Spatial Orienting Research Articles

Gaze-cueing requires intact face processing – Insights from acquired prosopagnosia

Gaze-cueing is the automatic spatial orienting of attention in the direction of perceived gaze. Participants respond faster to targets located at positions congruent with the direction of gaze, compared to incongruent ones (gaze cueing effect, GCE). However, it still remains unclear whether its occurrence depends on intact integration of information from the entire eye region or face, rather than simply the presence of the eyes per se. To address this question, we investigated the GCE in PS, an extensively studied case of pure acquired prosopagnosia. In our gaze-cueing paradigm, we manipulated the duration at which cues were presented (70ms vs. 400ms) and the availability of facial information (full-face vs. eyes-only). For 70ms cue duration, we found a context-dependent dissociation between PS and controls: PS showed a GCE for eyes-only stimuli, whereas controls showed a GCE only for full-face stimuli. For 400ms cue duration, PS showed gaze-cueing independently of stimulus context, whereas in healthy controls a GCE again emerged only for full-face stimuli. Our findings suggest that attentional deployment based on the gaze direction of briefly presented faces requires intact processing of facial information, which affords salience to the eye region.

Is Inhibition of Return Modulated by Involuntary Orienting of Spatial Attention: An ERP Study.

Inhibition of return (IOR) is a mechanism that indicates individuals’ faster responses or higher accuracy to targets appearing in the novel location relative to the cued location. According to the “reorienting hypothesis,” disengagement from the cued location is necessary for the generation of IOR. However, more and more studies have questioned this theory because of dissociation between voluntary or involuntary spatial orienting and the IOR effect. To further explore the “reorienting hypothesis” of IOR, the present experiment employed an atypical cue-target paradigm which combined a spatially non-predictive peripheral cue that was presumed to trigger IOR with a spatially non-predictive central cue that was used to reflexively trigger a shift of attention. The results showed that a significant IOR effect did not interact with automatic spatial orienting as measured in mean RTs and accuracy as well as the Nd component. These findings suggested that the IOR effect triggered by peripheral cue was independent of automatic orienting generated by a central cue. Therefore, the present study provided evidence from location task and neural aspects, which again challenged the “reorienting hypothesis” of IOR.

Differential white matter involvement associated with distinct visuospatial deficits after right hemisphere stroke

Visuospatial attention depends on the integration of multiple processes, and people with right hemisphere lesions after a stroke may exhibit severe or no visuospatial deficits. The anatomy of core components of visuospatial attention is an area of intense interest. Here we examine the relationship between the disruption of core components of attention and lesion distribution in a heterogeneous group (N = 70) of patients with right hemisphere strokes regardless of the presence of clinical neglect. Deficits of lateralized spatial orienting, measured as the difference in reaction times for responding to visual targets in the contralesional or ipsilesional visual field, and deficits in re-orienting attention, as measured by the difference in reaction times for invalidly versus validly cued targets, were measured using a computerized spatial orienting task. Both measures were related through logistic regression and a novel ridge regression method to anatomical damage measured with magnetic resonance imaging. While many regions were common to both deficit maps, a deficit in lateralized spatial orienting was more associated with lesions in the white matter underlying the posterior parietal cortex, and middle and inferior frontal gyri. A deficit in re-orienting of attention toward unattended locations was associated with lesions in the white matter of the posterior parietal cortex, insular cortex and less so with white matter involvement of the anterior frontal lobe. An hodological analysis also supports this partial dissociation between the white matter tracts that are damaged in lateralized spatial biases versus impaired re-orienting. Our results underscore that the integrity of fronto-parietal white matter tracts is crucial for visuospatial attention and that different attention components are mediated by partially distinct neuronal substrates.

Behavioral and neural correlates of disrupted orienting attention in posttraumatic stress disorder.

