Feature-Specific Salience Maps in Human Cortex.

Priority map theory is a leading framework for understanding how various aspects of stimulus displays and task demands guide visual attention. Per this theory, the visual system computes a priority map, which is a representation of visual space indexing the relative importance, or priority, of locations in the environment. Priority is computed based on both salience, defined based on image-computable properties; and relevance, defined by an individual's current goals, and is used to direct attention to the highest-priority locations for further processing. Computational theories suggest that priority maps identify salient locations based on individual feature dimensions (e.g., color, motion), which are integrated into an aggregate priority map. While widely accepted, a core assumption of this framework, the existence of independent feature dimension maps in visual cortex, remains untested. Here, we tested the hypothesis that retinotopic regions selective for specific feature dimensions (color or motion) in human cortex act as neural feature dimension maps, indexing salient locations based on their preferred feature. We used fMRI activation patterns to reconstruct spatial maps while male and female human participants viewed stimuli with salient regions defined by relative color or motion direction. Activation in reconstructed spatial maps was localized to the salient stimulus position in the display. Moreover, the strength of the stimulus representation was strongest in the ROI selective for the salience-defining feature. Together, these results suggest that feature-selective extrastriate visual regions highlight salient locations based on local feature contrast within their preferred feature dimensions, supporting their role as neural feature dimension maps.SIGNIFICANCE STATEMENT Identifying salient information is important for navigating the world. For example, it is critical to detect a quickly approaching car when crossing the street. Leading models of computer vision and visual search rely on compartmentalized salience computations based on individual features; however, there has been no direct empirical demonstration identifying neural regions as responsible for performing these dissociable operations. Here, we provide evidence of a critical double dissociation that neural activation patterns from color-selective regions prioritize the location of color-defined salience while minimally representing motion-defined salience, whereas motion-selective regions show the complementary result. These findings reveal that specialized cortical regions act as neural "feature dimension maps" that are used to index salient locations based on specific features to guide attention.

The dynamics of statistical learning in visual search and its interaction with salience processing: An EEG study.

Visual attention can be guided by statistical regularities in the environment, that people implicitly learn from past experiences (statistical learning, SL). Moreover, a perceptually salient element can automatically capture attention, gaining processing priority through a bottom-up attentional control mechanism. The aim of our study was to investigate the dynamics of SL and if it shapes attentional target selection additively with salience processing, or whether these mechanisms interact, e.g. one gates the other. In a visual search task, we therefore manipulated target frequency (high vs. low) across locations while, in some trials, the target was salient in terms of colour. Additionally, halfway through the experiment, the high-frequency location changed to the opposite hemifield. EEG activity was simultaneously recorded, with a specific interest in two markers related to target selection and post-selection processing, respectively: N2pc and SPCN. Our results revealed that both SL and saliency significantly enhanced behavioural performance, but also interacted with each other, with an attenuated saliency effect at the high-frequency target location, and a smaller SL effect for salient targets. Concerning processing dynamics, the benefit of salience processing was more evident during the early stage of target selection and processing, as indexed by a larger N2pc and early-SPCN, whereas SL modulated the underlying neural activity particularly later on, as revealed by larger late-SPCN. Furthermore, we showed that SL was rapidly acquired and adjusted when the spatial imbalance changed. Overall, our findings suggest that SL is flexible to changes and, combined with salience processing, jointly contributes to establishing attentional priority.

Spatial bias in anti-saccade endpoints following bilateral dorsal posterior parietal lesions.

Anti-saccades are eye movements in which the saccade is executed in the opposite direction of a visual target and are often hypometric. Because the visual target and saccade goal are decoupled, it has been suggested that competition between the two locations occurs and needs to be resolved. It has been hypothesized that the hypometria of anti-saccades reflects this spatial competition by revealing a bias towards the visual target. To confirm that this hypometria is not simply due to reduced gain, we tested 10 healthy subjects on three different anti-saccade spatial configuration tasks: 90° away across hemifields, 90° away within the same hemifield and 180° away (classic, diagonally opposite). Specifically, we examined whether saccade endpoints showed evidence for the visual target location's interference with anti-saccade programming and execution processes. Among other neural substrates involved in anti-saccades production, the dorsal posterior parietal cortex (PPC) has been implicated in the spatial inhibition of contralateral visual target. To gain insight into the neural processes involved in spatial competition during anti-saccades, we also tested one patient with a bilateral dorsal PPC lesion. In all spatial configurations, we observed that anti-saccade endpoints demonstrated a spatial bias towards the visual target for all participants, likely due to an incomplete inhibition of the visual target location. This spatial bias was exacerbated in our patient, which suggests that the dorsal PPC contributes to the amalgamation of the two competing spatial representations.

