Tracking the location of visuospatial attention in a contingent capture paradigm

Currently, there is considerable controversy regarding the degree to which top-down control can affect attentional capture by salient events. According to the contingent capture hypothesis, attentional capture by a salient stimulus is contingent on a match between the properties of the stimulus and top-down attentional control settings. In contrast, bottom-up saliency accounts argue that the initial capture of attention is determined solely by the relative salience of the stimulus, and the effect of top-down attentional control is limited to effects on the duration of attentional engagement on the capturing stimulus. In the present study, we tested these competing accounts by utilizing the N2pc event-related potential component to track the locus of attention during an attentional capture task. The results were completely consistent with the contingent capture hypothesis: An N2pc wave was elicited only by distractors that possessed the target-defining attribute. In a second experiment, we expanded upon this finding by exploring the effect of target-distractor similarity on the duration that attention dwells at the distractor location. In this experiment, only distractors possessing the target-defining attribute (color) captured visuospatial attention to their location and the N2pc increased in duration and in magnitude when the capture distractor also shared a second target attribute (category membership). Finally, in three additional control experiments, we replicated the finding of an N2pc generated by distractors, only if they shared the target-defining attribute. Thus, our results demonstrate that attentional control settings influence both which stimuli attract attention and to what extent they are processed.     

Attentional capture by salient distractors during visual search is determined by temporal task demands

The question whether attentional capture by salient but task-irrelevant visual stimuli is triggered in a bottom-up fashion or depends on top-down task settings is still unresolved. Strong support for bottom-up capture was obtained in the additional singleton task, in which search arrays were visible until response onset. Equally strong evidence for top-down control of attentional capture was obtained in spatial cueing experiments in which display durations were very brief. To demonstrate the critical role of temporal task demands on salience-driven attentional capture, we measured ERP indicators of capture by task-irrelevant color singletons in search arrays that could also contain a shape target. In Experiment 1, all displays were visible until response onset. In Experiment 2, display duration was limited to 200 msec. With long display durations, color singleton distractors elicited an N2pc component that was followed by a late Pd component, suggesting that they triggered attentional capture, which was later replaced by location-specific inhibition. When search arrays were visible for only 200 msec, the distractor-elicited N2pc was eliminated and was replaced by a Pd component in the same time range, indicative of rapid suppression of capture. Results show that attentional capture by salient distractors can be inhibited for short-duration search displays, in which it would interfere with target processing. They demonstrate that salience-driven capture is not a purely bottom-up phenomenon but is subject to top-down control.     

Involuntary attentional capture is determined by task set: evidence from event-related brain potentials

To find out whether attentional capture by irrelevant but salient visual objects is an exogenous bottom-up phenomenon, or can be modulated by current task set, two experiments were conducted where the N2pc component was measured as an electrophysiological marker of attentional selection in response to spatially uninformative color singleton cues that preceded target arrays. When observers had to report the orientation of a uniquely colored target bar among distractor bars (color task), behavioral spatial cueing effects were accompanied by an early cue-induced N2pc, indicative of rapid attentional capture by color singleton cues. In contrast, when they reported the orientation of target bars presented without distractors (onset task), no behavioral cueing effects were found and no early N2pc was triggered to physically identical cue arrays. Experiment 2 ruled out an alternative interpretation of these N2pc differences in terms of distractor inhibition. These results do not support previous claims that attentional capture is initially unaffected by top-down intention, and demonstrate the central role of task set in involuntary attentional orienting.     

Dissociable effects of bottom-up and top-down factors on the processing of unattended fearful faces

While the role of attention in determining the neural fate of unattended emotional items has been investigated in the past, it remains unclear whether bottom-up and top-down factors have differential effects in shaping responses evoked by such stimuli. To study the effects of bottom-up and top-down factors on the processing of neutral and fearful faces, we employed functional magnetic resonance imaging (fMRI) while participants performed attentional tasks that manipulated these factors. To probe the impact of top-down mechanisms on the processing of face distractors, target letters either had to be found among several distinct nontarget letters (attentional load condition) or among identical nontarget letters (baseline condition). To probe the impact of bottom-up factors, we decreased the salience of the targets by reducing their size and contrast relative to baseline (salience condition). Our findings revealed that bottom-up and top-down manipulations produced dissociable effects on amygdala and fusiform gyrus responses to fearful-face distractors when task difficulty was equated. When the attentional load of the main task was high, weaker responses were evoked by fearful-face distractors relative to baseline during the early trials. By contrast, decreasing target salience resulted in increased responses relative to baseline. The present findings suggest that responses evoked by unattended fearful faces are modulated by several factors, including attention and stimulus salience.     

