Endogenous Attention Research Articles

Coupling of saccade plans to endogenous attention during urgent choices

The neural mechanisms that willfully direct attention to specific locations in space are closely related to those for generating targeting eye movements (saccades). However, the degree to which the voluntary deployment of attention to a location necessarily activates a corresponding saccade plan remains unclear. One problem is that attention and saccades are both automatically driven by salient sensory events; another is that the underlying processes unfold within tens of milliseconds only. Here, we use an urgent task design to resolve the evolution of a visuomotor choice on a moment-by-moment basis while independently controlling the endogenous (goal-driven) and exogenous (salience-driven) contributions to performance. Human participants saw a peripheral cue and, depending on its color, either looked at it (prosaccade) or looked at a diametrically opposite, uninformative non-cue (antisaccade). By varying the luminance of the stimuli, the exogenous contributions could be cleanly dissociated from the endogenous process guiding the choice over time. According to the measured time courses, generating a correct antisaccade requires about 30 ms more processing time than generating a correct prosaccade based on the same perceptual signal. The results indicate that saccade plans elaborated during fixation are biased toward the location where attention is endogenously deployed, but the coupling is weak and can be willfully overridden very rapidly.

Endogenous Attention Affects Decision-related Neural Activity but Not Afferent Visual Responses.

Endogenous shifts of spatial attention toward an upcoming stimulus are associated with improvements in behavioral responses to the stimulus, preparatory retinotopic shifts in alpha power, and changes in ERPs. Although attentional modulation of several early sensory ERPs is well established, there is still debate about under what circumstances attention affects the earliest cortical visual evoked response-the C1 ERP component-which is putatively generated from afferent input into primary visual cortex. Moreover, the effects of spatial attention on the recently discovered ERP signature of evidence accumulation-the central parietal positivity (CPP)-have not been fully characterized. The present study assessed the effect of spatial attention on the C1 and CPP components through a spatially cued contrast discrimination task using stimuli that were specifically designed to produce large-amplitude C1 responses and that varied in sensory evidence strength to characterize the CPP. Participants responded according to which of two checkerboard stimuli had greater contrast following an 80% valid cue toward the upper or lower visual field. Prestimulus alpha power changed topographically based on the cue, suggesting participants shifted attention to prepare for the upcoming stimuli. Despite these attentional shifts in alpha power and the fact that the stimuli reliably elicited C1 responses several times greater than many prior studies, there was no evidence of an attention effect on the C1. The CPP, however, showed a clear increase in build-up rate on valid trials. Our findings suggest that endogenous attention may not affect the early C1 ERP component but may improve behavior at a decision stage, as reflected in brain signals related to evidence accumulation (the CPP).

Effect of attention on ensemble perception: Comparison between exogenous attention, endogenous attention, and depth.

Ensemble perception is an important ability of human beings that allows one to extract summary information for scenes and environments that contain information that far exceeds the processing limit of the visual system. Although attention has been shown to bias ensemble perception, two important questions remain unclear: (1) whether direct manipulations on different types of spatial attention could produce similar effects on ensembles and (2) whether factors potentially influencing the attention distribution, such as depth perception, could evoke an indirect effect of attention on ensemble representation. This study aims to address these questions. In Experiments 1 and 2, two types of precues were used to evoke exogenous and endogenous attention, respectively, and the ensemble color perceptions were examined. We found that both exogenous and endogenous attention biased ensemble representation towards the attended items, and the latter produced a greater effect. In Experiments 3 and 4, we examined whether depth perception could affect color ensembles by indirectly influencing attention allocation in 3D space. The items were separated in two depth planes, and no explicit cues were applied. The results showed that color ensemble was biased to closer items when depth information was task relevant. This suggests that ensemble perception is naturally biased in 3D space, probably through the mechanism of attention. Computational modeling consistently showed that attention exerted a direct shift on the ensemble statistics rather than averaging the feature values over the cued and noncued items, providing evidence against an averaging process of individual perception.