Prior work has revealed that posttraumatic stress disorder (PTSD) is associated with altered (a) attentional performance and (b) resting-state functional connectivity (rsFC) in brain networks linked to attention. Here, we sought to characterize and link these behavioral and brain-based alterations in the context of Posner and Peterson's tripartite model of attention. Male military veterans with PTSD (N = 49; all deployed to Iraq or Afghanistan) and healthy age-and-gender-matched community controls (N = 26) completed the Attention Network Task. A subset of these individuals (36 PTSD and 21 controls) also underwent functional magnetic resonance imaging (fMRI) to assess rsFC. The behavioral measures revealed that the PTSD group was impaired at disengaging spatial attention, relative to the control group. FMRI measures further revealed that, relative to the control group, the PTSD group exhibited greater rsFC between the salience network and (a) the default mode network, (b) the dorsal attention network, and (c) the ventral attention network. Moreover, problems with disengaging spatial attention increased the rsFC between the networks above in the control group, but not in the PTSD group. The present findings link PTSD to both altered orienting of spatial attention and altered relationships between spatial orienting and functional connectivity involving the salience network. Interventions that target orienting and disengaging spatial attention may be a new avenue for PTSD research.

Moderation of nicotine effects on covert orienting of attention tasks by poor placebo performance and cue validity

Introduction and rationaleGiven baseline-dependent effects of nicotine on other forms of attention, there is reason to believe that inconsistent findings for the effects of nicotine on attentional orienting may be partly due to individual differences in baseline (abstinence state) functioning. Individuals with low baseline attention may benefit more from nicotine replacement. MethodThe effects of nicotine as a function of baseline performance (bottom, middle, and top third of mean reaction times during placebo) were assessed in 52 habitual abstinent smokers (26 females/26 males) utilizing an arrow-cued covert orienting of attention task. ResultsCompared to a placebo patch, a 14mg nicotine patch produced faster overall reaction times (RTs). In addition, individuals with slower RTs during the placebo condition benefitted more from nicotine on cued trials than did those who had shorter (faster) RTs during placebo. Nicotine also enhanced the validity effect (shorter RTs to validly vs. invalidly cued targets), but this nicotine benefit did not differ as a function of overall placebo-baseline performance. ConclusionsThese findings support the view that nicotine enhances cued spatial attentional orienting in individuals who have slower RTs during placebo (nicotine-free) conditions; however, baseline-dependent effects may not generalize to all aspects of spatial attention. These findings are consistent with findings indicating that nicotine's effects vary as a function of task parameters rather than simple RT speeding or cognitive enhancement.

Competition between Visual Events Modulates the Influence of Salience during Free-Viewing of Naturalistic Videos.

In daily life the brain is exposed to a large amount of external signals that compete for processing resources. The attentional system can select relevant information based on many possible combinations of goal-directed and stimulus-driven control signals. Here, we investigate the behavioral and physiological effects of competition between distinctive visual events during free-viewing of naturalistic videos. Nineteen healthy subjects underwent functional magnetic resonance imaging (fMRI) while viewing short video-clips of everyday life situations, without any explicit goal-directed task. Each video contained either a single semantically-relevant event on the left or right side (Lat-trials), or multiple distinctive events in both hemifields (Multi-trials). For each video, we computed a salience index to quantify the lateralization bias due to stimulus-driven signals, and a gaze index (based on eye-tracking data) to quantify the efficacy of the stimuli in capturing attention to either side. Behaviorally, our results showed that stimulus-driven salience influenced spatial orienting only in presence of multiple competing events (Multi-trials). fMRI results showed that the processing of competing events engaged the ventral attention network, including the right temporoparietal junction (R TPJ) and the right inferior frontal cortex. Salience was found to modulate activity in the visual cortex, but only in the presence of competing events; while the orienting efficacy of Multi-trials affected activity in both the visual cortex and posterior parietal cortex (PPC). We conclude that in presence of multiple competing events, the ventral attention system detects semantically-relevant events, while regions of the dorsal system make use of saliency signals to select relevant locations and guide spatial orienting.

