Preparatory activity during visual search reflects attention-guiding objects rather than search targets

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Abstract

Efficient behavior requires the rapid attentional selection of task-relevant objects. Previous research has shown that target-selective neurons in visual cortex increase their baseline firing rate when participants are cued to search for a target object. Such preparatory activity represents a key finding for theories of visual search, as it may reflect a top-down bias that guides spatial attention, favoring processing of target-matching input for subsequent report. However, in daily life, visual search is often guided by non-target objects that are neither externally cued nor reported. For instance, when looking for a pen, we may direct our attention to the office desk where we expect the pen to be. These “anchor objects” (e.g., the desk) thereby guide search for associated objects (e.g., the pen) in scenes. Here, we used fMRI and eye tracking to test whether preparatory activity during visual search represents the target (the pen), the guiding anchor object (the desk) or both. In an anchor-guided search task, participants (N=34) learned associations between targets and anchors and searched for these targets in scenes. To fully dissociate target from anchor processing, target-anchor associations were reversed across different scene contexts. Participants’ first fixations were reliably guided towards the target-associated anchor. Importantly, preparatory fMRI activity patterns in lateral occipital cortex (LOC) represented the target-associated anchor rather than the target. Whole-brain analyses additionally identified a region in the right intraparietal sulcus that represented the anchor. Our results show that preparatory activity in visual cortex represents a self-generated guiding template, supporting visual search in structured daily-life environments.

Significance Statement

Quickly finding relevant objects in complex environments is challenging, yet we are remarkably efficient at it. Theories of attention propose that this is mediated by preparatory biases in visual cortex, such that, for example, looking for a blue pen increases the activity of neurons tuned to blue, elongated objects, favoring the processing of such objects once they appear in view. However, guidance is often based on features that are not the target: when looking for a pen, we first direct our attention to the office desk. Here we show that preparatory activity in visual cortex represents the features that are most useful for guidance (e.g., the desk), rather than the target, clarifying the role of preparatory activity in naturalistic search.

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