Prefrontal Control of Proactive and Reactive Mechanisms of Visual Suppression.

In everyday life, we are continuously struggling at focusing on our current goals while at the same time avoiding distractions. Attention is the neuro-cognitive process devoted to the selection of behaviorally relevant sensory information while at the same time preventing distraction by irrelevant information. Distraction can be prevented proactively, by strategically prioritizing task-relevant information at the expense of irrelevant information, or reactively, by suppressing the ongoing processing of distractors. The distinctive neuronal signature of these suppressive mechanisms is still largely unknown. Thanks to machine-learning decoding methods applied to prefrontal cortical activity, we monitor the dynamic spatial attention with an unprecedented spatial and temporal resolution. We first identify independent behavioral and neuronal signatures for long-term (learning-based spatial prioritization) and short-term (dynamic spatial attention) mechanisms. We then identify distinct behavioral and neuronal signatures for proactive and reactive suppression mechanisms. We find that while distracting task-relevant information is suppressed proactively, task-irrelevant information is suppressed reactively. Critically, we show that distractor suppression, whether proactive or reactive, strongly depends on the implementation of both long-term and short-term mechanisms of selection. Overall, we provide a unified neuro-cognitive framework describing how the prefrontal cortex deals with distractors in order to flexibly optimize behavior in dynamic environments.

Gaze-contingent display technology can help to reduce the ipsilesional attention bias in hemispatial neglect following stroke.

BACKGROUND: Hemispatial neglect results from unilateral brain damage and represents a disabling unawareness for objects in the hemispace opposite the brain lesion (contralesional). The patients' attentional bias for ipsilesional hemispace represents a hallmark of neglect, which results from an imbalanced attentional priority map in the brain. The aim of this study was to investigate whether gaze-contingent display (GCD) technology, reducing the visual salience of objects in ipsilesional hemispace, is able to rebalance this map and increase awareness and exploration of objects in the neglected contralesional hemispace. METHODS: Using remote eye-tracking, we recorded gaze positions in 19 patients with left hemispatial neglect following right-hemisphere stroke and 22 healthy control subjects, while they were watching static naturalistic scenes. There were two task conditions, free viewing (FV) or goal-directed visual search (VS), and four modification conditions including the unmodified original picture, a purely static modification and two differently strong modifications with an additional gaze-contingent mask (GC-LOW, GC-HIGH), that continuously reduced color saturation and contrast of objects in the right hemispace. RESULTS: The patients' median gaze position (Center of Fixation) in the original pictures was markedly deviated to the right in both tasks (FV: 6.8° ± 0.8; VS: 5.5° ± 0.7), reflecting the neglect-typical ipsilesional attention bias. GC modification significantly reduced this bias in FV (GC-HIGH: d = - 3.2 ± 0.4°; p < 0.001). Furthermore, in FV and VS, GC modification increased the likelihood to start visual exploration in the (neglected) left hemifield by about 20%. This alleviation of the ipsilesional fixation bias was not associated with an improvement in detecting left-side targets, in contrast, the GC mask even decreased and slowed the detection of right-side targets. Subjectively, patients found the intervention pleasant and most of the patients did not notice any modification. CONCLUSIONS: GCD technology can be used to positively influence visual exploration patterns in patients with hemispatial neglect. Despite an alleviation of the neglect-related ipsilesional fixation bias, a concomitant functional benefit (improved detection of contralesional targets) was not achieved. Future studies may investigate individualized GCD-based modifications as augmented reality applications during the activities of daily living.

Massive Effects of Saliency on Information Processing in Visual Working Memory.

