Independent oscillatory patterns determine performance fluctuations in children with attention deficit/hyperactivity disorder

Abstract

The maintenance of stable goal-directed behaviour is a hallmark of conscious executive control in humans. Notably, both correct and error human actions may have a subconscious activation-based determination. One possible source of subconscious interference may be the default mode network that, in contrast to attentional network, manifests intrinsic oscillations at very low (<0.1 Hz) frequencies. In the present study, we analyse the time dynamics of performance accuracy to search for multisecond periodic fluctuations of error occurrence. Attentional lapses in attention deficit/hyperactivity disorder are proposed to originate from interferences from intrinsically oscillating networks. Identifying periodic error fluctuations with a frequency <0.1 Hz in patients with attention deficit/hyperactivity disorder would provide a behavioural evidence for such interferences. Performance was monitored during a visual flanker task in 92 children (7- to 16-year olds), 47 with attention deficit/hyperactivity disorder, combined type and 45 healthy controls. Using an original approach, the time distribution of error occurrence was analysed in the frequency and time–frequency domains in order to detect rhythmic periodicity. Major results demonstrate that in both patients and controls, error behaviour was characterized by multisecond rhythmic fluctuations with a period of ∼12 s, appearing with a delay after transition to task. Only in attention deficit/hyperactivity disorder, was there an additional ‘pathological’ oscillation of error generation, which determined periodic drops of performance accuracy each 20–30 s. Thus, in patients, periodic error fluctuations were modulated by two independent oscillatory patterns. The findings demonstrate that: (i) attentive behaviour of children is determined by multisecond regularities; and (ii) a unique additional periodicity guides performance fluctuations in patients. These observations may re-conceptualize the understanding of attentive behaviour beyond the executive top-down control and may reveal new origins of psychopathological behaviours in attention deficit/hyperactivity disorder.