Constraining the Possible Mechanisms Underlying Performance Improvements Following Peripheral Vision Training

AbstractSome training paradigms can improve performance specific to the trained portion of the visual field. Similarly, experience with both pathological and simulated central vision loss can result in compensatory improvement in performance specific to a spared retinal location. The mechanisms underlying these improvements are still debated. Modifications in the capacity to allocate attention to trained locations might explain some of the changes in performance after learning, especially given similarities between behavioral improvements due to training and improvements due to changes in attention. Using a gaze-contingent simulated scotoma paradigm which simulates central vision loss, we tested whether training to use peripheral vision influenced three aspects of visual attention: habitual attention, dynamic exogenous attention, and dynamic endogenous attention. After training, performance improvements were consistent with increased habitual attention to the trained location. Conversely, measures of dynamic shifts of attention (exogenous and endogenous attention) improved similarly in both trained and untrained locations. The lack of retinotopic specificity in dynamic attention improvements suggests that retinotopically specific perceptual improvements following simulated central vision loss are not mediated by dynamic attention changes. On the other hand, habitual attention did change retinotopically, leaving the possibility open that this aspect of attention may drive some retinotopically specific training effects. This work constrains the range of mechanisms that could underlie performance improvements after peripheral vision training, suggesting that habitual attention and dynamic attention are affected independently.

Dissociable Effects of Endogenous and Exogenous Attention on Crowding: Evidence from Event-Related Potentials.

Crowding is a common visual phenomenon that can significantly impair the recognition of objects in peripheral vision. Two recent behavioral studies have revealed that both exogenous and endogenous attention can alleviate crowding, but exogenous attention seems to be more effective. The present study employed the event-related potential (ERP) technique to explore the electrophysiological characteristics of the influence of these two types of attention on crowding. In the experiment, participants were required to judge whether the letter "T" was upright or inverted, which may be preceded by an exogenous cue or an endogenous cue indicating the location of the target letter. The behavioral results showed that while exogenous cues reduced crowding in all stimulus onset asynchronies (SOAs), endogenous attention took effects only in long SOA. The ERP results indicated that both endogenous and exogenous cues significantly alleviated the inhibition of visual crowding on the N1 component. However, the endogenous cue was effective only under long SOA, while the exogenous cue was effective only under short SOA conditions. In addition, invalid exogenous cues induced a larger P3 wave amplitude than valid ones in the short SOA condition, but endogenous attention did not show such a difference. These results indicate that both endogenous and exogenous attention can alleviate the effects of visual crowding, but they differ in effect size and temporal dynamics.

How preferences enslave attention: calling into question the endogenous/exogenous dichotomy from an active inference perspective

AbstractIt is easy to think of attention as a purely sensorimotor, exogenous mechanism divorced from the influence of an agent’s preferences and needs. However, according to the active inference framework, such a strict reduction cannot be straightforwardly invoked, since all cognitive and behavioural processes can at least be described as maximising the evidence for a generative model entailed by the ongoing existence of that agent; that is, the minimisation of variational free energy. As such, active inference models could cast an (embodied) cognitive mechanism like attention, described in this paper as a relevance filter, as constrained (or enslaved) by these prior preferences for which an agent must seek evidence, whether or not such priors are having direct, real-time neurocognitive effects on the sensorimotor loops that couple the attending agent and her surrounding environment. This duality with respect to the role of priors corresponds to a wider, ongoing debate in the active inference community regarding the framework’s explanatory power. More specifically, the debate centres on whether the notion of a generative model and the priors embedded ubiqitously therein act as a purely useful instrumental tool for scientists aiming to model the behaviours of self-organising entities, or, rather, the brain (and body) is genuinely constituted by a predictive hierarchy within which higher-order dynamics constrain and contextualise activity unfolding at lower levels. With a focus on the second (ontologically realist) construal of active inference presented here, this paper argues that in cognitive systems endowed with attentional schema, higher-order preferences do, indeed, impose a demonstrable and powerful modulating effect on the way attention unfolds. Furthermore, these preferences in question transcend the contingent, task-relevant goals that have already been shown to bias attention. Rather, attention is powerfully tuned by the most-deep rooted priors the agent possesses, such that, when sensory evidence against these priors is observed and free energy spikes, the agent attentionally prioritises the homeostatic restoration of these preferred states over their shorter-term desires. This suggests that, at its core, attention is a goal-driven process, which calls into question the putative dichotomy that exists between endogenous (goal-directed) attention and exogenous (stimulus-driven) attention. What emerges in its place is a symbiotic relationship between attention and preferences, whereby the fulfilment of the latter rests on successful application of the former, and the former derives its function from the organismic need to find evidence for the latter.

