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

Brain. 2011 Jun;134(Pt 6):1740-50. doi: 10.1093/brain/awr107.

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.

Publication types

  • Randomized Controlled Trial
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Attention / physiology*
  • Attention Deficit Disorder with Hyperactivity / complications*
  • Child
  • Cognition Disorders / etiology*
  • Cognition Disorders / pathology
  • Electroencephalography / methods
  • Feedback
  • Female
  • Humans
  • Male
  • Neuropsychological Tests
  • Nonlinear Dynamics
  • Pattern Recognition, Visual
  • Periodicity*
  • Photic Stimulation
  • Reaction Time / physiology
  • Time Factors