Biology subjects

Theeuwes, J.

Publications and source records attributed to Theeuwes, J..

At least 19 recordsLinked to original sources

bioRxiv2025

The neural correlates of parallel and serial search

For almost half a century, target-distractor similarity has been known to induce different visual search modes. When a target is highly salient, it can pop out, suggesting parallel processing of all items irrespective of set size. By contrast, high similarity among items requires item-by-item comparison with an attentional template, a characteristic of serial search. Despite this long-standing distinction, little is known about the neural correlates of search modes, as typical differences in visual displays confound interpretation. Here, we contrasted the neural correlates of serial and parallel search under visually identical displays. Across distinct blocks, we biased 24 participants (21 female) toward parallel or serial search by varying target-distractor similarity, thereby directing attentional focus toward a single feature or conjunction. Embedded among inducer trials, test trials were visually identical across all blocks and afforded both parallel and serial search. Behavioral analyses confirmed successful induction of distinct search modes during test trials. EEG decoding reliably discriminated search modes and these neural patterns generalized across inducer and test trials. Attentional deployment toward the target differed across search modes, revealing topographical differences in target location representations. The strength of target-location representations correlated with response times, indicating that during parallel test trials participants switched search strategies when the target was not detected early. Moreover, target representations diverged between search modes: a temporally stable pattern emerged during serial search, suggesting reliance on working memory, whereas parallel search was characterized by more dynamic representations, likely reflecting prioritization of the relevant feature. These findings demonstrate that search history shapes search mode, giving rise to clearly distinct neural dynamics even under visually identical stimulation.

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bioRxiv2025

Dynamic competition between bottom-up saliency and top-down goals in early visual cortex

Task-irrelevant yet salient stimuli can elicit automatic, bottom-up attentional capture and compete with top-down, goal-directed processes for neural representation. However, the temporal dynamics underlying this competition, and how they influence early visual processing, remain poorly understood. Here, we combined electroencephalography (EEG) with Rapid Invisible Frequency Tagging (RIFT) to non-invasively and simultaneously track early visual cortex responses to target and distractor. Both target and distractor evoked stronger initial RIFT responses than nontargets, reflecting top-down and bottom-up attentional effects on early visual processing. Importantly, the presence of a distractor attenuated the initial RIFT response to the target, reflecting competition during the initial stages of visual processing and predicting subsequent behavioral performance. RIFT responses to the distractor eventually even decreased below responses to the target and nontarget, representing active suppression of task-irrelevant but salient stimuli. We show that the dynamic interplay between top-down control and bottom-up saliency directly impacts early visual responses, thereby illuminating a complete timeline of attentional competition in visual cortex.

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bioRxiv2025

Pre-search attentional focus supports learned suppression in visual search

Salient distractors often capture our attention, disrupting ongoing tasks. Recent studies suggest that, through statistical learning, prior experiences regarding distractor locations can reduce distraction by suppressing their corresponding locations. However, the proactive neural mechanisms supporting this learned suppression remain unclear. Our findings demonstrate that participants learn to suppress locations that are more likely to contain distractors relative to other locations. Using frequency tagging in electroencephalography (EEG) recordings, we observed significantly different tagging responses between high- and low-probability locations, along with a general decrease in alpha power (8-12 Hz) prior to search onset. Notably, the higher tagging frequency power at high-probability locations suggests that participants allocated greater attentional focus to these locations in anticipation of the search. These results suggest that anticipatory attentional deployment precedes the suppression of high-probability distractor locations after the onset of visual search.