Endogenous attention samples rhythmically under spatial uncertainty

Endogenous attention samples rhythmically under spatial uncertainty

Time course of microsaccades directionality during an endogenous attention task

Time course of microsaccades directionality during an endogenous attention task

Leader–follower dynamics during early social interactions matter for infant word learning

We know little about the mechanisms through which leader-follower dynamics during dyadic play shape infants' language acquisition. We hypothesized that infants' decisions to visually explore a specific object signal focal increases in endogenous attention, and that when caregivers respond to these proactive behaviors by naming the object it boosts infants' word learning. To examine this, we invited caregivers and their 14-mo-old infants to play with novel objects, before testing infants' retention of the novel object-label mappings. Meanwhile, their electroencephalograms were recorded. Results showed that infants' proactive looks toward an object during play associated with greater neural signatures of endogenous attention. Furthermore, when caregivers named objects during these episodes, infants showed greater word learning, but only when caregivers also joined their focus of attention. Our findings support the idea that infants' proactive visual explorations guide their acquisition of a lexicon.

Coupling of saccade plans to endogenous attention during urgent choices.

The neural mechanisms that willfully direct attention to specific locations in space are closely related to those for generating targeting eye movements (saccades). However, the degree to which the voluntary deployment of attention to a location necessarily activates a corresponding saccade plan remains unclear. One problem is that attention and saccades are both automatically driven by salient sensory events; another is that the underlying processes unfold within tens of milliseconds only. Here, we use an urgent task design to resolve the evolution of a visuomotor choice on a moment-by-moment basis while independently controlling the endogenous (goal-driven) and exogenous (salience-driven) contributions to performance. Human participants saw a peripheral cue and, depending on its color, either looked at it (prosaccade) or looked at a diametrically opposite, uninformative non-cue (antisaccade). By varying the luminance of the stimuli, the exogenous contributions could be cleanly dissociated from the endogenous process guiding the choice over time. According to the measured timecourses, generating a correct antisaccade requires about 30 ms more processing time than generating a correct prosaccade based on the same perceptual signal. The results indicate that saccade plans elaborated during fixation are biased toward the location where attention is endogenously deployed, but the coupling is weak and can be willfully overridden very rapidly.

Fixational eye movements and their associated evoked potentials during natural vision are altered in schizophrenia

BackgroundVisual exploration is abnormal in schizophrenia; however, few studies have investigated the physiological responses during selecting objectives in more ecological scenarios. This study aimed to demonstrate that people with schizophrenia have difficulties observing the prominent elements of an image due to a deficit mechanism of sensory modulation (active sensing) during natural vision. MethodsAn electroencephalogram recording with eye tracking data was collected on 18 healthy individuals and 18 people affected by schizophrenia while looking at natural images. These had a prominent color element and blinking produced by changes in image luminance. ResultsWe found fewer fixations when all images were scanned, late focus on prominent image areas, decreased amplitude in the eye-fixation-related potential, and decreased intertrial coherence in the SCZ group. ConclusionsThe decrease in the visual attention response evoked by the prominence of visual stimuli in patients affected by schizophrenia is generated by a reduction in endogenous attention mechanisms to initiate and maintain visual exploration. Further work is required to explain the relationship of this decrease with clinical indicators.

Conscious but not thinking-Mind-blanks during visuomotor tracking: An fMRI study of endogenous attention lapses.

