Differentiating SCT and inattentive symptoms in ADHD using fMRI measures of cognitive control

Abstract

Attention Deficit/Hyperactivity Disorder (ADHD) is associated with different impairment profiles in the symptom domains of hyperactivity/impulsivity and/or inattention. An additional symptom domain of sluggish cognitive tempo (SCT) has also been proposed. Although there is a degree of correlation between the SCT symptom domain and inattention, it has been proposed as a distinct disorder independent of ADHD. The objective of this study was to examine the neural substrates of cue-related preparatory processes associated with SCT symptoms versus inattentive symptoms in a group of adolescents with ADHD. We also compared cue-related effects in the entire ADHD group compared with a group of typically developing (TD) peers. A modified cued flanker paradigm and fMRI examined brain activity associated with attention preparation and motor response preparation. Between group contrasts between the ADHD and TD group revealed significant hypoactivity in the ADHD group during general attention preparation in the supplementary motor area (SMA) and in the right superior parietal lobe (SPL) during response preparation. In the ADHD group, greater numbers of SCT symptoms were associated with hypoactivity in the left SPL to cues in general whereas greater numbers of inattentive symptoms were associated with greater activity in the SMA to cues that provided no information and less activity in the thalamus during response preparation. Hypoactivity in the SPL with increasing SCT symptoms may be associated with impaired reorienting or shifting of attention. Altered activity in the SMA and thalamus with increasing inattention may be associated with a general problem with response preparation, which may also reflect inefficient processing of the response preparation cue. Our results support a degree of differentiation between SCT and inattentive symptom profiles within adolescents with ADHD.

Keywords: ADHD; Adolescent; Cognitive control; Sluggish cognitive tempo; fMRI.

Fig. 1

Two trials from our modified flanker task. In this example yellow is the informative color. The top trial demonstrates the response preparation cue. The left hand in yellow indicates that a left hand response will be required to the following flanker. The bottom trial demonstrates the null cue. The null cue provides no information about the nature of the following flanker or the response that will be required. All stimuli were surrounded by a white border and participants were instructed to restrict their gaze within it; the inter-trial interval was indicated by a color change of the surrounding border from white to green.

Fig. 2

Reaction times to null, response preparation and warning cues. Both groups benefited from response preparation (RP) cues in the form of faster RT.

Fig. 3

Top panels: conjunction maps displaying brain activity during correct incongruent trials. A) TD group and B) ADHD group different red, orange and yellow colors represent the activation to correct incongruent trials during the different cue conditions; red = null cues; orange = response preparation cues; and yellow = warning cues. The remaining colors represent regions of overlap between these conditions and overlap between them. Green represents areas of overlap between activation during correct incongruent stimuli during all the cue types. Less differentiation between cue types is observed in the ADHD group. Regions of the basal ganglia, bilateral frontal and medial frontal regions were associated with uncued trials only (red) with activation in similar regions all cue types (in green). Bottom panel: C) between group activation: the TD group displayed greater activity than the ADHD group during response preparation cued incongruents in R SPL (dark blue) and during warning cued trials in the SMA (light blue).

Fig. 4

Significant correlations with symptoms. IA = inattentive symptoms, SCT = sluggish cognitive tempo symptoms. Red text labels indicate positive correlations, blue text labels indicate negative correlations. A) Significant correlations with symptoms for null cue trials. Dark blue cluster indicates a negative correlation with SCT in L SPL with or without controlling for inattentive symptoms. Light blue voxels are only significant when we control for inattentive symptoms. The orange cluster represents a positive correlation with inattentive symptoms in SMA. B) Significant correlations with symptoms for cued trials. Green clusters indicate negative correlations with SCT in bilateral SPL and SMA when not controlling for inattentive symptoms. Dark blue is a negative correlation with SCT in L SPL with or without controlling for inattentive symptoms. Light blue voxels represent a negative correlation with SCT when controlling for inattentive symptoms in L SPL. The violet clusters are negative correlations with inattentive symptoms in bilateral thalamus.