Limitations in the ability to temporarily represent information in visual working memory (VWM) are crucial for visual cognition. Whether VWM processing is dependent on an object's saliency (i.e., how much it stands out) has been neglected in VWM research. Therefore, we developed a novel VWM task that allows direct control over saliency. In three experiments with this task (on 10, 31, and 60 adults, respectively), we consistently found that VWM performance is strongly and parametrically influenced by saliency and that both an object's relative saliency (compared with concurrently presented objects) and absolute saliency influence VWM processing. We also demonstrated that this effect is indeed due to bottom-up saliency rather than differential fit between each object and the top-down attentional template. A simple computational model assuming that VWM performance is determined by the weighted sum of absolute and relative saliency accounts well for the observed data patterns.

Attention Priority Map of Face Images in Human Early Visual Cortex.

Attention priority maps are topographic representations that are used for attention selection and guidance of task-related behavior during visual processing. Previous studies have identified attention priority maps of simple artificial stimuli in multiple cortical and subcortical areas, but investigating neural correlates of priority maps of natural stimuli is complicated by the complexity of their spatial structure and the difficulty of behaviorally characterizing their priority map. To overcome these challenges, we reconstructed the topographic representations of upright/inverted face images from fMRI BOLD signals in human early visual areas primary visual cortex (V1) and the extrastriate cortex (V2 and V3) based on a voxelwise population receptive field model. We characterized the priority map behaviorally as the first saccadic eye movement pattern when subjects performed a face-matching task relative to the condition in which subjects performed a phase-scrambled face-matching task. We found that the differential first saccadic eye movement pattern between upright/inverted and scrambled faces could be predicted from the reconstructed topographic representations in V1-V3 in humans of either sex. The coupling between the reconstructed representation and the eye movement pattern increased from V1 to V2/3 for the upright faces, whereas no such effect was found for the inverted faces. Moreover, face inversion modulated the coupling in V2/3, but not in V1. Our findings provide new evidence for priority maps of natural stimuli in early visual areas and extend traditional attention priority map theories by revealing another critical factor that affects priority maps in extrastriate cortex in addition to physical salience and task goal relevance: image configuration.SIGNIFICANCE STATEMENT Prominent theories of attention posit that attention sampling of visual information is mediated by a series of interacting topographic representations of visual space known as attention priority maps. Until now, neural evidence of attention priority maps has been limited to studies involving simple artificial stimuli and much remains unknown about the neural correlates of priority maps of natural stimuli. Here, we show that attention priority maps of face stimuli could be found in primary visual cortex (V1) and the extrastriate cortex (V2 and V3). Moreover, representations in extrastriate visual areas are strongly modulated by image configuration. These findings extend our understanding of attention priority maps significantly by showing that they are modulated, not only by physical salience and task-goal relevance, but also by the configuration of stimuli images.

Superior colliculus encodes visual saliency during smooth pursuit eye movements.

The saliency map has played a long-standing role in models and theories of visual attention, and it is now supported by neurobiological evidence from several cortical and subcortical brain areas. While visual saliency is computed during moments of active fixation, it is not known whether the same is true while engaged in smooth pursuit of a moving stimulus, which is very common in real-world vision. Here, we examined extrafoveal saliency coding in the superior colliculus, a midbrain area associated with attention and gaze, during smooth pursuit eye movements. We found that SC neurons from the superficial visual layers showed a robust representation of peripheral saliency evoked by a conspicuous stimulus embedded in a wide-field array of goal-irrelevant stimuli. In contrast, visuomotor neurons from the intermediate saccade-related layers showed a poor saliency representation, even though most of these neurons were visually responsive during smooth pursuit. These results confirm and extend previous findings that place the SCs in a unique role as a saliency map that monitors peripheral vision during foveation of stationary and now moving objects.

Dissociable signatures of visual salience and behavioral relevance across attentional priority maps in human cortex.