Attention lapses (ALs) are complete lapses of responsiveness in which performance is briefly but completely disrupted and during which, as opposed to microsleeps, the eyes remain open. Although the phenomenon of ALs has been investigated by behavioural and physiological means, the underlying cause of an AL has largely remained elusive. This study aimed to investigate the underlying physiological substrates of behaviourally identified endogenous ALs during a continuous visuomotor task, primarily to answer the question: Were the ALs during this task due to extreme mind-wandering or mind-blanks? The data from two studies were combined, resulting in data from 40 healthy non-sleep-deprived subjects (20M/20F; mean age 27.1 years, 20-45). Only 17 of the 40 subjects were used in the analysis due to a need for a minimum of two ALs per subject. Subjects performed a random 2-D continuous visuomotor tracking task for 50 and 20 min in Studies 1 and 2, respectively. Tracking performance, eye-video, and functional magnetic resonance imaging (fMRI) were recorded simultaneously. A human expert visually inspected the tracking performance and eye-video recordings to identify and categorise lapses of responsiveness as microsleeps or ALs. Changes in neural activity during 85 ALs (17 subjects) relative to responsive tracking were estimated by whole-brain voxel-wise fMRI and by haemodynamic response (HR) analysis in regions of interest (ROIs) from seven key networks to reveal the neural signature of ALs. Changes in functional connectivity (FC) within and between the key ROIs were also estimated. Networks explored were the default mode network, dorsal attention network, frontoparietal network, sensorimotor network, salience network, visual network, and working memory network. Voxel-wise analysis revealed a significant increase in blood-oxygen-level-dependent activity in the overlapping dorsal anterior cingulate cortex and supplementary motor area region but no significant decreases in activity; the increased activity is considered to represent a recovery-of-responsiveness process following an AL. This increased activity was also seen in the HR of the corresponding ROI. Importantly, HR analysis revealed no trend of increased activity in the posterior cingulate of the default mode network, which has been repeatedly demonstrated to be a strong biomarker of mind-wandering. FC analysis showed decoupling of external attention, which supports the involuntary nature of ALs, in addition to the neural recovery processes. Other findings were a decrease in HR in the frontoparietal network before the onset of ALs, and a decrease in FC between default mode network and working memory network. These findings converge to our conclusion that the ALs observed during our task were involuntary mind-blanks. This is further supported behaviourally by the short duration of the ALs (mean 1.7 s), which is considered too brief to be instances of extreme mind-wandering. This is the first study to demonstrate that at least the majority of complete losses of responsiveness on a continuous visuomotor task are, if not due to microsleeps, due to involuntary mind-blanks.

Endogenous attention enhances contrast appearance regardless of stimulus contrast.

There has been enduring debate on how attention alters contrast appearance. Recent research indicates that exogenous attention enhances contrast appearance for low-contrast stimuli but attenuates it for high-contrast stimuli. Similarly, one study has demonstrated that endogenous attention heightens perceived contrast for low-contrast stimuli, yet none have explored its impact on high-contrast stimuli. In this study, we investigated how endogenous attention alters contrast appearance, with a specific focus on high-contrast stimuli. In Experiment 1, we utilized the rapid serial visual presentation (RSVP) paradigm to direct endogenous attention, revealing that contrast appearance was enhanced for both low- and high-contrast stimuli. To eliminate potential influences from the confined attention field in the RSVP paradigm, Experiment 2 adopted the letter identification paradigm, deploying attention across a broader visual field. Results consistently indicated that endogenous attention increased perceived contrast for high-contrast stimuli. Experiment 3 employed equiluminant chromatic letters as stimuli in the letter identification task to eliminate potential interference from contrast adaption, which might have occurred in Experiment 2. Remarkably, the boosting effect of endogenous attention persisted. Combining the results from these experiments, we propose that endogenous attention consistently enhances contrast appearance, irrespective of stimulus contrast levels. This stands in contrast to the effects of exogenous attention, suggesting that mechanisms through which endogenous attention alters contrast appearance may differ from those of exogenous attention.

Transcranial Alternating Current Stimulation over Frontal Eye Fields Mimics Attentional Modulation of Visual Processing.

Attentional control over sensory processing has been linked to neural alpha oscillations and related inhibition of cerebral cortex. Despite the wide consensus on the functional relevance of alpha oscillations for attention, precise neural mechanisms of how alpha oscillations shape perception and how this top-down modulation is implemented in cortical networks remain unclear. Here, we tested the hypothesis that alpha oscillations in frontal eye fields (FEFs) are causally involved in the top-down regulation of visual processing in humans (male and female). We applied sham-controlled, intermittent transcranial alternating current stimulation (tACS) over bilateral FEF at either 10 Hz (alpha) or 40 Hz (gamma) to manipulate attentional preparation in a visual discrimination task. Under each stimulation condition, we measured psychometric functions for contrast perception and introduced a novel linear mixed modeling approach for statistical control of neurosensory side effects of the electric stimulation. tACS at alpha frequency reduced the slope of the psychometric function, resulting in improved subthreshold and impaired superthreshold contrast perception. Side effects on the psychometric functions were complex and showed large interindividual variability. Controlling for the impact of side effects on the psychometric parameters by using covariates in the linear mixed model analysis reduced this variability and strengthened the perceptual effect. We propose that alpha tACS over FEF mimicked a state of endogenous attention by strengthening a fronto-occipitoparietal network in the alpha band. We speculate that this network modulation enhanced phasic gating in occipitoparietal cortex leading to increased variability of single-trial psychometric thresholds, measurable as a reduction of psychometric slope.

