Prefrontal Cortex Codes Representations of Target Identity and Feature Uncertainty.

Many objects in the real world have features that vary over time, creating uncertainty in how they will look in the future. This uncertainty makes statistical knowledge about the likelihood of features critical to attention demanding processes such as visual search. However, little is known about how the uncertainty of visual features is integrated into predictions about search targets in the brain. In the current study, we test the idea that regions prefrontal cortex code statistical knowledge about search targets before the onset of search. Across 20 human participants (13 female; 7 male), we observe target identity in the multivariate pattern and uncertainty in the overall activation of dorsolateral prefrontal cortex (DLPFC) and inferior frontal junction (IFJ) in advance of the search display. This indicates that the target identity (mean) and uncertainty (variance) of the target distribution are coded independently within the same regions. Furthermore, once the search display appears the univariate IFJ signal scaled with the distance of the actual target from the expected mean, but more so when expected variability was low. These results inform neural theories of attention by showing how the prefrontal cortex represents both the identity and expected variability of features in service of top-down attentional control.SIGNIFICANCE STATEMENT Theories of attention and working memory posit that when we engage in complex cognitive tasks our performance is determined by how precisely we remember task-relevant information. However, in the real world the properties of objects change over time, creating uncertainty about many aspects of the task. There is currently a gap in our understanding of how neural systems represent this uncertainty and combine it with target identity information in anticipation of attention demanding cognitive tasks. In this study, we show that the prefrontal cortex represents identity and uncertainty as unique codes before task onset. These results advance theories of attention by showing that the prefrontal cortex codes both target identity and uncertainty to implement top-down attentional control.

Object-based attention during scene perception elicits boundary contraction in memory.

Boundary contraction and extension are two types of scene transformations that occur in memory. In extension, viewers extrapolate information beyond the edges of the image, whereas in contraction, viewers forget information near the edges. Recent work suggests that image composition influences the direction and magnitude of boundary transformation. We hypothesize that selective attention at encoding is an important driver of boundary transformation effects, selective attention to specific objects at encoding leading to boundary contraction. In this study, one group of participants (N = 36) memorized 15 scenes while searching for targets, while a separate group (N = 36) just memorized the scenes. Both groups then drew the scenes from memory with as much object and spatial detail as they could remember. We asked online workers to provide ratings of boundary transformations in the drawings, as well as how many objects they contained and the precision of remembered object size and location. We found that search condition drawings showed significantly greater boundary contraction than drawings of the same scenes in the memorize condition. Search drawings were significantly more likely to contain target objects, and the likelihood to recall other objects in the scene decreased as a function of their distance from the target. These findings suggest that selective attention to a specific object due to a search task at encoding will lead to significant boundary contraction.

Multisensory processing impacts memory for objects and their sources.

Multisensory object processing improves recognition memory for individual objects, but its impact on memory for neighboring visual objects and scene context remains largely unknown. It is therefore unclear how multisensory processing impacts episodic memory for information outside of the object itself. We conducted three experiments to test the prediction that the presence of audiovisual objects at encoding would improve memory for nearby visual objects, and improve memory for the environmental context in which they occurred. In Experiments 1a and 1b, participants viewed audiovisual-visual object pairs or visual-visual object pairs with a control sound during encoding and were subsequently tested on their memory for each object individually. In Experiment 2, objects were paired with semantically congruent or meaningless control sounds and appeared within four different scene environments. Memory for the environment was tested. Results from Experiments 1a and 1b showed that encoding a congruent audiovisual object did not significantly benefit memory for neighboring visual objects, but Experiment 2 showed that encoding a congruent audiovisual object did improve memory for the environments in which those objects were encoded. These findings suggest that multisensory processing can influence memory beyond the objects themselves and that it has a unique role in episodic memory formation. This is particularly important for understanding how memories and associations are formed in real-world situations, in which objects and their surroundings are often multimodal.

Attentional Guidance and Match Decisions Rely on Different Template Information During Visual Search.

When searching for a target object, we engage in a continuous "look-identify" cycle in which we use known features of the target to guide attention toward potential targets and then to decide whether the selected object is indeed the target. Target information in memory (the target template or attentional template) is typically characterized as having a single, fixed source. However, debate has recently emerged over whether flexibility in the target template is relational or optimal. On the basis of evidence from two experiments using college students (Ns = 30 and 70, respectively), we propose that initial guidance of attention uses a coarse relational code, but subsequent decisions use an optimal code. Our results offer a novel perspective that the precision of template information differs when guiding sensory selection and when making identity decisions during visual search.

