Negative emotions enhance memory-guided attention in a visual search task by increasing frontoparietal, insular, and parahippocampal cortical activity

Previous literature has demonstrated that long-term memory representations guide the deployment of attentional resources during visual search in real-world pictures. However, it is currently unknown whether such a memory-guided visual search effect might be affected by the emotional context of the picture. Here, we addressed this question using functional magnetic resonance imaging (fMRI). Participants were asked to encode the position of a high-contrast target stimulus embedded in emotional (negative or positive) or neutral pictures. At retrieval, they performed a visual search for the target presented at the same location as encoding, but at a much lower contrast. Behavioral data showed that negative emotional pictures enhanced the effect of memory-guided attention, improving participants’ target detection performance. At the neural level, this effect was supported by increased activation in a large circuit of regions involving the dorsal and ventral frontoparietal cortex, insular and parahippocampal cortex. We propose that these regions might form an integrated neural circuit that is recruited to select and process previously encoded target locations (i.e., memory-guided attention sustained by the frontoparietal cortex) embedded in emotional contexts (i.e., emotional contexts recollection supported by the parahippocampal cortex and emotional monitoring supported by the insular cortex). Ultimately, these findings reveal that negative emotions can enhance memory-guided visual search performance by increasing neural activity in a large-scale brain circuit, contributing to disentangle the complex relationship between emotion, attention, and memory.