Attentional development is altered in toddlers with congenital heart disease.

Congenital Heart Disease (CHD) is the most common congenital abnormality. Survival rates are over 90%, however infants with CHD remain at high risk of attention and executive function impairments. These abilities are difficult to assess in toddlers because clinical assessments rely on language abilities which are commonly delayed in CHD. Our aim was to characterise visual attention in toddlers with CHD compared to controls and identify associations with parent-rated effortful control. Thirty toddlers with CHD (19 male, median (IQR) age at assessment 22.2 (22-23.1) months) and 66 controls from the developing human connectome project (36 male, age at assessment 22 (21.5-23.8) months) using eye-tracking tasks designed to assess multiple components of visual attention. Analyses of co-variance and regressions were used to identify differences between groups and relationships between gaze behaviours and parent-rated effortful control. Toddlers with CHD were less accurate when switching behaviours (set-shifting) [median (IQR) 79%, (28-100)] compared to controls [100% (86-100), pFDR=0.032], with worse accuracy associated with lower parent-rated effortful control in CHD but not controls (interaction pFDR=0.028). Reaction times were slower during selective [CHD 1243ms (986-1786), controls 1065ms (0851-1397), pFDR<0.001] and exogenous attention tasks [CHD 312ms (279-358), control 289 (249-331), (pFDR=0.032) and endogenous attention was less mature (prolonged looks at facial stimuli CHD 670ms (518-885), control 500ms (250-625), (pFDR=0.006). These results were unrelated to differences in cognition or socioeconomic status. In contrast, the allocation of attentional resources was preserved in CHD. We identified a profile of altered attention and early executive functioning development in CHD. Eye-tracking may provide clinically feasible, early objective measures of attention and executive function development in CHD.

Early Electrophysiological Correlates of Perceptual Consciousness Are Affected by Both Exogenous and Endogenous Attention.

It has been proposed that visual awareness negativity (VAN), which is an early ERP component, constitutes a neural correlate of visual consciousness that is independent of perceptual and cognitive mechanisms. In the present study, we investigated whether VAN is indeed a specific marker of phenomenal awareness or rather reflects the involvement of attention. To this end, we reanalyzed data collected in a previously published EEG experiment in which awareness of visual stimuli and two aspects that define attentional involvement, namely, the inherent saliency and task relevance of a stimulus, were manipulated orthogonally. During the experimental procedure, participants (n = 41) were presented with images of faces that were backward-masked or unmasked, fearful or neutral, and defined as task-relevant targets or task-irrelevant distractors. Single-trial ERP analysis revealed that VAN was highly dependent on attentional manipulations in the early time window (140-200 msec), up to the point that the effect of awareness was not observed for attentionally irrelevant stimuli (i.e., neutral faces presented as distractors). In the late time window (200-350 msec), VAN was present in all attentional conditions, but its amplitude was significantly higher in response to fearful faces and task-relevant face images than in response to neutral ones and task-irrelevant ones, respectively. In conclusion, we demonstrate that the amplitude of VAN is highly dependent on both exogenous (stimulus saliency) and endogenous attention (task requirements). Our results challenge the view that VAN constitutes an attention-independent correlate of phenomenal awareness.

Looming Angry Faces: Preliminary Evidence of Differential Electrophysiological Dynamics for Filtered Stimuli via Low and High Spatial Frequencies.