Temporal integration of feature probability distributions.

Humans are surprisingly good at learning the statistical characteristics of their visual environment. Recent studies have revealed that not only can the visual system learn repeated features of visual search distractors, but also their actual probability distributions. Search times were determined by the frequency of distractor features over consecutive search trials. The search displays applied in these studies involved many exemplars of distractors on each trial and while there is clear evidence that feature distributions can be learned from large distractor sets, it is less clear if distributions are well learned for single targets presented on each trial. Here, we investigated potential learning of probability distributions of single targets during visual search. Over blocks of trials, observers searched for an oddly colored target that was drawn from either a Gaussian or a uniform distribution. Search times for the different target colors were clearly influenced by the probability of that feature within trial blocks. The same search targets, coming from the extremes of the two distributions were found significantly slower during the blocks where the targets were drawn from a Gaussian distribution than from a uniform distribution indicating that observers were sensitive to the target probability determined by the distribution shape. In Experiment 2, we replicated the effect using binned distributions and revealed the limitations of encoding complex target distributions. Our results demonstrate detailed internal representations of target feature distributions and that the visual system integrates probability distributions of target colors over surprisingly long trial sequences.

Idiosyncratic Patterns of Representational Similarity in Prefrontal Cortex Predict Attentional Performance.

The efficiency of finding an object in a crowded environment depends largely on the similarity of nontargets to the search target. Models of attention theorize that the similarity is determined by representations stored within an "attentional template" held in working memory. However, the degree to which the contents of the attentional template are individually unique and where those idiosyncratic representations are encoded in the brain are unknown. We investigated this problem using representational similarity analysis of human fMRI data to measure the common and idiosyncratic representations of famous face morphs during an identity categorization task; data from the categorization task were then used to predict performance on a separate identity search task. We hypothesized that the idiosyncratic categorical representations of the continuous face morphs would predict their distractability when searching for each target identity. The results identified that patterns of activation in the lateral prefrontal cortex (LPFC) as well as in face-selective areas in the ventral temporal cortex were highly correlated with the patterns of behavioral categorization of face morphs and search performance that were common across subjects. However, the individually unique components of the categorization behavior were reliably decoded only in right LPFC. Moreover, the neural pattern in right LPFC successfully predicted idiosyncratic variability in search performance, such that reaction times were longer when distractors had a higher probability of being categorized as the target identity. These results suggest that the prefrontal cortex encodes individually unique components of categorical representations that are also present in attentional templates for target search. SIGNIFICANCE STATEMENT: Everyone's perception of the world is uniquely shaped by personal experiences and preferences. Using functional MRI, we show that individual differences in the categorization of face morphs between two identities could be decoded from the prefrontal cortex and the ventral temporal cortex. Moreover, the individually unique representations in prefrontal cortex predicted idiosyncratic variability in attentional performance when looking for each identity in the "crowd" of another morphed face in a separate search task. Our results reveal that the representation of task-related information in prefrontal cortex is individually unique and preserved across categorization and search performance. This demonstrates the possibility of predicting individual behaviors across tasks with patterns of brain activity.

Dynamics of Feature-based Attentional Selection during Color-Shape Conjunction Search.

Feature-based attentional selection is accomplished by increasing the gain of sensory neurons encoding target-relevant features while decreasing that of other features. But how do these mechanisms work when targets and distractors share features? We investigated this in a simplified color-shape conjunction search task using ERP components (N2pc, PD, and SPCN) that index lateralized attentional processing. In Experiment 1, we manipulated the presence and frequency of color distractors while holding shape distractors constant. We tested the hypothesis that the color distractor would capture attention, requiring active suppression such that processing of the target can continue. Consistent with this hypothesis, we found that color distractors consistently captured attention, as indexed by a significant N2pc, but were reactively suppressed (indexed by PD). Interestingly, when the color distractor was present, target processing was sustained (indexed by SPCN), suggesting that the dynamics of attentional competition involved distractor suppression interlinked with sustained target processing. In Experiment 2, we examined the contribution of shape to the dynamics of attentional competition under similar conditions. In contrast to color distractors, shape distractors did not reliably capture attention, even when the color distractor was very frequent and attending to target shape would be beneficial. Together, these results suggest that target-colored objects are prioritized during color-shape conjunction search, and the ability to select the target is delayed while target-colored distractors are actively suppressed.

