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.

Separate and overlapping mechanisms of statistical regularities and salience processing in the occipital cortex and dorsal attention network.

Attention selects behaviorally relevant inputs for in-depth processing. Beside the role of traditional signals related to goal-directed and stimulus-driven control, a debate exists regarding the mechanisms governing the effect of statistical regularities on attentional selection, and how these are integrated with other control signals. Using a visuo-spatial search task under fMRI, we tested the joint effects of statistical regularities and stimulus-driven salience. We found that both types of signals modulated occipital activity in a spatially specific manner. Salience acted primarily by reducing the attention bias towards the target location when associated with irrelevant distractors, while statistical regularities reduced this attention bias when the target was presented at a low probability location, particularly at the lower levels of the visual hierarchy. In addition, we found that both statistical regularities and salience activated the dorsal frontoparietal network. Additional exploratory analyses of functional connectivity revealed that only statistical regularities modulated the inter-regional coupling between the posterior parietal cortex and the occipital cortex. These results show that statistical regularities and salience signals are both spatially represented at the occipital level, but that their integration into attentional processing priorities relies on dissociable brain mechanisms.

Statistical learning of target and distractor spatial probability shape a common attentional priority computation.

Converging evidence recently put forward the notion that dedicated neurocognitive mechanisms do exist for the suppression of salient, but irrelevant distractors. Along this line, it is plausible to hypothesize that, in appropriate contexts, experience-dependent forms of attentional learning might selectively induce plastic changes within this dedicated circuitry, thus allowing an independent shaping of priorities at the service of attentional filtering. Conversely, previous work suggested that statistical learning (SL) of both target and distractor spatial probability distributions converge in adjusting only the overall attentional priority of locations: in fact, in the presence of an independent manipulation, either related to the target or to the distractor only, SL induces indirect effects (e.g., changes in filtering efficiency due to an uneven distribution of targets), suggesting that SL-induced plastic changes affect a shared neural substrate. Here we tested whether, when (conflicting) target- and distractor-related manipulations are concurrently applied to the very same locations, dedicated mechanisms might support the selective encoding of spatial priority in relation to the specific attentional operation involved. In three related experiments, human healthy participants discriminated the direction of a target arrow, while ignoring a salient distractor, if present; both target and distractor spatial probability distributions were concurrently manipulated in relation to each single location. Critically, the selection bias produced by the target-related SL was marginally reduced by an adverse distractor contingency, and the suppression bias generated by the distractor-related SL was erased, or even reversed, by an adverse target contingency. Our results suggest that even conflicting target- and distractor-related SL manipulations result in the adjustment of a unique spatial priority computation, likely because the process directly relies on direct plastic alterations of shared spatial priority map(s).

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.

Effects of top-down and bottom-up attention on post-selection posterior contralateral negativity.

We examined the effect of combined top-down and bottom-up attentional control sources in easy and difficult visual search tasks. Applying a new analysis on previously acquired data, we focused on the sustained posterior contralateral negativity (SPCN) and the response-locked posterior contralateral negativity (RLpcN), to better understand processes following target selection. We used the signed-area approach to measure the negative area, where the signal was either locked to the target or the response onsets. We further split the RLpcN into an early and a late segment to capture the dynamics of selection and post-selection processes. In Experiment 1, participants reported the orientation of a uniquely tilted target. In Experiment 2, participants reported the position of a small gap within the uniquely tilted target. In both experiments, endogenous cues manipulated top-down attention (valid vs. neutral), and salient color singletons (either the target or a distractor) manipulated bottom-up attention. We hypothesized that the SPCN and the later segment of the RLpcN would be modulated by task difficulty and target salience, as they are associated with post-selection processes, such as response selection and working memory. The early segment of the RLpcN was hypothesized to be modulated by the cueing manipulation and presence of a salient distractor, as they affect target selection. An effect of distractor presence was observed on the early segment of the RLpcN, and our results further supported the hypotheses regarding the SPCN and the later segment of the RLpcN, providing novel insights into post-selection processes in visual search.

Dynamic causal interactions between occipital and parietal cortex explain how endogenous spatial attention and stimulus-driven salience jointly shape the distribution of processing priorities in 2D visual space.