Looming motion interacts with threatening emotional cues in the initial stages of visual processing. However, the underlying neural networks are unclear. The current study investigated if the interactive effect of threat elicited by angry and looming faces is favoured by rapid, magnocellular neural pathways and if exogenous or endogenous attention influences such processing. Here, EEG/ERP techniques were used to explore the early ERP responses to moving emotional faces filtered for high spatial frequencies (HSF) and low spatial frequencies (LSF). Experiment 1 applied a passive-viewing paradigm, presenting filtered angry and neutral faces in static, approaching, or receding motions on a depth-cued background. In the second experiment, broadband faces (BSF) were included, and endogenous attention was directed to the expression of faces. Our main results showed that regardless of attentional control, P1 was enhanced by BSF angry faces, but neither HSF nor LSF faces drove the effect of facial expressions. Such findings indicate that looming motion and threatening expressions are integrated rapidly at the P1 level but that this processing relies neither on LSF nor on HSF information in isolation. The N170 was enhanced for BSF angry faces regardless of attention but was enhanced for LSF angry faces during passive viewing. These results suggest the involvement of a neural pathway reliant on LSF information at the N170 level. Taken together with previous reports from the literature, this may indicate the involvement of multiple parallel neural pathways during early visual processing of approaching emotional faces.

Endogenous attention modulates automaticity of number processing.

Numerals (i.e., symbolic representations of numerical magnitude) are widespread in our environment and are fundamental to many decisions we make. It has been suggested that the processing of numerical magnitude is automatic. Various robust psychological effects, such as the distance effect (Moyer & Landauer, Nature, 215 (5109), 1519-1520, 1967) and the physical size-congruity effect (SiCE; Henik & Tzelgov, Memory & Cognition, 10 (4), 389-395, 1982), support this claim. Importantly, these effects demonstrate that the processing of numerical magnitude occurs unintentionally and while irrelevant to the task. These aspects often serve as criteria to assess the automatic nature of mental processes. However, evidence for the involvement of attention in the processing of magnitude of numerals somewhat subverts the automaticity account that was originally put forward. To reconcile between evidence in support of the automaticity account and evidence that compromises this account, we drew on another account of automaticity. This account distinguishes between strongly automatic and partly automatic mental processes based on their susceptibility to attentional influences. In the current study, we manipulated endogenous attention while participants completed numerical and physical comparisons of numerals, separately. We observed modulations of the SiCE for physical comparisons but not for numerical comparisons of numerals. That is, the processing of numerical magnitude when irrelevant was subjected to attentional influences, but the processing of their physical magnitude (i.e., size) was not. Therefore, we concluded that processing the numerical magnitude is partly automatic, whereas processing their physical magnitude is strongly automatic.

A lateralized alpha-band marker of the interference of exogenous attention over endogenous attention.

Scientists differentiate top-down from bottom-up visuospatial attention processes. While bottom-up attention is rapidly engaged by emerging demands from the environment, top-down attention in contrast reflects slow voluntary shifts of spatial attention. Several lines of research substantiate the idea that top-down and bottom-up attentional processes involve distinct functional systems. An increasing number of studies, however, argue that both attention systems share brain processing resources. The current study examines how salient visual events that engage bottom-up processes interfere with top-down attentional processes. Using neurophysiological recordings and multivariate pattern classification techniques, the authors show that these patterns of interference occur within the alpha-band of neural activity (8-12Hz), which implies that bottom-up and top-down attention processes share this narrow-band frequency brain resource. The results further demonstrate that patterns of alpha-band activity explains, in part, the interference between top-down and bottom-up attention at the behavioral level.

Invited Session I: 30 years of normalization in the visual system: Testing and expanding the Reynolds & Heeger Normalization Model of Attention.

I present evidence supporting key predictions of the Reynolds-Heeger Normalization Model of Attention: 1) Both exogenous and endogenous covert spatial attention, can affect performance by contrast or response gain changes, depending on the stimulus size and the relative size of the attention field. 2) Feature-based attention improves performance, consistent with a change in response gain, when the featural extent of the attention field is small (low uncertainty) or large (high uncertainty) relative to the featural extent of the stimulus. 3) An expanded model of spatial resolution and attention that distinguishes between exogenous and endogenous attention, focusing on texture-based segmentation as a model system, which has revealed a dissociation between these types of attention across eccentricity. Our model emulates sensory encoding to segment figures from their background and predict performance. To explain attentional effects, exogenous and endogenous attention require separate operating regimes across spatial frequency. The model reproduces behavioral performance across several experiments and resolves three unexplained phenomena: 1) the parafoveal advantage in segmentation, 2) the uniform improvements across eccentricity by endogenous attention, and 3) the peripheral improvements and central impairments by exogenous attention. This model provides a generalizable framework for predicting effects of endogenous and exogenous attention on perception across the visual field.