduction

Inconsistent performance on reaction time tasks is one of the most prominent features of cognitive performance in ADHD (Kofler et al 2013; Tamm et al 2012). We further demonstrated that RTV baseline performance (in a slowunrewarded condition) measures the same aetiological process as captured by the RTV improvement across conditions (from the baseline condition to a fast rewarded condition) (Kuntsi et al 2012). These findings support theories that emphasise the malleability of the observed high RTV in ADHD, such as those that link ADHD to difficulties regulating arousal (Halperin et al 2008; Johnson et al 2007; O’Connell et al 2009; Sergeant 2005; Van der Meere 2002). While RTV captures a large proportion of the familial influences underlying ADHD, it largely separates from a second familial cognitive impairment in ADHD that captures executive control processes, such as response inhibition (Kuntsi et al 2010)

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