Visuo-spatial attention prioritizes the processing of relevant inputs via different types of signals, including current goals and stimulus salience. Complex mixtures of these signals engage in everyday life situations, but little is known about how these signals jointly modulate distributed patterns of activity across the occipital regions that represent visual space. Here, we measured spatio-topic, quadrant-specific occipital activity during the processing of visual displays containing both task-relevant targets and salient color-singletons. We computed spatial bias vectors indexing the effect of attention in 2D space, as coded by distributed activity in the occipital cortex. We found that goal-directed spatial attention biased activity towards the target and that salience further modulated this endogenous effect: salient distractors decreased the spatial bias, while salient targets increased it. Analyses of effective connectivity revealed that the processing of salient distractors relied on the modulation of the bidirectional connectivity between the occipital and the posterior parietal cortex, as well as the modulation of the lateral interactions within the occipital cortex. These findings demonstrate that goal-directed attention and salience jointly contribute to shaping processing priorities in the occipital cortex and highlight that multiple functional paths determine how spatial information about these signals is distributed across occipital regions.

An EEG study of the combined effects of top-down and bottom-up attentional selection under varying task difficulty.

We examined the effect of combined top-down and bottom-up attentional control sources, using known attention-related EEG components that are thought to reflect target selection (N2pc) and distractor suppression (PD ). We used endogenous cues (valid vs. neutral) for top-down attentional control, and salience in the form of color singletons (either the target or a distractor) for bottom-up attentional control in visual search. Crucially, in two experiments, the task was of increasing difficulty, reporting the orientation of a tilted target (Experiment 1), or the position of a small gap within the target among tilted non-targets (Experiment 2). Our results showed strong cueing effects on RT and accuracy in both experiments, demonstrating a general facilitation of responses to validly cued targets. Whereas the processing of salient targets was not improved compared with non-salient targets, the presence of a salient distractor consistently worsened performance. The N2pc and PD were only observed in trials where targets were preceded by neutral cues in Experiment 1, and for validly cued targets and salient neutrally cued targets in Experiment 2. A cueing effect was found on the PD in Experiment 1, showing an amplitude reduction in trials where the target was validly cued. These results support the idea that bottom-up attentional allocation occurs only when top-down allocation of attention is absent or inefficient. Therefore, these results indicate that attentional selection and suppression during visual search are both influenced by top-down cueing and give support to theories that focus on the interaction between the two types of attention.

Modulating the influence of recent trial history on attentional capture via transcranial magnetic stimulation (TMS) of right TPJ.

In visual search, salient yet task-irrelevant distractors in the stimulus array interfere with target selection. This is due to the unwanted shift of attention towards the salient stimulus-the so-called attentional capture effect, which delays deployment of attention onto the target. Although powerful and automatic, attentional capture by a salient distractor is nonetheless antagonized by distractor-filtering mechanisms and is further modulated by cross-trial contingencies: The distractor cost is typically more robust when no distraction has been experienced in the immediate past, compared to when a distractor was present on the immediately preceding trial. Here, we used transcranial magnetic stimulation (TMS) to shed light on the causal role of two crucial nodes of the ventral attention network, namely the Temporo-Parietal Junction (TPJ) and the Middle Frontal Gyrus (MFG), in the exogenous control of attention (i.e., attentional capture) and its history-dependent modulation. Participants were asked to discriminate the direction of a target arrow while ignoring a task-irrelevant salient distractor, when present. Immediately after display onset, 10 Hz triple-pulse TMS was delivered either to TPJ or MFG on the right hemisphere. Results demonstrated that stimulation of right TPJ-but not of right MFG, strongly modulated attentional capture as a function of the type of previous trial, by somewhat enhancing the distractor-related cost when the preceding trial was a distractor-absent trial and significantly decreasing the cost when the preceding trial was a distractor-present trial. These findings indicate that TMS of right TPJ exacerbates the effect of the recent history, likely reflecting enhanced updating of the predictive model that dynamically governs proactive distractor-filtering mechanisms. More generally, the results attest to a role of TPJ in mediating the history-dependent modulation of attentional capture.

Probing the Neural Mechanisms for Distractor Filtering and Their History-Contingent Modulation by Means of TMS.