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bioRxiv2025

Statistical learning drives anticipatory micro-saccades toward suppressed distractor locations

Statistical learning enables individuals to suppress locations associated with salient distractors, yet the mechanisms underlying this suppression remain unclear. Proactive accounts propose that suppression operates without prior attentional allocation to distractor locations, whereas reactive accounts suggest that suppression requires covert attention to the distractor location before it can be engaged. To address this ongoing debate, the current study recorded micro-saccades--an index of covert attention--during the pre-stimulus interval, alongside electroencephalogram (EEG) data collected during a visual search task. Participants were instructed to ignore a salient distractor that occurred more frequently at a specific location. Statistical learning reduced attentional capture for distractors presented at this high-probability location, and this effect was accompanied by oculomotor markers: micro-saccade rates decreased before stimulus onset relative to a control condition. Strikingly, these anticipatory micro-saccades were more often directed toward high-probability distractor locations than away from them, consistent with a reactive suppression mechanism. In parallel, alpha-band activity (8-14 Hz) carried decodable representations of high-probability distractor locations, indicating preparatory neural tuning. Overall, these findings provide evidence that the oculomotor system is closely involved in encoding and responding to learned spatial regularities.

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bioRxiv2024

Dual-format attentional template during preparation in human visual cortex

Goal-directed attention relies on forming internal templates of key information relevant for guiding behavior, particularly when preparing for upcoming sensory inputs. However, evidence on how these attentional templates is represented during preparation remains controversial. Here, we combine functional magnetic resonance imaging (fMRI) with an orientation cueing task to isolate preparatory activity from stimulus-evoked responses. Using multivariate pattern analysis, we found decodable information of the to-be-attended orientation during preparation; yet preparatory activity patterns were different from those evoked when actual orientations were perceived. When perturbing the neural activity by means of a visual impulse (pinging technique), the preparatory activity patterns in visual cortex resembled those associated with perceiving these orientations. The observed differential patterns with and without the impulse perturbation suggest a predominantly non-sensory format and a latent, sensory-like format of representation during preparation. Furthermore, the emergence of the sensory-like template coincided with enhanced information connectivity between V1 and frontoparietal areas and was associated with improved behavioral performance. By engaging this dual-format mechanism during preparation, the brain is able to encode both abstract, non-sensory information and more detailed, sensory information, potentially providing advantages for adaptive attentional control. For example, consistent with recent theories of visual search, a predominantly non-sensory template can support the initial guidance and a latent sensory-like format can support prospective stimulus processing.

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bioRxiv2024

The spatial reference frame of history-driven distractor suppression and target enhancement

The world around us is inherently structured and often repetitive. Research has shown that we can implicitly learn to prioritize relevant objects and locations while filtering out distracting information, creating an integrated priority map for attention allocation. The current study examines whether providing an object-like reference frame would induce an object-centered attentional bias or whether the bias would remain in egocentric (viewpoint-centered) coordinates. The search display consisted of six stimuli that were surrounded by a wheel and square frame. In two experiments, either a distractor or a target appeared more frequently in one location, leading to the suppression or enhancement of that location, respectively. Learning blocks were followed by test blocks, where the frame rotated, creating egocentric-matching and object-centered locations. These experiments showed that both target and distractor learning relied on an egocentric reference frame only. In follow-up experiments, the likely target and distractor location rotated dynamically with the frame during learning. This revealed that participants can learn to enhance a likely target location in an object-centered manner. We hypothesized that while space-based learning feeds into a priority map reliant on an egocentric reference frame, object-based learning allows for implicit prioritization of subparts of objects independent of their spatial orientation. Public significance statementOur brains cannot process the overwhelming amount of visual information we encounter daily. Fortunately, the world is inherently structured and has patterns we can learn, helping us to selectively focus on whats important and ignore distractions. This study examines how we use these patterns in dynamic, ever-changing environments. The findings show that when regularities are learned in static settings, our learned attentional biases remain tied to our static viewpoints. But in dynamic environments, attentional priorities can be tied to objects, irrespective of the objects orientation, while suppressed distractor locations remain tied to specific viewpoints. This discovery helps us understand how our brain adapts to complex, real-world situations.