Ocular exposure to blue-enriched light has an asymmetric influence on neural activity and spatial attention

Brain networks subserving alertness in humans interact with those for spatial attention orienting. We employed blue-enriched light to directly manipulate alertness in healthy volunteers. We show for the first time that prior exposure to higher, relative to lower, intensities of blue-enriched light speeds response times to left, but not right, hemifield visual stimuli, via an asymmetric effect on right-hemisphere parieto-occipital α-power. Our data give rise to the tantalising possibility of light-based interventions for right hemisphere disorders of spatial attention.

The interplay of goal-driven and stimulus-driven influences on spatial orienting.

Search for a target stimulus among distractors is subject to both goal-driven and stimulus-driven influences. Variables that selectively modify these influences have shown strong interaction effects on saccade trajectories toward the target, suggesting the involvement of a shared spatial orienting mechanism. However, subsequent manual response times (RTs) have revealed additive effects, suggesting that different mechanisms are involved. In the present study, we tested the hypothesis that an interaction for RTs is obscured by preceding multisaccade trajectories, promoted by the continuous presence of distractors in the display. In two experiments, we compared a condition in which distractors were removed soon after the presentation of the search display to a standard condition in which distractors were not removed. The results showed additive goal-driven and stimulus-driven effects on RTs in the standard condition, but an interaction when distractors were removed. These findings support the view that both variables influence a shared spatial orienting mechanism.

Automaticity of phasic alertness: Evidence for a three-component model of visual cueing.

The automaticity of phasic alertness is investigated using the attention network test. Results show that the cueing effect from the alerting cue-double cue-is strongly enhanced by the task relevance of visual cues, as determined by the informativeness of the orienting cue-single cue-that is being mixed (80% vs. 50% valid in predicting where the target will appear). Counterintuitively, the cueing effect from the alerting cue can be negatively affected by its visibility, such that masking the cue from awareness can reveal a cueing effect that is otherwise absent when the cue is visible. Evidently, then, top-down influences-in the form of contextual relevance and cue awareness-can have opposite influences on the cueing effect from the alerting cue. These findings lead us to the view that a visual cue can engage three components of attention-orienting, alerting, and inhibition-to determine the behavioral cueing effect. We propose that phasic alertness, particularly in the form of specific response readiness, is regulated by both internal, top-down expectation and external, bottom-up stimulus properties. In contrast to some existing views, we advance the perspective that phasic alertness is strongly tied to temporal orienting, attentional capture, and spatial orienting. Finally, we discuss how translating attention research to clinical applications would benefit from an improved ability to measure attention. To this end, controlling the degree of intraindividual variability in the attentional components and improving the precision of the measurement tools may prove vital.

Attention-related EEG markers in adult ADHD

ADHD status affects both bottom-up sensory processing and top-down attentional selection, impairing professional and social functioning. The objective of the study was to investigate the functional mechanisms of attention deficits in adult ADHD by examining the electrophysiological activities associated with bottom-up attentional cueing (temporal and spatial orienting of attention) and top-down control (conflict resolution). Continuous EEG was recorded in 21 adult ADHD patients (40.05±9.5 years) and 20 healthy adults (25.5±4 years) during performance of the Attention Network Test (ANT). We examined the cue and target-related P1, N1 and P3 components as well as the contingent negative variation (CNV) developing between cue and target. Oscillatory responses were analyzed in the alpha (8–13Hz) and beta (14–19Hz) frequency bands. ADHD patients performed similarly to controls but showed reduced P3 amplitude, larger early CNV decrementing over time, reduced preparatory activation in both alpha and beta bands, as well as flattened target-related posterior alpha and beta responses. As compared to controls, the inverted CNV pattern suggested peculiar preparatory processing in ADHD patients. The singular pattern of target-related beta response indicated increased inhibitory processes in the case of easier task resolution and more generally, the lack of association between conflict resolution speed and beta activity supported alternative executive processing in ADHD patients. Overall, the reduced activation of the functional networks devoted to bottom-up and top-down attention suggests that adult ADHD patients engage reduced cortical resources in this composite task, compatible with the cortical hypoarousal model.