The interactions of multisensory integration with endogenous and exogenous attention

Stimuli from multiple sensory organs can be integrated into a coherent representation through multiple phases of multisensory processing; this phenomenon is called multisensory integration. Multisensory integration can interact with attention. Here, we propose a framework in which attention modulates multisensory processing in both endogenous (goal-driven) and exogenous (stimulus-driven) ways. Moreover, multisensory integration exerts not only bottom-up but also top-down control over attention. Specifically, we propose the following: (1) endogenous attentional selectivity acts on multiple levels of multisensory processing to determine the extent to which simultaneous stimuli from different modalities can be integrated; (2) integrated multisensory events exert top-down control on attentional capture via multisensory search templates that are stored in the brain; (3) integrated multisensory events can capture attention efficiently, even in quite complex circumstances, due to their increased salience compared to unimodal events and can thus improve search accuracy; and (4) within a multisensory object, endogenous attention can spread from one modality to another in an exogenous manner.     

Attention-related networks in Alzheimer's disease: a resting functional MRI study

In addition to memory deficits, attentional impairment is a common manifestation of Alzheimer's disease (AD). The present study examines the abnormalities of attention-related functional networks in AD using resting functional MRI (fMRI) technique and evaluates the sensitivity and specificity of these networks as potential biomarkers compared with the default mode network (DMN). Group independent component analysis (Group ICA) was applied to fMRI data from 15 AD patients and 16 normal healthy elderly controls (NC) to derive the dorsal attention network (DAN) and the ventral attention network (VAN) which are respectively responsible for the endogenous attention orienting ("top-down") process and the exogenous attention re-orienting ("bottom-up") process. Receiver operating characteristic (ROC) curve analysis was performed for activity in core regions within each of these networks. Functional connectivity analysis revealed disrupted DAN and preserved (less impaired) VAN in AD patients compared with NC, which might indicate impairment of a "top-down" and intact "bottom-up" attentional processing mechanisms in AD. ROC curve analysis suggested that activity in the left intraparietal sulcus and left frontal eye field from DAN as well as the posterior cingulate cortex from the DMN could serve as sensitive and specific biomarkers distinguishing AD from NC.     

Identification of attention and cognitive control networks in a parametric auditory fMRI study

In the competition for limited processing resources, top-down attention and cognitive control processes are needed to separate relevant from irrelevant sensory information and to interact with the environment in a meaningful way. The demands for the recruitment of top-down control processes depend on the relative salience of the competing stimuli. In the present event-related functional magnetic resonance imaging (fMRI) study we investigated the dynamics of neuronal networks during varying degrees of top-down control demands. We tested 20 participants with a dichotic auditory discrimination task in which the relative perceptual salience of two simultaneously presented syllables was parametrically varied by manipulating the inter-aural intensity differences (IIDs) and instructing the subjects to selectively attend to either the louder or weaker of the two stimuli. A significant interaction of IID manipulation and attentional instruction was detected bilaterally in the inferior parietal lobe and pre-supplementary motor area, and in the precentral gyrus, anterior cingulate cortex, and inferior frontal gyrus of the right hemisphere. The post hoc analysis of the interaction pattern allowed for an assignment of these regions to either of two sets of regions which can be interpreted to constitute two different brain networks: a fronto-parietal attention control network, involved in the integration of saliency-based and instruction-based processing preferences, and a medial-lateral frontal cognitive control network, involved in the processing of the conflicts arising in the attempt to follow the attentional instruction in face of the varying inter-aural stimulus salience.     