Computational models posit that visual attention is guided by activity within spatial maps that index the image-computable salience and the behavioral relevance of objects in the scene. These spatial maps are theorized to be instantiated as activation patterns across a series of retinotopic visual regions in occipital, parietal, and frontal cortex. Whereas previous research has identified sensitivity to either the behavioral relevance or the image-computable salience of different scene elements, the simultaneous influence of these factors on neural "attentional priority maps" in human cortex is not well understood. We tested the hypothesis that visual salience and behavioral relevance independently impact the activation profile across retinotopically organized cortical regions by quantifying attentional priority maps measured in human brains using functional MRI while participants attended one of two differentially salient stimuli. We found that the topography of activation in priority maps, as reflected in the modulation of region-level patterns of population activity, independently indexed the physical salience and behavioral relevance of each scene element. Moreover, salience strongly impacted activation patterns in early visual areas, whereas later visual areas were dominated by relevance. This suggests that prioritizing spatial locations relies on distributed neural codes containing graded representations of salience and relevance across the visual hierarchy. NEW & NOTEWORTHY We tested a theory which supposes that neural systems represent scene elements according to both their salience and their relevance in a series of "priority maps" by measuring functional MRI activation patterns across human brains and reconstructing spatial maps of the visual scene. We found that different regions indexed either the salience or the relevance of scene items, but not their interaction, suggesting an evolving representation of salience and relevance across different visual areas.

Remapping, Spatial Stability, and Temporal Continuity: From the Pre-Saccadic to Postsaccadic Representation of Visual Space in LIP.

As our eyes move, we have a strong percept that the world is stable in space and time; however, the signals in cortex coming from the retina change with each eye movement. It is not known how this changing input produces the visual percept we experience, although the predictive remapping of receptive fields has been described as a likely candidate. To explain how remapping accounts for perceptual stability, we examined responses of neurons in the lateral intraparietal area while animals performed a visual foraging task. When a stimulus was brought into the response field of a neuron that exhibited remapping, the onset of the postsaccadic representation occurred shortly after the saccade ends. Whenever a stimulus was taken out of the response field, the presaccadic representation abruptly ended shortly after the eyes stopped moving. In the 38% (20/52) of neurons that exhibited remapping, there was no more than 30 ms between the end of the presaccadic representation and the start of the postsaccadic representation and, in some neurons, and the population as a whole, it was continuous. We conclude by describing how this seamless shift from a presaccadic to postsaccadic representation could contribute to spatial stability and temporal continuity.

A role for the anterior insular cortex in the global neuronal workspace model of consciousness.

According to the global neuronal workspace model of consciousness, consciousness results from the global broadcast of information throughout the brain. The global neuronal workspace is mainly constituted by a fronto-parietal network. The anterior insular cortex is part of this global neuronal workspace, but the function of this region has not yet been defined within the global neuronal workspace model of consciousness. In this review, I hypothesize that the anterior insular cortex implements a cross-modal priority map, the function of which is to determine priorities for the processing of information and subsequent entrance in the global neuronal workspace.

Reward association facilitates distractor suppression in human visual search.

Although valuable objects are attractive in nature, people often encounter situations where they would prefer to avoid such distraction while focusing on the task goal. Contrary to the typical effect of attentional capture by a reward-associated item, we provide evidence for a facilitation effect derived from the active suppression of a high reward-associated stimulus when cuing its identity as distractor before the display of search arrays. Selection of the target is shown to be significantly faster when the distractors were in high reward-associated colour than those in low reward-associated or non-rewarded colours. This behavioural reward effect was associated with two neural signatures before the onset of the search display: the increased frontal theta oscillation and the strengthened top-down modulation from frontal to anterior temporal regions. The former suggests an enhanced working memory representation for the reward-associated stimulus and the increased need for cognitive control to override Pavlovian bias, whereas the latter indicates that the boost of inhibitory control is realized through a frontal top-down mechanism. These results suggest a mechanism in which the enhanced working memory representation of a reward-associated feature is integrated with task demands to modify attentional priority during active distractor suppression and benefit behavioural performance.

Modeling peripheral visual acuity enables discovery of gaze strategies at multiple time scales during natural scene search.