Eye Movements during Auditory Attention Predict Individual Differences in Dorsal Attention Network Activity.

The neural mechanisms supporting auditory attention are not fully understood. A dorsal frontoparietal network of brain regions is thought to mediate the spatial orienting of attention across all sensory modalities. Key parts of this network, the frontal eye fields (FEF) and the superior parietal lobes (SPL), contain retinotopic maps and elicit saccades when stimulated. This suggests that their recruitment during auditory attention might reflect crossmodal oculomotor processes; however this has not been confirmed experimentally. Here we investigate whether task-evoked eye movements during an auditory task can predict the magnitude of activity within the dorsal frontoparietal network. A spatial and non-spatial listening task was used with on-line eye-tracking and functional magnetic resonance imaging (fMRI). No visual stimuli or cues were used. The auditory task elicited systematic eye movements, with saccade rate and gaze position predicting attentional engagement and the cued sound location, respectively. Activity associated with these separate aspects of evoked eye-movements dissociated between the SPL and FEF. However these observed eye movements could not account for all the activation in the frontoparietal network. Our results suggest that the recruitment of the SPL and FEF during attentive listening reflects, at least partly, overt crossmodal oculomotor processes during non-visual attention. Further work is needed to establish whether the network’s remaining contribution to auditory attention is through covert crossmodal processes, or is directly involved in the manipulation of auditory information.

Functional connectivity between posterior hippocampus and retrosplenial complex predicts individual differences in navigational ability.

Individuals vary widely in their ability to orient and navigate within the environment. Previous neuroimaging research has shown that hippocampus (HC) and scene-responsive regions (retrosplenial complex [RSC] and parahippocampal gyrus/parahippocampal place area [PPA]) were crucial for spatial orienting and navigation. Resting-state functional connectivity and a self-reported questionnaire of navigational ability were used to examine the hypothesis that the pattern of reciprocal connections between these regions reflects individual differences in spatial navigation. It was found that the functional connectivity between the posterior HC and RSC was significantly higher in good than in poor navigators. These results confirmed the crucial role of hippocampal and extra-hippocampal regions in spatial navigation and provided new insight into how spontaneous brain activity may account for individual differences in spatial ability. © 2016 Wiley Periodicals, Inc.

Spatial Cognition: Grid Cells Support Imagined Navigation

Grid cells in the entorhinal cortex represent an animal's current location during navigation. A new study indicates that grid cells in humans also represent information about imagined movement and spatial orienting, suggesting that the entorhinal network has a flexible role in spatial representation.

1-Hz Repetitive Transcranial Magnetic Stimulation over the Posterior Parietal Cortex Modulates Spatial Attention

Lesion and neuroimaging studies have suggested that regions in the posterior parietal cortex (PPC) are involved in visual spatial attention. The aim of this study was to investigate the potential effects on spatial attention resulting from a transient parietal impairment induced by 1-Hz repetitive transcranial magnetic stimulation (rTMS). We examined 50 healthy subjects using the attention network test (ANT) after first applying rTMS to right or left PPC. The right parietal rTMS, but not left PPC rTMS, caused a significant slowing in the mean reaction time (RT) to target presentation following a spatial cue during the ANT test. There were no significant effects of rTMS on mean RT under the no-cue, center-cue, and double-cue conditions, or for each flanker type among the experimental groups. Moreover, after rTMS to the right PPC, test subjects displayed deficits in networks related to alerting and orienting, whereas they exhibited improvement following rTMS to the left PPC. These findings indicate that the right PPC serves an important function in spatial orienting and the alerting activities. We interpreted the enhancement in alerting and spatial orienting function following low-frequency rTMS of left PPC as reflecting a disinhibition of right PPC via an inter-hemispheric inhibition account.