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bioRxiv2024

Pinging the Hidden Attentional Priority Map: Suppression Needs Attention

Attentional capture by an irrelevant salient distractor is attenuated when the distractor is presented more frequently in one location compared to other locations, suggesting that people learn to suppress an irrelevant salient location. However, to date it is unclear whether this suppression is proactive, applied before attention has been directed to the distractor location, or reactive, occurring after attention has been directed to that specific location. The aim of the present study is to investigate how suppression is accomplished by using the pinging technique, which allows one to probe how attention is distributed across the visual field prior to the presentation of the search display. In an EEG experiment, participants performed a visual search task wherein they were tasked with identifying a shape singleton in the presence of an irrelevant color singleton. Compared to all other locations, this color singleton appeared more frequently at a specific location, which was termed the high-probability location. Prior to the search task, we introduced a continuous recall spatial memory task to reveal the hidden attentional priority map. Participants had to memorize the location of a memory cue continuously and report this location after the visual search task. Critically, after the presentation of the memory cue but before the onset of the search display, a neutral placeholder display was presented to probe how the hidden priority map is reconfigured by the learned distractor suppression. Behaviorally, there was clear evidence that the high-probability location was suppressed, as search was more efficient when the distractor appeared at this location. To examine the priority map prior to search, we adopted an inverted encoding approach to reconstruct the tuning profile of the memorized position in the spatial memory task. Inverted modeling resulted in reliable tuning profiles during memory maintenance that gradually decayed and that were revived again by the onset of a neutral placeholder display preceding search. After the onset of the placeholders, the tuning profile observed was characterized by a spatial gradient centered over the high-probability location, with tuning being most pronounced at the-to-be suppressed location. This finding suggests that while learned suppression is initiated prior to search display onset, it is preceded by an initial phase of spatial selection, which is in line with a reactive suppression account. Together these results further our understanding of the mechanism of spatial distractor suppression.

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bioRxiv2024

Proactive distractor suppression in early visual cortex

Avoiding distraction by salient yet irrelevant stimuli is critical when accomplishing daily tasks. One possible mechanism to accomplish this is by suppressing stimuli that may be distracting such that they no longer compete for attention. While the behavioral benefits of distractor suppression are well-established, its neural underpinnings are not yet fully understood. In an fMRI study, we examined whether and how sensory responses in early visual areas show signs of distractor suppression after incidental learning of spatial statistical regularities. Participants were exposed to an additional singleton task where, unbeknownst to them, one location more frequently contained a salient distractor. We analyzed whether visual responses in terms of fMRI BOLD were modulated by this distractor predictability. Our findings indicate that implicit spatial priors shape sensory processing even at the earliest stages of cortical visual processing, evident in early visual cortex as a suppression of stimuli at locations which frequently contained distracting information. Notably, while this suppression was spatially (receptive field) specific, it did extend to nearby neutral locations, and occurred regardless of whether distractors, nontarget items or targets were presented at this location, suggesting that suppression arises before stimulus identification. Crucially, we observed similar spatially specific neural suppression even if search was only anticipated, but no search display was presented. Our results highlight proactive modulations in early visual cortex, where potential distractions are suppressed preemptively, before stimulus onset, based on learned expectations. Combined, our study underscores how the brain leverages implicitly learned prior knowledge to optimize sensory processing and attention allocation.

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bioRxiv2024

Distractor suppression operates exclusively in retinotopic coordinates

Our attention is influenced by past experiences, and recent studies have shown that individuals learn to extract statistical regularities in the environment, resulting in attentional suppression of locations that are likely to contain a distractor (high-probability location). However, little is known as to whether this learned suppression operates in retinotopic (relative to the eyes) or spatiotopic (relative to the world) coordinates. In the current study, two circular search arrays were presented side by side. Participants learned the high-probability location from a learning array presented on one side of the display (e.g., left). After several trials, participants shifted their gaze to the center of the the test array (e.g., located on the right side) in which all locations were equally likely to contain the distractor. Due to the saccade, the test array contained both a spatiotopic and a retinotopic matching location relative to the original high-probability location. The current findings show that, following saccadic eye movements, the learned suppression remained in retinotopic coordinates only, with no measurable transfer to spatiotopic coordinates. Even in a rich environment, attentional suppression still operated exclusively in retinotopic coordinates. We speculate that learned suppression may be resolved by changing synaptic weights in early visual areas. Significance statementIn our daily lives, attention is shaped by past experiences, guiding us to suppress locations that are likely to contain distractions. While this phenomenon has been studied extensively with static search displays, the real world is dynamic - we are constantly moving our eyes. This study addressed this issue by investigating what happens when we learn to suppress a likely distractor location while making eye movements. Do we suppress the same location in space (spatiotopic), or does the learned suppression persist relative to our eyes (retinotopic)? The current findings provide clear evidence of suppression in retinotopic coordinates only.