Polarity-dependent Effects of Biparietal Transcranial Direct Current Stimulation on the Interplay between Target Location and Distractor Saliency in Visual Attention.

Visual attention allows the allocation of limited neural processing resources to stimuli based on their behavioral priorities. The selection of task-relevant visual targets entails the processing of multiple competing stimuli and the suppression of distractors that may be either perceptually salient or perceptually similar to targets. The posterior parietal cortex controls the interaction between top-down (task-driven) and bottom-up (stimulus-driven) processes competing for attentional selection, as well as spatial distribution of attention. Here, we examined whether biparietal transcranial direct current stimulation (tDCS) would modulate the interaction between top-down and bottom-up processes in visual attention. Visual attention function was assessed with a visual discrimination task, in which a lateralized target was presented alone or together with a contralateral, similar or salient, distractor. The accuracy and RTs were measured before and during three stimulation sessions (sham, right anodal/left cathodal, left anodal/right cathodal). The analyses demonstrated (i) polarity-dependent effects of tDCS on the accuracy of target discrimination, but only when the target was presented with a similar distractor; (ii) the tDCS-triggered effects on the accuracy of discriminating targets, accompanied by a similar distractor, varied according to the target location; and (iii) overall detrimental effects of tDCS on RTs were observed, regardless of target location, distractor type, and polarity of the stimulation. We conclude that the observed polarity, distractor type, and target location-dependent effects of biparietal tDCS on the accuracy of target detection resulted from both a modulation of the interaction between top-down and bottom-up attentional processes and the interhemispheric competition mechanisms guiding attentional selection and spatial deployment of attention.

Effective connectivity during feature-based attentional capture: evidence against the attentional reorienting hypothesis of TPJ.

The most prevalent neurobiological theory of attentional control posits 2 distinct brain networks: The dorsal and ventral attention networks. The role of the dorsal attentional network in top-down attentional control is well established, but there is less evidence for the putative role of the ventral attentional network in initiating stimulus-driven reorienting. Here, we used functional magnetic resonance imaging and dynamic causal modeling (DCM) to test the role of the ventral and dorsal networks in attentional reorienting during instances of attentional capture by a target-colored distracter. In the region of interest analyses, we found that frontal eye field (FEF) was selectively activated by conditions where attention was reoriented (i.e. to spatial cues and target-colored distracters). In contrast, temporoparietal junction (TPJ) responded positively to all stimulus conditions. The DCM results indicated that FEF received sensory inputs earlier than TPJ, and that only the connection from FEF to TPJ was modulated by the appearance of the target-colored distracter. The results provide novel empirical evidence against the idea that TPJ generates stimulus-driven reorientations of attention. We conclude that our results are incompatible with existing theories of TPJ involvement in the stimulus-driven reorientation of attention and discuss alternative explanations such as contextual updating.

Learned associations serve as target proxies during difficult but not easy visual search.

The target template contains information in memory that is used to guide attention during visual search and is typically thought of as containing features of the actual target object. However, when targets are hard to find, it is advantageous to use other information in the visual environment that is predictive of the target's location to help guide attention. The purpose of these studies was to test if newly learned associations between face and scene category images lead observers to use scene information as a proxy for the face target. Our results showed that scene information was used as a proxy for the target to guide attention but only when the target face was difficult to discriminate from the distractor face; when the faces were easy to distinguish, attention was no longer guided by the scene unless the scene was presented earlier. The results suggest that attention is flexibly guided by both target features as well as features of objects that are predictive of the target location. The degree to which each contributes to guiding attention depends on the efficiency with which that information can be used to decode the location of the target in the current moment. The results contribute to the view that attentional guidance is highly flexible in its use of information to rapidly locate the target.

Task-adaptive changes to the target template in response to distractor context: Separability versus similarity.

Theories of attention hypothesize the existence of an attentional template that contains target features in working or long-term memory. It is frequently assumed that the template contains a veridical copy of the target, but recent studies suggest that this is not true when the distractors are linearly separable from the target. In such cases, target representations shift "off-veridical" in response to the distractor context, presumably because doing so is adaptive and increases the representational distinctiveness of targets from distractors. However, some have argued that the shifts may be entirely explained by perceptual biases created by simultaneous color contrast. Here we address this debate and test the more general hypothesis that the target template is adaptively shaped by elements of the distractor context needed to distinguish targets from distractors. We used a two-dimensional target and separately manipulated the linear separability of one dimension (color) and the visual similarity of the other (orientation). We found that target shifting along the linearly separable color dimension was dependent on the similarity of targets-to-distractors along the other dimension. The target representations were consistent with a postexperiment strategy questionnaire in which participants reported using color more when orientation was hard to use, and orientation more when it was easier to use. We conclude that the target template is task-adaptive and exploit features in the distractor context that most predictably distinguish targets from distractors to increase visual search efficiency. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Terms of debate: Consensus definitions to guide the scientific discourse on visual distraction.