Distinct Computational Principles Govern Multisensory Integration in Primary Sensory and Association Cortices

Human observers typically integrate sensory signals in a statistically optimal fashion into a coherent percept by weighting them in proportion to their reliabilities. An emerging debate in neuroscience is to which extent multisensory integration emerges already in primary sensory areas or is deferred to higher-order association areas. This fMRI study used multivariate pattern decoding to characterize the computational principles that define how auditory and visual signals are integrated into spatial representations across the cortical hierarchy. Our results reveal small multisensory influences that were limited to a spatial window of integration in primary sensory areas. By contrast, parietal cortices integrated signals weighted by their sensory reliabilities and task relevance in line with behavioral performance and principles of statistical optimality. Intriguingly, audiovisual integration in parietal cortices was attenuated for large spatial disparities when signals were unlikely to originate from a common source. Our results demonstrate that multisensory interactions in primary and association cortices are governed by distinct computational principles. In primary visual cortices, spatial disparity controlled the influence of non-visual signals on the formation of spatial representations, whereas in parietal cortices, it determined the influence of task-irrelevant signals. Critically, only parietal cortices integrated signals weighted by their bottom-up reliabilities and top-down task relevance into multisensory spatial priority maps to guide spatial orienting.

Memory-based attentional capture by colour and shape contents in visual working memory

ABSTRACTCurrent theories assume that there is substantial overlap between visual working memory (VWM) and visual attention functioning, such that active representations in VWM automatically act as an attentional set, resulting in attentional biases towards objects that match the mnemonic content. Most evidence for this comes from visual search tasks in which a distractor similar to the memory interferes with the detection of a simultaneous target. Here we provide additional evidence using one of the most popular paradigms in the literature for demonstrating an active attentional set: The contingent spatial orienting paradigm of Folk and colleagues. This paradigm allows memory-based attentional biases to be more directly attributed to spatial orienting. Experiment 1 demonstrated a memory-contingent spatial attention effect for colour but not for shape contents of VWM. Experiment 2 tested the hypothesis that the placeholders used for spatial cueing interfered with the shape processing, and showed that memory-based attentional capture for shape returned when placeholders were removed. The results of the present study are consistent with earlier findings from distractor interference paradigms, and provide additional evidence that biases in spatial orienting contribute to memory-based influences on attention.

Folate and long-chain polyunsaturated fatty acid supplementation during pregnancy has long-term effects on the attention system of 8.5-y-old offspring: a randomized controlled trial

During fetal and perinatal periods, many nutrients, such as long-chain polyunsaturated fatty acids [contained in fish oil (FO)] and folate, are important in achieving normal brain development. Several studies have shown the benefits of early nutrition on children's neurocognitive development. However, the evidence with regard to the attention system is scarce. The aim of this study was to analyze the long-term effects of FO, 5-methyltetrahydrofolate (5-MTHF), or FO+5-MTHF prenatal supplementation on attention networks. Participants were 136 children born to mothers from the NUHEAL (Nutraceuticals for a Healthy Life) project (randomly assigned to receive FO and/or 5-MTHF or placebo prenatal supplementation) who were recalled for a new examination 8.5 y later. The response conflict-resolution ability (using congruent and incongruent conditions)), alerting, and spatial orienting of attention were evaluated with behavioral measures (Attention Network Test), electroencephalography/event-related potentials (ERPs), and standardized low-resolution brain electromagnetic tomography (sLORETA). Children born to mothers supplemented with 5-MTHF alone solved the response conflict more quickly than did the placebo and the FO+5-MTHF groups (all P < 0.05). Differences between ERP amplitudes for the conflict conditions were also observed. sLORETA analysis showed higher activation of the right midcingulate cortex for the incongruent condition. In addition, a significant slowing down of response speed depending on the warning cue in the 5-MTHF and FO groups was observed. Folate supplementation during pregnancy, rather than FO or FO+5-MTHF supplementation, improves children's ability to solve response conflicts. This advantage seems to be based on the higher activation of the midcingulate cortex, indicating that early nutrition influences the functionality of specific brain areas involved in executive functions. This trial was registered at clinicaltrials.gov as NCT01180933.