Deconstructing the architecture of dorsal and ventral attention systems with dynamic causal modeling

Attentional orientation to a spatial cue and reorientation-after invalid cueing-are mediated by two distinct networks in the human brain. A bilateral dorsal frontoparietal network, comprising the intraparietal sulcus (IPS) and the frontal eye fields (FEF), controls the voluntary deployment of attention and may modulate visual cortex in preparation for upcoming stimulation. In contrast, reorienting attention to invalidly cued targets engages a right-lateralized ventral frontoparietal network comprising the temporoparietal junction (TPJ) and ventral frontal cortex. The present fMRI study investigated the functional architecture of these two attentional systems by characterizing effective connectivity during lateralized orienting and reorienting of attention, respectively. Subjects performed a modified version of Posner's location-cueing paradigm. Dynamic causal modeling (DCM) of regional responses in the dorsal and ventral network, identified in a conventional (SPM) whole-brain analysis, was used to compare different functional architectures. Bayesian model selection showed that top-down connections from left and right IPS to left and right visual cortex, respectively, were modulated by the direction of attention. Moreover, model evidence was highest for a model with directed influences from bilateral IPS to FEF, and reciprocal coupling between right and left FEF. Invalid cueing enhanced forward connections from visual areas to right TPJ, and directed influences from right TPJ to right IPS and IFG (inferior frontal gyrus). These findings shed further light on the functional organization of the dorsal and ventral attentional network and support a context-sensitive lateralization in the top-down (backward) mediation of attentional orienting and the bottom-up (forward) effects of invalid cueing.     

Trait anxiety modulates the neural efficiency of inhibitory control

An impairment of attentional control in the face of threat-related distracters is well established for high-anxious individuals. Beyond that, it has been hypothesized that high trait anxiety more generally impairs the neural efficiency of cognitive processes requiring attentional control-even in the absence of threat-related stimuli. Here, we use fMRI to show that trait anxiety indeed modulates brain activation and functional connectivities between task-relevant brain regions in an affectively neutral Stroop task. In high-anxious individuals, dorsolateral pFC showed stronger task-related activation and reduced coupling with posterior lateral frontal regions, dorsal ACC, and a word-sensitive area in the left fusiform gyrus. These results support the assumption that a general (i.e., not threat-specific) impairment of attentional control leads to reduced neural processing efficiency in anxious individuals. The increased dorsolateral pFC activation is interpreted as an attempt to compensate for suboptimal connectivity within the cortical network subserving task performance.     

An event-related fMRI study of exogenous orienting: supporting evidence for the cortical basis of inhibition of return?

This event-related fMRI experiment examined the neural substrates of exogenous visuospatial attention. Exogenous attention produces a biphasic response pattern denoted by facilitation at short cue-target intervals and inhibition of return (IOR) at longer intervals. Whereas the volitional orienting of attention has been well described in the literature, the neural systems that support exogenous facilitation and IOR in humans are relatively unknown. In direct comparisons to valid facilitation trials, valid IOR trials produced unique foci of activation in the right posterior parietal, superior temporal, middle temporal, middle occipital, anterior cingulate, and dorsal medial thalamic areas. Valid IOR trials also resulted in activation of motor exploratory and frontal areas previously associated with inhibition and oculomotor control. In contrast, invalid IOR compared to facilitation trials only activated anterior cortical structures. These results provide support for both attentional and oculomotor theories of IOR and suggest that IOR may be mediated by two networks. One network may mediate the inhibitory bias following an exogenous cue, whereas a separate network may be activated when a response must be made to stimuli that appear in inhibited locations of space.     

