Preparatory attentional templates in prefrontal and sensory cortex encode target-associated information

Visual search relies on the ability to use information about the target in working memory to guide attention and make target-match decisions. The representation of target features is referred to as the “attentional” or “target” template and is thought to be encoded within an inferior frontal junction (IFJ)-visual attentional network (Baldauf & Desimone, 2014; Bichot et al., 2015). The template typically contains veridical target information that is used to facilitate sensory processing of target during search. However, many behavioral studies have shown that target-associated information (e.g., statistically co-occurring object pairs) is used to guide attention, especially when target discrimination is difficult (Battistoni et al., 2017; de Lange et al., 2018; Peelen et al., 2024; Vo et al., 2019; Yu et al., 2023; Zhou & Geng, 2024). Thus, while target-associated information is known to impact search performance, its presence within the IFJ-visual attentional network during the preparatory period, before search begins, has never been demonstrated. Here, we use fMRI and multivariate pattern analysis to test if attentional guidance by target-associated information is explicitly represented in the preparatory period, either in conjunction with the target or even in place of it. Participants were first trained on four face-scene category pairings after which they completed a cued visual search task for the same faces. Each trial began with a face cue, followed by a delay period, and then a search display with two lateralized faces superimposed on scene images. The critical results showed that while face information could be decoded in the fusiform face area (FFA), superior parietal lobule (SPL), and dorsolateral prefrontal cortex (dLPFC) during the cue period, face information could not be decoded in any brain regions during the delay period. In contrast, the associated scene was decoded only in ventrolateral prefrontal cortex (vLPFC) during the cue period, but most importantly, in the IFJ and the parahippocampal place area (PPA) during the delay period. Our results are a novel demonstration that target-associated information from memory can supplant the veridical target in the brain’s “target template” in anticipation of difficult visual search.