Hypothesis-driven research rests on clearly articulated scientific theories. The building blocks for communicating these theories are scientific terms. Obviously, communication - and thus, scientific progress - is hampered if the meaning of these terms varies idiosyncratically across (sub)fields and even across individual researchers within the same subfield. We have formed an international group of experts representing various theoretical stances with the goal to homogenize the use of the terms that are most relevant to fundamental research on visual distraction in visual search. Our discussions revealed striking heterogeneity and we had to invest much time and effort to increase our mutual understanding of each other's use of central terms, which turned out to be strongly related to our respective theoretical positions. We present the outcomes of these discussions in a glossary and provide some context in several essays. Specifically, we explicate how central terms are used in the distraction literature and consensually sharpen their definitions in order to enable communication across theoretical standpoints. Where applicable, we also explain how the respective constructs can be measured. We believe that this novel type of adversarial collaboration can serve as a model for other fields of psychological research that strive to build a solid groundwork for theorizing and communicating by establishing a common language. For the field of visual distraction, the present paper should facilitate communication across theoretical standpoints and may serve as an introduction and reference text for newcomers.

A common neural mechanism for preventing and terminating the allocation of attention.

Much is known about the mechanisms by which attention is focused to facilitate perception, but little is known about what happens to attention after perception of the attended object is complete. One possibility is that the focus of attention passively fades. A second possibility is that attention is actively terminated after the completion of perception so that the brain can be prepared for the next target. The present study investigated this issue with event-related potentials in humans, focusing on the N2pc component (a neural measure of attentional deployment) and the Pd component (a neural measure of attentional suppression). We found that active suppression occurred both to prevent the allocation of attention to known distractors and to terminate attention after the perception of an attended object was complete. In addition, the neural measure of active suppression was correlated with a behavioral measure of trial-to-trial variations in the allocation of attention. Active suppression therefore appears to be a general-purpose mechanism that both prevents and terminates the allocation of attention.

A match made by modafinil: probability matching in choice decisions and spatial attention.

When predicting where a target or reward will be, participants tend to choose each location commensurate with the true underlying probability (i.e., probability match). The strategy of probability matching involves independent sampling of high and low probability locations on separate trials. In contrast, models of probabilistic spatial attention hypothesize that on any given trial attention will either be weighted toward the high probability location or be distributed equally across all locations. Thus, the strategies of probabilistic sampling by choice decisions and spatial attention appear to differ with regard to low-probability events. This distinction is somewhat surprising because similar brain mechanisms (e.g., pFC-mediated cognitive control) are thought to be important in both functions. Thus, the goal of the current study was to examine the relationship between choice decisions and attentional selection within single trials to test for any strategic differences, then to determine whether that relationship is malleable to manipulations of catecholamine-modulated cognitive control with the drug modafinil. Our results demonstrate that spatial attention and choice decisions followed different strategies of probabilistic information selection on placebo, but that modafinil brought the pattern of spatial attention into alignment with that of predictive choices. Modafinil also produced earlier learning of the probability distribution. Together, these results suggest that enhancing cognitive control mechanisms (e.g., through prefrontal cortical function) leads spatial attention to follow choice decisions in selecting information according to rule-based expectations.

Object memory is multisensory: Task-irrelevant sounds improve recollection.

Hearing a task-irrelevant sound during object encoding can improve visual recognition memory when the sound is object-congruent (e.g., a dog and a bark). However, previous studies have only used binary old/new memory tests, which do not distinguish between recognition based on the recollection of details about the studied event or stimulus familiarity. In the present research, we hypothesized that hearing a task-irrelevant but semantically congruent natural sound at encoding would facilitate the formation of richer memory representations, resulting in increased recollection of details of the encoded event. Experiment 1 replicates previous studies showing that participants were more confident about their memory for items that were initially encoded with a congruent sound compared to an incongruent sound. Experiment 2 suggests that congruent object-sound pairings specifically facilitate recollection and not familiarity-based recognition memory, and Experiment 3 demonstrates that this effect was coupled with more accurate memory for audiovisual congruency of the item and sound from encoding rather than another aspect of the episode. These results suggest that even when congruent sounds are task-irrelevant, they promote formation of multisensory memories and subsequent recollection-based retention. Given the ubiquity of encounters with multisensory objects in our everyday lives, considering their impact on episodic memory is integral to building models of memory that apply to naturalistic settings.