Dissociable neural mechanisms for encoding predictable and unpredictable events

Attention is a necessary condition for the formation of new episodic memories, yet little is known about how dissociable attentional mechanisms for "top-down" and "bottom-up" orienting contribute to encoding. Here, subjects performed an intentional encoding task in which to-be-learned items were interspersed with irrelevant stimuli such that subjects could anticipate the appearance of some study items but not others. Subjects were more likely to later remember stimuli whose appearance was predictable at encoding. Electroencephalographic data were acquired during the study phase of the experiment to assess how synchronous neural activity related to later memory for predictable stimuli (to which attention could be oriented in a top-down fashion) and unpredictable stimuli (which rely to a greater extent on bottom-up attentional orienting). Over left frontal regions, gamma-band activity (25-55 Hz) early (approximately 150 msec) in the epoch was a robust predictor of later memory for predictable items, consistent with an emerging view that links high-frequency neural synchrony to top-down attention. By contrast, later (approximately 400 msec) theta-band activity (4-8 Hz) over the left and midline frontal cortex predicted subsequent memory for unpredictable items, suggesting a role in bottom-up attentional orienting. These results reveal for the first time the contribution of dissociable attentional mechanisms to successful encoding and contribute to a growing literature dedicated to understanding the role of neural synchrony in cognition.     

Emotionally negative stimuli can overcome attentional deficits in patients with visuo-spatial hemineglect

Left unilateral spatial neglect resulting from right brain damage is characterized by loss of awareness for stimuli in the contralesional side of space, despite intact visual pathways. We examined using fMRI whether patients with neglect are more likely to consciously detect in the neglected hemifield, emotionally negative complex scenes rather than visually similar neutral pictures and if so, what neural mechanisms mediate this effect. Photographs of emotional and neutral scenes taken from the IAPS were presented in a divided visual field paradigm. As expected, the detection rate for emotional stimuli presented in the neglected field was higher than for neutral ones. Successful detection of emotional scenes as opposed to neutral stimuli in the left visual field (LVF) produced activations in the parahippocampal and anterior cingulate areas in the right hemisphere. Detection of emotional stimuli presented in the intact right visual field (RVF) activated a distributed network of structures in the left hemisphere, including anterior and posterior cingulate cortex, insula, as well as visual striate and extrastriate areas. LVF-RVF contrasts for emotional stimuli revealed activations in right and left attention related prefrontal areas whereas RVF-LVF comparison showed activations in the posterior cingulate and extrastriate visual cortex in the left hemisphere. An additional analysis contrasting detected vs. undetected emotional LVF stimuli showed involvement of left anterior cingulate, right frontal and extrastriate areas. We hypothesize that beneficial role of emotion in overcoming neglect is achieved by activation of frontal and limbic lobe networks, which provide a privileged access of emotional stimuli to attention by top-down modulation of processing in the higher-order extrastriate visual areas. Our results point to the importance of top-down regulatory role of the frontal attentional systems, which might enhance visual activations and lead to greater salience of emotional stimuli for perceptual awareness.     

Top-down and bottom-up attention to memory: a hypothesis (AtoM) on the role of the posterior parietal cortex in memory retrieval

Recent neuroimaging studies have implicated the posterior parietal cortex in episodic memory retrieval, but there is uncertainty about its specific role. Research in the attentional domain has shown that superior parietal lobe (SPL) regions along the intraparietal sulcus are implicated in the voluntary orienting of attention to relevant aspects of the environment, whereas inferior parietal lobe (IPL) regions at the temporo-parietal junction mediate the automatic allocation of attention to task-relevant information. Here we propose that the SPL and the IPL play conceptually similar roles in episodic memory retrieval. We hypothesize that the SPL allocates top-down attention to memory retrieval, whereas the IPL mediates the automatic, bottom-up attentional capture by retrieved memory contents. By reviewing the existing fMRI literature, we show that the posterior intraparietal sulcus of SPL is consistently active when the need for top-down assistance to memory retrieval is supposedly maximal, e.g., for memories retrieved with low vs. high confidence, for familiar vs. recollected memories, for recognition of high vs. low frequency words. On the other hand, the supramarginal gyrus of IPL is consistently active when the attentional capture by memory contents is supposedly maximal, i.e., for strong vs. weak memories, for vividly recollected vs. familiar memories, for memories retrieved with high vs. low confidence. We introduce a model of episodic memory retrieval that characterizes contributions of posterior parietal cortex.     