In visual search, the presence of a salient, yet task-irrelevant, distractor in the stimulus array interferes with target selection and slows down performance. Neuroimaging data point to a key role of the frontoparietal dorsal attention network in dealing with visual distractors; however, the respective roles of different nodes within the network and their hemispheric specialization are still unresolved. Here, we used transcranial magnetic stimulation (TMS) to evaluate the causal role of two key regions of the dorsal attention network in resisting attentional capture by a salient singleton distractor: the frontal eye field (FEF) and the cortex within the intraparietal sulcus (IPS). The task of the participants (male/female human volunteers) was to discriminate the pointing direction of a target arrow while ignoring a task-irrelevant salient distractor. Immediately after stimulus onset, triple-pulse 10 Hz TMS was delivered either to IPS or FEF on either side of the brain. Results indicated that TMS over the right FEF significantly reduced the behavioral cost engendered by the salient distractor relative to left FEF stimulation. No such effect was obtained with stimulation of IPS on either side of brain. Interestingly, this FEF-dependent reduction in distractor interference interacted with the contingent trial history, being maximal when no distractor was present on the previous trial relative to when there was one. Our results provide direct causal evidence that the right FEF houses key mechanisms for distractor filtering, pointing to a pivotal role of the frontal cortex of the right hemisphere in limiting interference from an irrelevant but attention-grabbing stimulus.SIGNIFICANCE STATEMENT Visually conspicuous stimuli attract our attention automatically and interfere with performance by diverting resources away from the main task. Here, we applied transcranial magnetic stimulation over four frontoparietal cortex locations (frontal eye field and intraparietal sulcus in each hemisphere) to identify regions of the dorsal attention network that help limit interference from task-irrelevant, salient distractors. Results indicate that the right FEF participates in distractor-filtering mechanisms that are recruited when a distracting stimulus is encountered. Moreover, right FEF implements adjustments in distraction-filtering mechanisms following recent encounters with distractors. Together, these findings indicate a different hemispheric contribution of the left versus right dorsal frontal cortex to distraction filtering. This study expands our understanding of how our brains select relevant targets in the face of task-irrelevant, salient distractors.

Revealing Dissociable Attention Biases in Chronic Smokers Through an Individual-Differences Approach.

Addiction is accompanied by attentional biases (AB), wherein drug-related cues grab attention independently of their perceptual salience. AB have emerged in different flavours depending on the experimental approach, and their clinical relevance is still debated. In chronic smokers we sought evidence for dissociable attention abnormalities that may play distinct roles in the clinical manifestations of the disorder. Fifty smokers performed a modified visual probe-task measuring two forms of AB and their temporal dynamics, and data on their personality traits and smoking history/status were collected. Two fully dissociable AB effects were found: A Global effect, reflecting the overall impact of smoke cues on attention, and a Location-specific effect, indexing the impact of smoke cues on visuospatial orienting. Importantly, the two effects could be neatly separated from one another as they: (i) unfolded with dissimilar temporal dynamics, (ii) were accounted for by different sets of predictors associated with personality traits and smoking history and (iii) were not correlated with one another. Importantly, the relevance of each of these two components in the single individual depends on a complex blend of personality traits and smoking habits, a result that future efforts addressing the clinical relevance of addiction-related AB should take into careful consideration.

Laws of concatenated perception: Vision goes for novelty, decisions for perseverance.

Every instant of perception depends on a cascade of brain processes calibrated to the history of sensory and decisional events. In the present work, we show that human visual perception is constantly shaped by two contrasting forces exerted by sensory adaptation and past decisions. In a series of experiments, we used multilevel modeling and cross-validation approaches to investigate the impact of previous stimuli and decisions on behavioral reports during adjustment and forced-choice tasks. Our results revealed that each perceptual report is permeated by opposite biases from a hierarchy of serially dependent processes: Low-level adaptation repels perception away from previous stimuli, whereas decisional traces attract perceptual reports toward the recent past. In this hierarchy of serial dependence, "continuity fields" arise from the inertia of decisional templates and not from low-level sensory processes. This finding is consistent with a Two-process model of serial dependence in which the persistence of readout weights in a decision unit compensates for sensory adaptation, leading to attractive biases in sequential perception. We propose a unified account of serial dependence in which functionally distinct mechanisms, operating at different stages, promote the differentiation and integration of visual information over time.

Optic Nerve Degeneration and Reduced Contrast Sensitivity Due to Folic Acid Deficiency: A Behavioral and Electrophysiological Study in Rhesus Monkeys.

