Neurodevelopmental changes in the responsiveness of systems involved in top down attention and emotional responding

Abstract

In this study, we aimed to investigate age related changes in systems implicated in top down attention and the implications of this for amygdala responses to emotional distracters. Fifty-one healthy subjects including 18 children (aged 10-14), 15 adolescents (aged 14-18), and 18 young adults (aged 18-25) completed the affective Stroop paradigm while undergoing functional MRI. While achieving comparable behavioral performance, children, relative to adolescents and adults, showed increased activation in areas including anterior cingulate gyrus and precentral gyrus in task relative to view trials. In addition, children showed increased activation within the amygdala and fusiform gyrus in response to emotional stimuli. Notably, the group difference within the amygdala was particularly pronounced during task trials. Also children showed increased connectivity between amygdala and superior frontal gyrus and bilateral postcentral gyrii in response to negative task trials. These data are consistent with previous work indicating less consolidated functional integrity in regions implicated in top down attention in children relative to older participants and extend this work by indicating that this less consolidated functional integrity leads to reduced automatic emotion regulation as a function of top down attention. Given that reduced automatic emotion regulation as a function of top down attention is considered a risk factor for the development of anxiety disorders, these data may contribute to an understanding of the increased risk for the development of these disorders at this age.

Keywords: Affective Stroop; Amygdala; Anterior cingulate gyrus; Development; Emotion; Top-down attention.

Published by Elsevier Ltd.

Figures

Figure 1

Example trial sequences. (a) negative view trial; (b) negative congruent trial; (c) negative incongruent trial.

Figure 2

Regions showing increased activation during aST performance (p=0.005) as a significant interaction of group-by-task; (A) Children showed increased activation of right anterior cingulate (coordinates; 7.5, 13.5, 29.5) and left medial frontal gyrus (coordinates; −4.5, −4.5, 62.5) during incongruent trials relative to adolescents and young adults; (B), (C) Parameter estimates for these regions. * = significant contrasts. Incong: Incongruent; Cong: Congruent.

Figure 3

Regions showing increased activation during aST performance as a significant interaction of group-by-emotion; (A) Children showed increased activation of left fusiform gyrus (coordinates; −34.5, −49.5, −9.5) in response to negative trials, relative to adolescents and young adults; (B) parameter estimates for this interaction; (C) Children showed increased activation of right anterior cingulate gyrus (coordinates; 4.5, 25.5, −3.5) in response to negative trials, relative to adolescents and young adults; (D) Parameter estimates for this interaction; (E) Children showing greater difference of activation in left amygdala anatomical ROI (coordinates; −22.5, −1.5, −21.5) between emotional (negative and positive) stimuli and neutral stimuli, relative to adolescents and young adults; (F) Parameter estimates for this region. * = significant contrasts. Neg: Negative; Neu: Neutral; Pos: Positive.

Figure 4

(A) Children showed increased activation of right amygdala anatomical ROI (coordinates; 25.5, −1.5, −21.5)in response to negative task trials compared to neutral task trials, and positive view trials compared to neutral view trials, relative to adolescents and young adults; (B) Parameter estimate for this region. * = significant contrasts. NegT: Negative task trial; NeuT: Neutral task trial; NegV: Negative view trial; NeuV: Neutral view trial; PosT: Positive task trial; PosV: Positive view trial.

Figure 5

(A) Children showed significantly increased connectivity of right postcentral gyrus (coordinates; 19.5, −34.5, 53.5) with left amygdala anatomical ROI seed (coordinates; −22.5, −1.5, −21.5) in response to negative task trials compared to neutral task trials, relative to adolescents and young adults; (B) average activation of this region. * = significant contrasts. NegT: Negative task trial; NeuT: Neutral task trial; NegV: Negative view trial; NeuV: Neutral view trial; PosT: Positive task trial; PosV: Positive view trial.