A neural basis for real-world visual search in human occipitotemporal cortex

Abstract

Mammals are highly skilled in rapidly detecting objects in cluttered natural environments, a skill necessary for survival. What are the neural mechanisms mediating detection of objects in natural scenes? Here, we use human brain imaging to address the role of top-down preparatory processes in the detection of familiar object categories in real-world environments. Brain activity was measured while participants were preparing to detect highly variable depictions of people or cars in natural scenes that were new to the participants. The preparation to detect objects of the target category, in the absence of visual input, evoked activity patterns in visual cortex that resembled the response to actual exemplars of the target category. Importantly, the selectivity of multivoxel preparatory activity patterns in object-selective cortex (OSC) predicted target detection performance. By contrast, preparatory activity in early visual cortex (V1) was negatively related to search performance. Additional behavioral results suggested that the dissociation between OSC and V1 reflected the use of different search strategies, linking OSC preparatory activity to relatively abstract search preparation and V1 to more specific imagery-like preparation. Finally, whole-brain searchlight analyses revealed that, in addition to OSC, response patterns in medial prefrontal cortex distinguished the target categories based on the search cues alone, suggesting that this region may constitute a top-down source of preparatory activity observed in visual cortex. These results indicate that in naturalistic situations, when the precise visual characteristics of target objects are not known in advance, preparatory activity at higher levels of the visual hierarchy selectively mediates visual search.T he selection of complex stimuli, such as objects, from cluttered environments presents a complicated problem: during real-world visual search, objects are present at unspecified locations and may have an almost infinite number of possible visual appearances. Despite these difficulties, the detection of highly familiar object categories (e.g., people or cars) in natural scenes has been shown to be remarkably fast (1). Surprisingly, such detection is even possible in the near absence of spatial attention, by stark contrast to the detection of simple feature conjunctions (e.g., discriminating "T" from "L") under comparable task conditions (2). On the basis of these and other findings, it has been suggested that mechanisms related to the visual search for familiar objects in natural scenes may differ from those related to the visual search for simple shapes in artificial scenes, such as typically studied in the laboratory (3). In the present study, we investigated the brain mechanisms mediating the selection of objects in real-world scenes. Specifically, we addressed the role and nature of top-down preparatory processes in the detection of familiar object categories in daily life environments.Theoretical accounts of visual search hold that top-down preparatio...

The neural basis of attentional control in visual search

“…The activity of neurons in inferior temporal cortex (IT) that selectively respond to a particular object is enhanced in a sustained fashion while monkeys prepare to find this object in an upcoming search display (Figure 3a), and such preparatory "baseline shifts" of neural activity level may reflect an activated attentional template [7]. Similar target-selective preparatory activation patterns have been found in human event-related brain potential (ERP) and fMRI experiments [8][9][10][11][12][13][14]. Some fMRI studies have demonstrated increased activity in colour-or motion-selective visual areas when observers prepare for targets defined in these dimensions [9][10][11].…”

“…Although spatially global working memory representations do exist in visual cortex [15], the question whether preparatory goalselective patterns of visual activity are generally position-invariant, and whether this is a necessary requirement for their role as attentional templates still needs to be systematically addressed. 5 In line with the involvement of prefrontal cortex in visual working memory (Box 1), preparatory activation patterns that are sensitive to current task goals have also been observed in prefrontal areas [13,20,21]. These effects may be linked to top-down aspects of attentional preparation, with prefrontal cortex controlling target-selective preparatory modulations of visual activity, but could also reflect explicit representations of search goals.…”

“…The existence of correlations between the target-selectivity of preparatory pre-stimulus activation patterns in visual cortex and the quality of subsequent target detection performance [10,[12][13][14]16] suggests that preparatory modulations of visual activity might indeed act as attentional templates that are causally involved in the control of visual search. However, this conclusion is by no means universally accepted [17][18][19].…”

“…Others have found more globally distributed goal-sensitive activation patterns in visual cortex during the preparation of search for specific target shapes [12], or for target object categories in real-world visual scenes (e.g., people, cars, houses, faces [13,14]). The exact locus of preparatory activity patterns within the visual processing hierarchy may depend on the nature of the current search goal [12], with lower-level visual areas responsible for representing simple target features [15], and higher-level regions involved in the preparation for more abstractly defined targets [13].…”

EPS Mid-Career Award 2014

“…Preparation for a specific target shape elicited a shape-selective pattern of neural activation in lateral occipital cortex during the interval before the target was presented (Stokes, Thompson, Nobre, & Duncan, 2009). Even search for categorydefined target objects in natural visual scenes (e.g., people or cars) was found to be preceded by preparatory category-selective activation patterns in visual cortex (Peelen & Kastner, 2011). …”