Executive attention control and emotional responding in attention-deficit/hyperactivity disorder--A functional MRI study

Soonjo Hwang, Stuart F White, Zachary T Nolan, W Craig Williams, Stephen Sinclair, R J R Blair, Soonjo Hwang, Stuart F White, Zachary T Nolan, W Craig Williams, Stephen Sinclair, R J R Blair

Abstract

Background: There are suggestions that patients with attention-deficit/hyperactivity disorder (ADHD) show impairment in executive attention control and emotion regulation. This study investigated emotion regulation as a function of the recruitment of executive attention in patients with ADHD.

Methods: Thirty-five healthy children/adolescents (mean age = 13.91) and twenty-six children/adolescents with ADHD (mean age = 14.53) participated in this fMRI study. They completed the affective Stroop paradigm viewing positive, neutral and negative images under varying cognitive loads. A 3-way ANOVA (diagnosis-by-condition-by-emotion) was conducted on the BOLD response data. Following this, 2 3-way ANOVAs (diagnosis-by-condition-by-emotion) were applied to context-dependent psychophysiological interaction (gPPI) analyses generated from a dorsomedial frontal cortex and an amygdala seed (identified from the BOLD response ANOVA main effects of condition and emotion respectively).

Results: A diagnosis-by-condition interaction within dorsomedial frontal cortex revealed reduced recruitment of dorsomedial frontal cortex as a function of increased task demands in the children/adolescents with ADHD relative to healthy children/adolescents. The level of reduction in recruitment of dorsomedial frontal cortex was significantly correlated with symptom severity (total and hyperactivity) measured by Conner's Parent Report Scale in the children/adolescents with ADHD. In addition, analysis of gPPI data from a dorsomedial frontal cortex seed revealed significant diagnosis-by-condition interactions within lateral frontal cortex; connectivity between dorsomedial frontal cortex and lateral frontal cortex was reduced in the patients with ADHD relative to comparison youth during congruent and incongruent task trials relative to view trials. There were no interactions of group, or main effect of group, within the amygdala in the BOLD response ANOVA (though children/adolescents with ADHD showed increased responses to positive images within temporal cortical regions during task trials; identified by the diagnosis-by-condition-by-emotion interaction). However, analysis of gPPI data from an amygdala seed revealed decreased connectivity between amygdala and lentiform nucleus in the presence of emotional stimuli in children/adolescents with ADHD (diagnosis-by-emotion interaction).

Conclusion: The current study demonstrated disrupted recruitment of regions implicated in executive function and impaired connectivity within those regions in children/adolescents with ADHD. There were also indications of heightened representation of emotional stimuli in patients with ADHD. However, as the findings were specific for positive stimuli, the suggestion of a general failure in emotion regulation in ADHD was not supported.

Keywords: Affective Stroop; Attention-deficit/hyperactivity disorder; Emotion regulation; Executive attention; fMRI.

Figures

Fig. 1
Fig. 1
Experiment design. Example trial sequences: (a) positive view trial; (b) positive congruent trial; (c) positive incongruent trial.
Fig. 2
Fig. 2
Dorsomedial frontal cortex region showing a significant diagnosis-by-condition interaction and fusiform gyri showing significant diagnosis-by-condition-by-emotion interactions. (A) Right dorsomedial frontal gyrus (coordinates: 1.5, 1.5, 53.5) showing a significant group-by-condition interaction; (B) parameter estimates for right dorsomedial frontal gyrus; (C) negative correlation between symptom severity as measured by Conner parent report scale and BOLD response to incongruent-view trials right dorsomedial frontal gyrus in patients with ADHD; (D) and (F) left fusiform gyri (coordinates: − 37.5, − 58.5, − 12.5 and − 22.5, − 55.5, − 6.5, respectively) showing a significant group-by-condition-by-emotion interaction; (E) and (G) parameter estimates for left fusiform gyri. *: regressor contrasts showing significant group differences. (B), (E), (G) Y axis — parameter estimates. Incong_View: incongruent trials — view trials; Cong_View: congruent trials — view trials; Neg_Neu_Incong: negative incongruent trials — neutral incongruent trials; Neg_Neu_Cong: negative congruent trials — neutral congruent trials; Neg_Neu_View: negative view trials — neutral view trials; Pos_Neu_Incong: positive incongruent trials — neutral incongruent trials; Pos_Neu_Cong: positive congruent trials — neutral congruent trials; Pos_Neu_View: positive view trials — neutral view trials.
Fig. 3
Fig. 3
GPPI connectivity data: (A) lateral frontal gyrus (coordinates: 46.5, 16.5, 35.5) showed a significant diagnosis-by-task interaction in connectivity with right dorsomedial frontal gyrus seed; (B) parameter estimates for lateral frontal gyrus. (C) left lentiform nucleus (coordinates: − 22.5, − 7.5, − 0.5) showing a significant diagnosis-by-emotion interaction in connectivity with right amygdala seed and; (D) parameter estimates for left lentiform nucleus. (B), (D) Y axis: parameter estimates. Incong_View: incongruent trials — view trials; Cong_View: congruent trials — view trials; Neg_Neu: negative trials — neutral trials; Pos_Neu: positive trials — neutral trials.

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