Dissociable effects of bottom-up and top-down factors on the processing of unattended fearful faces

Abstract

While the role of attention in determining the neural fate of unattended emotional items has been investigated in the past, it remains unclear whether bottom-up and top-down factors have differential effects in shaping responses evoked by such stimuli. To study the effects of bottom-up and top-down factors on the processing of neutral and fearful faces, we employed functional magnetic resonance imaging (fMRI) while participants performed attentional tasks that manipulated these factors. To probe the impact of top-down mechanisms on the processing of face distractors, target letters either had to be found among several distinct nontarget letters (attentional load condition) or among identical nontarget letters (baseline condition). To probe the impact of bottom-up factors, we decreased the salience of the targets by reducing their size and contrast relative to baseline (salience condition). Our findings revealed that bottom-up and top-down manipulations produced dissociable effects on amygdala and fusiform gyrus responses to fearful-face distractors when task difficulty was equated. When the attentional load of the main task was high, weaker responses were evoked by fearful-face distractors relative to baseline during the early trials. By contrast, decreasing target salience resulted in increased responses relative to baseline. The present findings suggest that responses evoked by unattended fearful faces are modulated by several factors, including attention and stimulus salience.

Figure 1

Sample stimulus displays containing face distractors for the (A) attentional load, (B) baseline, and (C) salience conditions (stimuli not drawn to scale).

Figure 2

General task activation in the absence of face distractors. (A) Contrasting responses during the salience condition to those during the baseline revealed decreased amygdala activity. (B) Contrasting responses during the attentional load condition to those during baseline revealed decreased amygdala activity (left) but increased left fusiform gyrus activity (right). See Methods for contrast abbreviations.

Figure 3

Time-related activity evoked by fearful and neutral distractors (early vs. late contrasts). During the salience condition, stronger responses to fearful (A) and neutral distractors (B) were observed in both the right amygdala (left) and the bilateral fusiform gyrus (right) during early trials. During the attentional load condition, weaker responses to fearful distractors were observed in both the amygdala and the fusiform gyrus (C) during early trials; weaker responses to neutral distractors were observed in the right fusiform gyrus during early trials (D). See Methods for contrast abbreviations.

Figure 4

Task effects on responses evoked by fearful and neutral distractors during early trials. (A,B,C) Conditions involving fearful-face distractors. (A) Responses evoked by fearful and neutral distractors during the salience condition were stronger relative to baseline both in the right amygdala (left) and the bilateral fusiform gyrus (right). (B) Responses evoked by fearful distractors during the attentional load condition were weaker relative to baseline both in the left amygdala (left) and the right fusiform gyrus activity (right). (C) Responses evoked by fearful distractors during the salience condition were stronger relative to the attentional load condition in both the right amygdala (left) and the bilateral fusiform gyrus (right). (D,E,F). Conditions involving neutral-face distractors exhibited similar activation profiles. See Methods for contrast abbreviations.

Figure 5

Valence effects. Stronger responses to fearful- relative to neutral-face distractors were observed in the amygdala during early trials for the (A) baseline (B) attentional load, and (C, left) salience conditions; for the latter condition, fusiform gyrus activity was also observed (C, right). During late trials, stronger responses to fearful- relative to neutral-face distractors were observed in the left amygdala for the attentional load condition (D). See Methods for contrast abbreviations.

Figure 6

Mean (A) accuracy and (B) reaction time as a function of task manipulations and the presence of face distractors during early trials.