Cue-locked lateralized components in a tactile spatial attention task: Evidence for a functional dissociation between ADAN and LSN.

ERP studies investigating the control processes responsible for spatial orienting in touch have consistently observed that the anterior directing attention negativity (ADAN) elicited by an attention-directing cue is followed by a sustained negativity contralateral to the cued hand. Recent evidence suggested that the later negativity, labeled late somatotopic negativity (LSN), might reflect distinct neurocognitive processes from those associated with the ADAN. To investigate the functional meaning of the ADAN and LSN components, we measured ERPs elicited by bilateral tactile cues indicating to covertly shift tactile attention to the left or right hand. Participants performed two spatial attention tasks that differed only for the difficulty of the target/nontarget discrimination at attended locations. The LSN but not the ADAN was sensitive to our experimental manipulation of task difficulty, suggesting that this component might reflect sensory-specific preparatory processes prior to a forthcoming tactile stimulus.

Effect of working memory load on electrophysiological markers of visuospatial orienting in a spatial cueing task simulating a traffic situation.

Visuospatial attentional orienting has typically been studied in abstract tasks with low ecological validity. However, real-life tasks such as driving require allocation of working memory (WM) resources to several subtasks over and above orienting in a complex sensory environment. The aims of this study were twofold: firstly, to establish whether electrophysiological signatures of attentional orienting commonly observed under simplified task conditions generalize to a more naturalistic task situation with realistic-looking stimuli, and, secondly, to assess how these signatures are affected by increased WM load under such conditions. Sixteen healthy participants performed a dual task consisting of a spatial cueing paradigm and a concurrent verbal memory task that simulated aspects of an actual traffic situation. Behaviorally, we observed a load-induced detriment of sensitivity to targets. In the EEG, we replicated orienting-related alpha lateralization, the lateralized ERPs ADAN, EDAN, and LDAP, and the P1-N1 attention effect. When WM load was high (i.e., WM resources were reduced), lateralization of oscillatory activity in the lower alpha band was delayed. In the ERPs, we found that ADAN was also delayed, while EDAN was absent. Later ERP correlates were unaffected by load. Our results show that the findings in highly controlled artificial tasks can be generalized to spatial orienting in ecologically more valid tasks, and further suggest that the initiation of spatial orienting is delayed when WM demands of an unrelated secondary task are high.

Attentional Network Differences Between Migraineurs and Non-migraine Controls: fMRI Evidence.

Migraine is a headache disorder characterized by sensitivity to light and sound. Recent research has revealed abnormal visual-spatial attention in migraineurs in between headache attacks. Here, we ask whether these attentional abnormalities can be attributed to specific regions of the known attentional network to help characterize the abnormalities in migraine. Specifically, the ventral frontoparietal network of attention is involved with assessing the behavioural relevance of unattended stimuli. Given the decreased suppression of unattended stimuli reported in migraineurs, we hypothesized that migraineurs would have abnormal processing in the ventral portion of the frontoparietal network of attention. To address this, we used functional magnetic resonance imaging to assess the attentional control networks during visual spatial-orienting tasks in migraineurs (N=16) as compared to non-migraine controls (N=16). We employed two visual orienting paradigms with target discrimination tasks: (1) voluntary orienting to central arrow cues, and (2) reflexive orienting to peripheral flash cues. While both groups showed activation in the key areas of attentional processing networks, migraineurs showed less activation than non-migraine controls in a key area of the ventral frontoparietal network of attention, the right temporal parietal junction (rTPJ), during both voluntary and reflexive visual spatial orienting. Given the role of rTPJ is to assess the visual environment for behaviorally relevant sensory stimuli outside the focus of attention and signal other attentional areas to reorient attention to behaviorally salient stimuli, our findings fit with previous research showing that migraineurs lack suppression of unattended events and have heightened orienting to sudden onset stimuli in peripheral locations.