Good-enough attentional guidance.

Theories of attention posit that attentional guidance operates on information held in a target template within memory. The template is often thought to contain veridical target features, akin to a photograph, and to guide attention to objects that match the exact target features. However, recent evidence suggests that attentional guidance is highly flexible and often guided by non-veridical features, a subset of features, or only associated features. We integrate these findings and propose that attentional guidance maximizes search efficiency based on a 'good-enough' principle to rapidly localize candidate target objects. Candidates are then serially interrogated to make target-match decisions using more precise information. We suggest that good-enough guidance optimizes the speed-accuracy-effort trade-offs inherent in each stage of visual search.

Contextual knowledge configures attentional control networks.

Contextual cues are predictive and provide behaviorally relevant information; they are not the main objective of the current task but can make behavior more efficient. Using fMRI, we investigated the brain networks involved in representing contextual information and translating it into an attentional control signal. Human subjects performed a visual search task for a low-contrast target accompanied by a single non-target that was either perceptually similar or more salient (i.e., higher contrast). Shorter reaction times (RTs) and higher accuracy were found on salient trials, suggesting that the salient item was rapidly identified as a non-target and immediately acts as a spatial "anti-cue" to reorient attention to the target. The relative saliency of the non-target determined BOLD responses in the left temporoparietal junction (TPJ) and inferior frontal gyrus (IFG). IFG correlated with RT specifically on salient non-target trials. In contrast, bilateral dorsal frontoparietal regions [including the frontal eye fields (FEFs)] were correlated with RT in all conditions. Effective connectivity analyses using dynamic causal modeling found an excitatory pathway from TPJ to IFG to FEF, suggesting that this was the pathway by which the contextual cue was translated into an attentional control signal that facilitated behavior. Additionally, the connection from FEF to TPJ was negatively modulated during target-similar trials, consistent with the inhibition of TPJ by dorsal attentional control regions during top-down serial visual search. We conclude that left TPJ and IFG form a sensory-driven network that integrates contextual knowledge with ongoing sensory information to provide an attentional control signal to FEF.

Visual search guidance uses coarser template information than target-match decisions.

When searching for an object, we use a target template in memory that contains task-relevant information to guide visual attention to potential targets and to determine the identity of attended objects. These processes in visual search have typically been assumed to rely on a common source of template information. However, our recent work (Yu et al., 2022) argued that attentional guidance and target-match decisions rely on different information during search, with guidance using a "fuzzier" version of the template compared with target decisions. However, that work was based on the special case of search for a target amongst linearly separable distractors (e.g., search for an orange target amongst yellower distractors). Real-world search targets, however, are infrequently linearly separable from distractors, and it remains unclear whether the differences between the precision of template information used for guidance compared with target decisions also applies under more typical conditions. In four experiments, we tested this question by varying distractor similarity during visual search and measuring the likelihood of attentional guidance to distractors and target misidentifications. We found that early attentional guidance is indeed less precise than that of subsequent match decisions under varying exposure durations and distractor set sizes. These results suggest that attentional guidance operates on a coarser code than decisions, perhaps because guidance is constrained by lower acuity in peripheral vision or the need to rapidly explore a wide region of space while decisions about selected objects are more precise to optimize decision accuracy.

Attentional priority is determined by predicted feature distributions.

Visual attention is often characterized as being guided by precise memories for target objects. However, real-world search targets have dynamic features that vary over time, meaning that observers must predict how the target could look based on how features are expected to change. Despite its importance, little is known about how target feature predictions influence feature-based attention, or how these predictions are represented in the target template. In Experiment 1 (N = 60 university students), we show observers readily track the statistics of target features over time and adapt attentional priority to predictions about the distribution of target features. In Experiments 2a and 2b (N = 480 university students), we show that these predictions are encoded into the target template as a distribution of likelihoods over possible target features, which are independent of memory precision for the cued item. These results provide a novel demonstration of how observers represent predicted feature distributions when target features are uncertain and show that these predictions are used to set attentional priority during visual search. (PsycInfo Database Record (c) 2022 APA, all rights reserved).