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bioRxiv2024

Neural representations of predicted events: Evidence from time-resolved EEG decoding

Through statistical learning, humans are able to extract temporal regularities, using the past to predict the future. Evidence suggests that learning relational structures makes it possible to anticipate the imminent future; yet, the neural dynamics of predicting the future and its time-course remain elusive. To examine whether future representations are denoted in a temporally discounted fashion, we used the high-temporal-resolution of electroencephalography (EEG). Observers were exposed to a fixed sequence of events at four unique spatial positions within the display. Using multivariate pattern analyses trained on independent pattern estimators, we were able to decode the spatial position of dots within full sequences, and within randomly intermixed partial sequences wherein only a single dot was presented. Crucially, within these partial sequences, subsequent spatial positions could be reliably decoded at their expected moment in time. These findings highlight the dynamic weight changes within the assumed spatial priority map and mark the first implementation of EEG to decode predicted, yet critically omitted events. Impact statementUtilizing high-temporal-resolution EEG, the dynamic weight changes of assumed spatial priority map were visualized by decoding the spatial position of expected, yet omitted, events at their expected moment in time.

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bioRxiv2023

The Electrophysiological Markers of Statistically Learned Attentional Enhancement: Evidence for a Saliency Based Mechanism

It has been well established that attention can be sharpened through the process of statistical learning - whereby visual search is optimally adapted to the spatial probabilities of a target in visual fields. Specifically, attentional processing becomes more efficient when targets appear at high relatively to low probability locations. Statistically learned attentional enhancement has been shown to differ behaviorally from the more well studied top-down and bottom-up forms of attention; and while the electrophysiological characteristics of top-down and bottom-up attention have been well explored, relatively little work has been done to characterize the electrophysiological correlates of statistically learned attentional enhancement. In the current study, EEG data was collected while participants performed the additional singleton task with an unbalanced target distribution. Encephalographic data was then analyzed for two well-known correlates of attentional processing - alpha lateralization and the N2pc component. Our results showed that statistically learned attentional enhancement is not characterized by alpha lateralization, thereby differentiating it from top-down enhancement. Yet targets at high probability locations did reliably produce larger N2pc amplitudes, a known marker of increased bottom-up capture due to higher target-distractor contrasts. These results support an interpretation of the probability cuing effects where the improved processing of targets at expected locations is mediated by a saliency-based mechanism - boosting the salience of targets appearing at high-probability locations relative to those at low-probability locations. Significance statementThings are easier to find when you have a good idea of where they should be - e.g. shoes on the floor and birds in the sky. Expectations of where things are likely to be found can be implicitly learned without much, if any, awareness. Until now, little was known about how these implicit spatial biases change the representation of items in the brain. In the current work, we present EEG recordings which suggest that the brain may represent items in common locations as more salient than in other locations in space. These findings inform how the brain represents implicit search expectations; supporting a model where items in expected areas in space capture attention more frequently because they are represented by the brain as more salient.

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bioRxiv2022

Electrophysiological indices of distractor processing in visual search are shaped by target expectations.