Purpose: The purpose of the research was to elucidate the role of folic acid (B9) deficiency in the development of nutritional optic neuritis and to characterize the neurophysiological consequences of optic nerve degeneration in the cortical visual system. Methods: A combined behavioral and electrophysiological approach was applied to study luminance contrast sensitivity in two macaque monkeys affected by nutritional optic neuritis and in two healthy monkeys for comparison. For one monkey, a follow-up approach was applied to compare visual performance before onset of optic neuropathy, during the disease, and after treatment. Results: Optic nerve degeneration developed as a consequence of insufficient dietary intake of folic acid in two exemplars of macaque monkeys. The degeneration resulted in markedly reduced luminance contrast sensitivity as assessed behaviorally. In one monkey, we also measured visual activity in response to varying contrast at the level of single neurons in the cortical visual system and found a striking reduction in contrast sensitivity, as well as a marked increase in the latency of neuronal responses. Prolonged daily folate supplementation resulted in a significant recovery of function. Conclusions: Folic acid deficiency per se can lead to the development of optic nerve degeneration in otherwise healthy adult animals. The optic nerve degeneration strongly affects contrast sensitivity and leads to a distinct reduction in the strength and velocity of the incoming signal to cortical visual areas of the macaque brain, without directly affecting excitability and functional properties of cortical neurons.

Preparatory activity for purposeful arm movements in the dorsomedial parietal area V6A: Beyond the online guidance of movement.

Over the years, electrophysiological recordings in macaque monkeys performing visuomotor tasks brought about accumulating evidence for the expression of neuronal properties (e.g., selectivity in the visuospatial and somatosensory domains, encoding of visual affordances and motor cues) in the posterior parietal area V6A that characterize it as an ideal neural substrate for online control of prehension. Interestingly, neuroimaging studies suggested a role of putative human V6A also in action preparation; moreover, pre-movement population activity in monkey V6A has been recently shown to convey grip-related information for upcoming grasping. Here we directly test whether macaque V6A neurons encode preparatory signals that effectively differentiate between dissimilar actions before movement. We recorded the activity of single V6A neurons during execution of two visuomotor tasks requiring either reach-to-press or reach-to-grasp movements in different background conditions, and described the nature and temporal dynamics of V6A activity preceding movement execution. We found striking consistency in neural discharges measured during pre-movement and movement epochs, suggesting that the former is a preparatory activity exquisitely linked to the subsequent execution of particular motor actions. These findings strongly support a role of V6A beyond the online guidance of movement, with preparatory activity implementing suitable motor programs that subsequently support action execution.

High-Acuity Information Is Retained through the Cortical Visual Hierarchy of Primates.

Vision requires perception of both coarse layout and fine details of objects. In this issue of Neuron, Lu et al. (2018) describe a possible basis for the latter: neuronal clusters in area V4 coding high-acuity information, despite the tendency along the visual hierarchy to generate global representations of objects.

Altering spatial priority maps via statistical learning of target selection and distractor filtering.

The cognitive system has the capacity to learn and make use of environmental regularities - known as statistical learning (SL), including for the implicit guidance of attention. For instance, it is known that attentional selection is biased according to the spatial probability of targets; similarly, changes in distractor filtering can be triggered by the unequal spatial distribution of distractors. Open questions remain regarding the cognitive/neuronal mechanisms underlying SL of target selection and distractor filtering. Crucially, it is unclear whether the two processes rely on shared neuronal machinery, with unavoidable cross-talk, or they are fully independent, an issue that we directly addressed here. In a series of visual search experiments, participants had to discriminate a target stimulus, while ignoring a task-irrelevant salient distractor (when present). We systematically manipulated spatial probabilities of either one or the other stimulus, or both. We then measured performance to evaluate the direct effects of the applied contingent probability distribution (e.g., effects on target selection of the spatial imbalance in target occurrence across locations) as well as its indirect or "transfer" effects (e.g., effects of the same spatial imbalance on distractor filtering across locations). By this approach, we confirmed that SL of both target and distractor location implicitly bias attention. Most importantly, we described substantial indirect effects, with the unequal spatial probability of the target affecting filtering efficiency and, vice versa, the unequal spatial probability of the distractor affecting target selection efficiency across locations. The observed cross-talk demonstrates that SL of target selection and distractor filtering are instantiated via (at least partly) shared neuronal machinery, as further corroborated by strong correlations between direct and indirect effects at the level of individual participants. Our findings are compatible with the notion that both kinds of SL adjust the priority of specific locations within attentional priority maps of space.

Temporally evolving gain mechanisms of attention in macaque area V4.