Like humans, monkeys make saccades nearly three times a second. To understand the factors guiding this frequent decision, computational models of vision attempt to predict fixation locations using bottom-up visual features and top-down goals. How do the relative influences of these factors evolve over multiple time scales? Here we analyzed visual features at fixations using a retinal transform that provides realistic visual acuity by suitably degrading visual information in the periphery. In a task in which monkeys searched for a Gabor target in natural scenes, we characterized the relative importance of bottom-up and task-relevant influences by decoding fixated from nonfixated image patches based on visual features. At fast time scales, we found that search strategies can vary over the course of a single trial, with locations of higher saliency, target-similarity, edge­energy, and orientedness looked at later on in the trial. At slow time scales, we found that search strategies can be refined over several weeks of practice, and the influence of target orientation was significant only in the latter of two search tasks. Critically, these results were not observed without applying the retinal transform. Our results suggest that saccade-guidance strategies become apparent only when models take into account degraded visual representation in the periphery.

Reward History and Statistical Learning Independently Impact Attention Search: An ERP Study.

Selection history is widely accepted as a vital source in attention control. Reward history indicates that a learned association captures attention even when the reward is no longer presented, while statistical learning indicates that a learned probability exerts its influence on attentional control (facilitation or inhibition). Existing research has shown that the effects of the reward history and statistical learning are additive, suggesting that these two components influence attention priority through different pathways. In the current study, leveraging the temporal resolution advantages of EEG, we explored whether these two components represent independent sources of attentional bias. The results revealed faster responses to the target at the high-probability location compared to low-probability locations. Both the target and distractor at high-probability locations elicited larger early Pd (50-150 ms) and Pd (150-250 ms) components. The reward distractor slowed the target search and elicited a larger N2pc (180-350 ms). Further, no interaction between statistical learning and the reward history was observed in RTs or N2pc. The different types of temporal progression in attention control indicate that statistical learning and the reward history independently modulate the attention priority map.

Neuronal Response to Reward and Luminance in Macaque LIP During Saccadic Choice.

Recent work in decision neuroscience suggests that visual saliency can interact with reward-based choice, and the lateral intraparietal cortex (LIP) is implicated in this process. In this study, we recorded from LIP neurons while monkeys performed a two alternative choice task in which the reward and luminance associated with each offer were varied independently. We discovered that the animal's choice was dictated by the reward amount while the luminance had a marginal effect. In the LIP, neuronal activity corresponded well with the animal's choice pattern, in that a majority of reward-modulated neurons encoded the reward amount in the neuron's preferred hemifield with a positive slope. In contrast, compared to their responses to low luminance, an approximately equal proportion of luminance-sensitive neurons responded to high luminance with increased or decreased activity, leading to a much weaker population-level response. Meanwhile, in the non-preferred hemifield, the strength of encoding for reward amount and luminance was positively correlated, suggesting the integration of these two factors in the LIP. Moreover, neurons encoding reward and luminance were homogeneously distributed along the anterior-posterior axis of the LIP. Overall, our study provides further evidence supporting the neural instantiation of a priority map in the LIP in reward-based decisions.

Integrated effects of top-down attention and statistical learning during visual search: An EEG study.

The present study aims to investigate how the competition between visual elements is solved by top-down and/or statistical learning (SL) attentional control (AC) mechanisms when active together. We hypothesized that the "winner" element that will undergo further processing is selected either by one AC mechanism that prevails over the other, or by the joint activity of both mechanisms. To test these hypotheses, we conducted a visual search experiment that combined an endogenous cueing protocol (valid vs. neutral cue) and an imbalance of target frequency distribution across locations (high- vs. low-frequency location). The unique and combined effects of top-down control and SL mechanisms were measured on behaviour and amplitudes of three evoked-response potential (ERP) components (i.e., N2pc, P1, CNV) related to attentional processing. Our behavioural results showed better performance for validly cued targets and for targets in the high-frequency location. The two factors were found to interact, so that SL effects emerged only in the absence of top-down guidance. Whereas the CNV and P1 only displayed a main effect of cueing, for the N2pc we observed an interaction between cueing and SL, revealing a cueing effect for targets in the low-frequency condition, but not in the high-frequency condition. Thus, our data support the view that top-down control and SL work in a conjoint, integrated manner during target selection. In particular, SL mechanisms are reduced or even absent when a fully reliable top-down guidance of attention is at play.

Impaired selection of a previously ignored singleton: Evidence for salience map plastic changes.