Electrocortical correlates of control of selective attention to spatial frequency

In the present study, we investigated control of selective attention to spatial frequency patterns, using a cueing paradigm. Subjects either used the instruction embedded in a word cue to prepare for the upcoming test stimulus (transient attention condition) or used the instruction they received before a block of trials (sustained reference condition), under completely similar stimulus conditions. The pattern of differential cue responses between these two conditions, reflecting top-down attentional control processes, was different between two groups of subjects, effectively canceling each other out. Despite comparable behavioral performance on both cues and targets, one group (n = 4) elicited a fronto-central-parietal positivity, starting 500 ms postcue over frontal and prefrontal areas, later including more central and posterior scalp sites, whereas another group (n = 8) started 400 ms postcue over central sites with a negativity, growing in strength over time and stabilizing over fronto-central sites. Only the group of eight subjects showed some evidence of occipital pretarget biasing activity. Independent of group, source modeling of the attentional control activity showed that attentional control was initiated in anterior, not posterior, parts of the brain. Furthermore, different underlying sources were found for both groups, in addition to signs of differential processing of target stimuli. Possible individual differences in attentional control ability and its relation to usage of different brain areas to deal with the task demands are discussed in more detail.     

Awareness-Dependent Normalization Framework of Visual Bottom-up Attention

Although bottom-up attention can improve visual performance with and without awareness to the exogenous cue, whether they are governed by a common neural computation remains unclear. Using a modified Posner paradigm with backward masking, we found that the cueing effect displayed a monotonic gradient profile (Gaussian-like), both with and without awareness, whose scope, however, was significantly wider with than without awareness. This awareness-dependent scope offered us a unique opportunity to change the relative size of the attention field to the stimulus, differentially modulating the gain of attentional selection, as proposed by the normalization model of attention. Therefore, for each human subject (male and female), the stimulus size was manipulated as their respective mean attention fields with and without awareness while stimulus contrast was varied in a spatial cueing task. By measuring the gain pattern of contrast-response functions on the spatial cueing effect derived by visible or invisible cues, we observed changes in the cueing effect consonant with changes in contrast gain for visible cues and response gain for invisible cues. Importantly, a complementary analysis confirmed that subjects'' awareness-dependent attention fields can be simulated by using the normalization model of attention. Together, our findings indicate an awareness-dependent normalization framework of visual bottom-up attention, placing a necessary constraint, namely, awareness, on our understanding of the neural computations underlying visual attention.SIGNIFICANCE STATEMENT Bottom-up attention is known to improve visual performance with and without awareness. We discovered that manipulating subjects'' awareness can modulate their attention fields of visual bottom-up attention, which offers a unique opportunity to regulate its normalization processes. On the one hand, by measuring the gain pattern of contrast-response functions on the spatial cueing effect derived by visible or invisible cues, we observed changes in the cueing effect consonant with changes in contrast gain for visible cues and response gain for invisible cues. On the other hand, by using the normalization model of attention, subjects'' awareness-dependent attention fields can be simulated successfully. Our study supports important predictions of the normalization model of visual bottom-up attention and further reveals its dependence on awareness.     

The neural correlates of attention orienting in visuospatial working memory for detecting feature and conjunction changes

The neural mechanisms of attentional orienting in visuospatial working memory for change detection were investigated. A spatial cue was provided with the onset time manipulated to allow more effective top-down control with an early cue than with a late cue. The change type was also manipulated so that accurate detection depended on color or the binding of color and location. The results showed that both the frontal and parietal regions subserved the change detection task without cueing. When data were collapsed over the two change types, early cueing increased activation in the right inferior frontal gyrus (IFG) and middle frontal gyrus (MFG) while late cueing increased activation in the right inferior parietal lobule (IPL) and temporoparietal junction (TPJ) as compared with the no-cue condition. The cue onset time led to different levels of enhancement in the frontal and posterior cortices related to top-down control and stimulus-driven orienting. For feature detection, early cueing increased activation in the right MFG and late cueing increased activation in the bilateral precuneus (PCu), right TPJ, and right cuneus. The neural correlates of conjunction detection involved the right PCu and cerebellum without cueing, were associated with the anterior MFG, left IFG, and the left STG with early cueing, and involved the right MFG, left IFG, and right IPL with late cueing. The left IFG was correlated with memory retrieval of the cued representation for conjunction detection, and the right posterior PCu was associated with maintenance and memory retrieval among competing stimuli.     