Although in many cases salient stimuli capture attention involuntarily, it has been proposed recently that under certain conditions the bottom-up signal generated by such stimuli can be proactively suppressed. In support of this signal suppression hypothesis, ERP studies have demonstrated that salient stimuli that do not capture attention elicit a distractor positivity (PD), a putative neural index of suppression. At the same time, it is becoming increasingly clear that regularities across preceding search episodes have a large influence on attentional selection. Yet to date, studies in support of the signal suppression hypothesis have largely ignored the role of selection history on the processing of distractors. The current study addressed this issue by examining how electrophysiological markers of attentional selection (N2pc) and suppression (PD) elicited by targets and distractors respectively were modulated when the search target randomly varied instead of being fixed across trials. Results showed that while target selection was unaffected by this manipulation, both in terms of manual response times, as well as in terms of the N2pc component, the PD component was reliably attenuated when the target features varied randomly across trials. This result demonstrates that the distractor PD, which is typically considered the marker of selective distractor processing cannot unequivocally be attributed to suppression only, as it also, at least in part, reflects the upweighting of target features.

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bioRxiv2022

Pinging the brain to reveal the hidden attentional priority map

Attention has been usefully thought of as organized in priority maps - putative maps of space where attentional priority is weighted across spatial regions in a winner-take-all competition for attentional deployment. Recent work has highlighted the influence of past experiences on the weighting of spatial priority - called selection history. Aside from being distinct from more well-studied, top-down forms of attentional enhancement, little is known about the neural substrates of history-mediated attentional priority. Using a task known to induce statistical learning of target distributions, in an EEG study we demonstrate that this otherwise invisible, latent attentional priority map can be visualized during the intertrial period using a pinging technique in conjunction with multivariate pattern analyses. Our findings not only offer a novel method of visualizing the history-mediated attentional priority map, but also shed light on the underlying mechanisms allowing our past experiences to influence future behaviour.

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bioRxiv2020

Attention and reinforcement learning in Parkinson's disease

Dopamine is known to be involved in several important cognitive processes, most notably in learning from rewards and in the ability to attend to task-relevant aspects of the environment. Both of these features of dopaminergic signalling have been studied separately in research involving Parkinsons disease (PD) patients, who exhibit diminished levels of dopamine. Here, we tie together some of the commonalities in the effects of dopamine on these aspects of cognition by having PD patients (ON and OFF dopaminergic medication) and healthy controls (HCs) perform two tasks that probe these processes. Within-patient behavioural measures of distractibility, from an attentional capture task, and learning performance, from a probabilistic classification reinforcement learning task, were included in one model to assess the role of distractibility during learning. Dopamine medication state and distractibility level were found to have an interactive effect on learning performance; less distractibility in PD ON was associated with higher accuracy during learning, and this was altered in PD OFF. Functional magnetic resonance imaging (fMRI) data acquired during the learning task furthermore allowed us to assess multivariate patterns of positive and negative outcomes in fronto-striatal and visual brain regions involved in both learning processes and the executive control of attention. Here, we demonstrate that while PD ON show a clearer distinction between outcomes than OFF in dorsolateral prefrontal cortex (DLPFC) and putamen, PD OFF show better distinction of activation patterns in visual regions that respond to the stimuli presented during the task. These results demonstrate that dopamine plays a key role in modulating the interaction between attention and learning at the level of both behaviour and activation patterns in the brain.

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bioRxiv2019

Multivariate analysis of EEG activity indexes contingent and non-contingent attentional capture

It is well known that salient yet irrelevant singleton can capture attention, even when this is inconsistent with the current goals of the observer (Theeuwes, 1992; 2010). Others however have claimed that capture is critically contingent on the goals of the observer: Capture is strongly modulated (or even eliminated) when the irrelevant singleton does not match the target-defining properties (Folk, Remington, & Johnston, 1992). There has been a long-standing debate on whether attentional capture can be explained by goal-driven and/or stimulus-driven accounts. Here, we shed further light on this phenomenon by using EEG activity (raw EEG and alpha power) to provide a time-resolved index of attentional orienting. Participants searched for a target defined by a pre-specified color. The search display was preceded by a singleton cue that either matched the color of the upcoming target (contingent cues), or that appeared in an irrelevant color (non-contingent cues). Multivariate analysis of raw EEG and alpha power revealed preferential tuning to the location of both contingent and non-contingent cues, with a stronger bias towards contingent than non-contingent cues. The time course of these effects, however, depended on the neural signal. Raw EEG data revealed attentional orienting towards the cue early on in the trial (>156 ms), while alpha power revealed sustained spatial selection in the cued locations at a later moment in the trial (>250 ms). Moreover, while raw EEG showed stronger capture by contingent cues during this early time window, the advantage for contingent cues arose during a later time window in alpha band activity. Thus, our findings suggest that raw EEG activity and alpha-band power tap into distinct neural processes that index movements of covert spatial attention. Both signals provide clear neural evidence that both contingent and non-contingent cues can capture attention, and that this process is robustly shaped by the target-defining properties in the current block of trials.