Spatial suppression of a salient colour distractor is achievable via statistical learning. Distractor suppression attenuates unwanted capture, but at the same time target selection at the most likely distractor location is impaired. This result corroborates the idea that the distractor salience is attenuated via inhibitory signals applied to the corresponding location in the priority map. What is less clear, however, is whether lingering impairment in target selection when the distractor is removed are due to the proactive strategic maintenance of the suppressive signal at the previous most likely distractor location or result from the fact that suppression has induced plastic changes in the priority map, probably changing input weights. Here, we provide evidence that supports the latter possibility, as we found that impairment in target selection persisted even when the singleton distractor in the training phase became the target of search in a subsequent test phase. This manipulation rules out the possibility that the observed impairments at the previous most likely distractor location were caused by a signal suppression maintained at this location. Rather, the results reveal that the inhibitory signals cause long-lasting changes in the priority map, which affect future computation of the target salience at the same location, and therefore the efficiency of attentional selection.

The posterior parietal area V6A: An attentionally-modulated visuomotor region involved in the control of reach-to-grasp action.

In the macaque, the posterior parietal area V6A is involved in the control of all phases of reach-to-grasp actions: the transport phase, given that reaching neurons are sensitive to the direction and amplitude of arm movement, and the grasping phase, since reaching neurons are also sensitive to wrist orientation and hand shaping. Reaching and grasping activity are corollary discharges which, together with the somatosensory and visual signals related to the same movement, allow V6A to act as a state estimator that signals discrepancies during the motor act in order to maintain consistency between the ongoing movement and the desired one. Area V6A is also able to encode the target of an action because of gaze-dependent visual neurons and real-position cells. Here, we advance the hypothesis that V6A also uses the spotlight of attention to guide goal-directed movements of the hand, and hosts a priority map that is specific for the guidance of reaching arm movement, combining bottom-up inputs such as visual responses with top-down signals such as reaching plans.

Region-aware network: Model human's Top-Down visual perception mechanism for crowd counting.

Background noise and scale variation are common problems that have been long recognized in crowd counting. Humans glance at a crowd image and instantly know the approximate number of human and where they are through attention the crowd regions and the congestion degree of crowd regions with a global receptive field. Hence, in this paper, we propose a novel feedback network with Region-Aware block called RANet by modeling human's Top-Down visual perception mechanism. Firstly, we introduce a feedback architecture to generate priority maps that provide prior about candidate crowd regions in input images. The prior enables the RANet pay more attention to crowd regions. Then we design Region-Aware block that could adaptively encode the contextual information into input images through global receptive field. More specifically, we scan the whole input images and its priority maps in the form of column vector to obtain a relevance matrix estimating their similarity. The relevance matrix obtained would be utilized to build global relationships between pixels. Our method outperforms state-of-the-art crowd counting methods on several public datasets.

An attentional limbo: Saccades become momentarily non-selective in between saliency-driven and relevance-driven selection.

Human vision involves selectively directing the eyes to potential objects of interest. According to most prominent theories, selection is the quantal outcome of an ongoing competition between saliency-driven signals on the one hand, and relevance-driven signals on the other, with both types of signals continuously and concurrently projecting onto a common priority map. Here, we challenge this view. We asked participants to make a speeded eye movement towards a target orientation, which was presented together with a non-target of opposing tilt. In addition to the difference in relevance, the target and non-target also differed in saliency, with the target being either more or less salient than the non-target. We demonstrate that saliency- and relevance-driven eye movements have highly idiosyncratic temporal profiles, with saliency-driven eye movements occurring rapidly after display onset while relevance-driven eye movements occur only later. Remarkably, these types of eye movements can be fully separated in time: We find that around 250 ms after display onset, eye movements are no longer driven by saliency differences between potential targets, but also not yet driven by relevance information, resulting in a period of non-selectivity, which we refer to as the attentional limbo. Binomial modeling further confirmed that visual selection is not necessarily the outcome of a direct battle between saliency- and relevance-driven signals. Instead, selection reflects the dynamic changes in the underlying saliency- and relevance-driven processes themselves, and the time at which an action is initiated then determines which of the two will emerge as the driving force of behavior.