Neural correlates of top-down letter processing

This fMRI study investigated top-down letter processing with an illusory letter detection task. Participants responded whether one of a number of different possible letters was present in a very noisy image. After initial training that became increasingly difficult, they continued to detect letters even though the images consisted of pure noise, which eliminated contamination from strong bottom-up input. For illusory letter detection, greater fMRI activation was observed in several cortical regions. These regions included the precuneus, an area generally involved in top-down processing of objects, and the left superior parietal lobule, an area previously identified with the processing of valid letter and word stimuli. In addition, top-down letter detection also activated the left inferior frontal gyrus, an area that may be involved in the integration of general top-down processing and letter-specific bottom-up processing. These findings suggest that these regions may play a significant role in top-down as well as bottom-up processing of letters and words, and are likely to have reciprocal functional connections to more posterior regions in the word and letter processing network.     

Neural Basis of Visual Attentional Orienting in Childhood Autism Spectrum Disorders

We examined spontaneous attention orienting to visual salience in stimuli without social significance using a modified Dot-Probe task during functional magnetic resonance imaging in high-functioning preadolescent children with Autism Spectrum Disorder (ASD) and age- and IQ-matched control children. While the magnitude of attentional bias (faster response to probes in the location of solid color patch) to visually salient stimuli was similar in the groups, activation differences in frontal and temporoparietal regions suggested hyper-sensitivity to visual salience or to sameness in ASD children. Further, activation in a subset of those regions was associated with symptoms of restricted and repetitive behavior. Thus, atypicalities in response to visual properties of stimuli may drive attentional orienting problems associated with ASD.     

Attentional orienting induced by arrows and eye-gaze compared with an endogenous cue

Exogenous orienting has been widely studied by using peripheral cues whereas endogenous orienting has been studied with directional central cues. However, recent evidence has shown that centrally presented eye-gaze and arrows may produce an automatic rather than voluntary orienting of attention. Therefore, the aim of the present study was to investigate the behavioural and electrophysiological (event-related potentials-ERP) correlates of the attentional shift induced by arrows and eye-gaze. In order to have a control condition, we compared arrows and eye-gaze with a purely endogenous cue, i.e., a texture arbitrarily coding one direction. We analyzed the ERP components (P1, N1, P2a, P2p, P3) elicited by the cue stimuli and the early lateralised attentional effect (early directing attention negativity-EDAN). In addition, in order to investigate the topography of the neural mechanisms underlying the cortical activity in each cueing condition, we applied a temporal segmentation procedure. The results showed that the three cueing conditions induced a different strength of activation within the same cortical network. Occipito-parietal regions were involved in the early processing of visual information, followed by an involvement of frontal areas, likely implicated in learning associations. These data confirm the assumption that, in contrast to purely endogenous cues, arrows and eye-gaze induce a very fast attentional shift. However, the similarity of the ERP components and of the topographical cortical maps among conditions suggest that this early orienting of attention is more likely related to an overlearned association mechanism rather than to a real exogenous attentional process.     

Hemispheric differences in attentional orienting by social cues

Research points to a right hemisphere bias for processing social stimuli. Hemispheric specialization for attention shifts cued by social stimuli, however, has been rarely studied. We examined the capacity of each hemisphere to orient attention in response to social and nonsocial cues using a lateralized spatial cueing paradigm. We compared the up/down orienting effects of eye gaze cues, arrow cues, and peripheral cues (change in luminance). Results revealed similar cueing effects in each visual field for nonsocial cues, but asymmetric effects for social cues. At both short (150 ms) and long (950 ms) cue-target intervals, gaze cueing was significant in the LVF, but not in the RVF. Thus, there is a right hemisphere bias for attentional orienting cued by social stimuli, but not for attentional orienting cued by nonsocial stimuli. This supports a theory of a separate neural system for socially cued orienting of attention, as well as a theory of separate parallel and simultaneous neural systems for attention in the two cerebral hemispheres.