Cognitive attention and perceptual saliency jointly govern our interaction with the environment. Yet, we still lack a universally accepted account of the interplay between attention and luminance contrast, a fundamental dimension of saliency. We measured the attentional modulation of V4 neurons' contrast response functions (CRFs) in awake, behaving macaque monkeys and applied a new approach that emphasizes the temporal dynamics of cell responses. We found that attention modulates CRFs via different gain mechanisms during subsequent epochs of visually driven activity: an early contrast-gain, strongly dependent on prestimulus activity changes (baseline shift); a time-limited stimulus-dependent multiplicative modulation, reaching its maximal expression around 150 ms after stimulus onset; and a late resurgence of contrast-gain modulation. Attention produced comparable time-dependent attentional gain changes on cells heterogeneously coding contrast, supporting the notion that the same circuits mediate attention mechanisms in V4 regardless of the form of contrast selectivity expressed by the given neuron. Surprisingly, attention was also sometimes capable of inducing radical transformations in the shape of CRFs. These findings offer important insights into the mechanisms that underlie contrast coding and attention in primate visual cortex and a new perspective on their interplay, one in which time becomes a fundamental factor.NEW & NOTEWORTHY We offer an innovative perspective on the interplay between attention and luminance contrast in macaque area V4, one in which time becomes a fundamental factor. We place emphasis on the temporal dynamics of attentional effects, pioneering the notion that attention modulates contrast response functions of V4 neurons via the sequential engagement of distinct gain mechanisms. These findings advance understanding of attentional influences on visual processing and help reconcile divergent results in the literature.

Reward-based plasticity of spatial priority maps: Exploiting inter-subject variability to probe the underlying neurobiology.

Recent evidence indicates that the attentional priority of objects and locations is altered by the controlled delivery of reward, reflecting reward-based attentional learning. Here, we take an approach hinging on intersubject variability to probe the neurobiological bases of the reward-driven plasticity of spatial priority maps. Specifically, we ask whether an individual's susceptibility to the reward-based treatment can be accounted for by specific predictors, notably personality traits that are linked to reward processing (along with more general personality traits), but also gender. Using a visual search protocol, we show that when different target locations are associated with unequal reward probability, different priorities are acquired by the more rewarded relative to the less rewarded locations. However, while males exhibit the expected pattern of results, with greater priority for locations associated with higher reward, females show an opposite trend. Critically, both the extent and the direction of reward-based adjustments are further predicted by personality traits indexing reward sensitivity, indicating that not only male and female brains are differentially sensitive to reward, but also that specific personality traits further contribute to shaping their learning-dependent attentional plasticity. These results contribute to a better understanding of the neurobiology underlying reward-dependent attentional learning and cross-subject variability in this domain.

Augmenting distractor filtering via transcranial magnetic stimulation of the lateral occipital cortex.

Visual selective attention (VSA) optimizes perception and behavioral control by enabling efficient selection of relevant information and filtering of distractors. While focusing resources on task-relevant information helps counteract distraction, dedicated filtering mechanisms have recently been demonstrated, allowing neural systems to implement suitable policies for the suppression of potential interference. Limited evidence is presently available concerning the neural underpinnings of these mechanisms, and whether neural circuitry within the visual cortex might play a causal role in their instantiation, a possibility that we directly tested here. In two related experiments, transcranial magnetic stimulation (TMS) was applied over the lateral occipital cortex of healthy humans at different times during the execution of a behavioral task which entailed varying levels of distractor interference and need for attentional engagement. While earlier TMS boosted target selection, stimulation within a restricted time epoch close to (and in the course of) stimulus presentation engendered selective enhancement of distractor suppression, by affecting the ongoing, reactive instantiation of attentional filtering mechanisms required by specific task conditions. The results attest to a causal role of mid-tier ventral visual areas in distractor filtering and offer insights into the mechanisms through which TMS may have affected ongoing neural activity in the stimulated tissue.

Altering spatial priority maps via reward-based learning.

Spatial priority maps are real-time representations of the behavioral salience of locations in the visual field, resulting from the combined influence of stimulus driven activity and top-down signals related to the current goals of the individual. They arbitrate which of a number of (potential) targets in the visual scene will win the competition for attentional resources. As a result, deployment of visual attention to a specific spatial location is determined by the current peak of activation (corresponding to the highest behavioral salience) across the map. Here we report a behavioral study performed on healthy human volunteers, where we demonstrate that spatial priority maps can be shaped via reward-based learning, reflecting long-lasting alterations (biases) in the behavioral salience of specific spatial locations. These biases exert an especially strong influence on performance under conditions where multiple potential targets compete for selection, conferring competitive advantage to targets presented in spatial locations associated with greater reward during learning relative to targets presented in locations associated with lesser reward. Such acquired biases of spatial attention are persistent, are nonstrategic in nature, and generalize across stimuli and task contexts. These results suggest that reward-based attentional learning can induce plastic changes in spatial priority maps, endowing these representations with the "intelligent" capacity to learn from experience.