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bioRxiv2019

Spontaneous eye blink rate predicts individual differences in exploration and exploitation during reinforcement learning

Spontaneous eye blink rate (sEBR) has been linked to striatal dopamine function and to how individuals make value-based choices after a period of reinforcement learning (RL). While sEBR is thought to reflect how individuals learn from the negative outcomes of their choices, this idea has not been tested explicitly. This study assessed how individual differences in sEBR relate to learning by focusing on the cognitive processes that drive RL. Using Bayesian latent mixture modelling to quantify the mapping between RL behaviour and its underlying cognitive processes, we were able to differentiate low and high sEBR individuals at the level of these cognitive processes. Further inspection of these cognitive processes indicated that sEBR uniquely indexed explore-exploit tendencies during RL: lower sEBR predicted exploitative choices for high valued options, whereas higher sEBR predicted exploration of lower value options. This relationship was additionally supported by a network analysis where, notably, no link was observed between sEBR and how individuals learned from negative outcomes. Our findings challenge the notion that sEBR predicts learning from negative outcomes during RL, and suggest that sEBR predicts individual explore-exploit tendencies. These then influence value sensitivity during choices to support successful performance when facing uncertain reward.

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bioRxiv2019

Anticipatory distractor suppression elicited by statistical regularities in visual search

Salient yet irrelevant objects often capture our attention and interfere with our daily tasks. Distraction by salient objects can be reduced by suppressing the location where they are likely to appear. The question we addressed here was whether suppression of frequent distractors is already implemented beforehand, in anticipation of the stimulus. Using electroencephalography (EEG), we recorded cortical activity of human participants searching for a target while ignoring a salient distractor. The distractor was presented more often at one location than at any other location. We found reduced capture for distractors at frequent locations, indicating that participants learned to avoid distraction. Critically, we found evidence for proactive suppression as already prior to display onset, there was enhanced power in parieto-occipital alpha oscillations contralateral to the frequent distractor location - a signal known to occur in anticipation of irrelevant information. Locked to display onset, event-related potentials analysis showed a distractor-suppression-related PD component for this location. Importantly, this PD was found regardless of whether distracting information was presented at the frequent location. In addition, there was an early PD component representing an early attentional index of the frequent distractor location. Our results are show anticipatory (proactive) suppression of frequent distractor locations in visual search already starting prior to display onset.

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bioRxiv2019

Learning in visual regions as support for the bias in future value-driven choice

Reinforcement learning can bias decision-making towards the option with the highest expected outcome. Cognitive learning theories associate this bias with the constant tracking of stimulus values and the evaluation of choice outcomes in the striatum and prefrontal cortex. Decisions however first require processing of sensory input, and to-date, we know far less about the interplay between learning and perception. This fMRI study (N=43), relates visual BOLD responses to value-beliefs during choice, and, signed prediction errors after outcomes. To understand these relationships, which co-occurred in the striatum, we sought relevance by evaluating the prediction of future value-based decisions in a separate transfer phase where learning was already established. We decoded choice outcomes with a 70% accuracy with a supervised machine learning algorithm that was given trial-by-trial BOLD from visual regions alongside more traditional motor, prefrontal, and striatal regions. Importantly, this decoding of future value-driven choice outcomes again highligted an important role for visual activity. These results raise the intriguing possibility that the tracking of value in visual cortex is supportive for the striatal bias towards the more valued option in future choice.

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