Gambling against neglect: Unconscious spatial biases induced by reward reinforcement in healthy people and brain-damaged patients

Orienting attention in space recruits fronto-parietal networks whose damage results in unilateral spatial neglect. However, attention orienting may also be governed by emotional and motivational factors; but it remains unknown whether these factors act through a modulation of the fronto-parietal attentional systems or distinct neural pathways. Here we asked whether attentional orienting is affected by learning about the reward value of targets in a visual search task, in a spatially specific manner, and whether these effects are preserved in right-brain damaged patients with left spatial neglect. We found that associating rewards with left-sided (but not right-sided) targets during search led to progressive exploration biases towards left space, in both healthy people and neglect patients. Such spatially specific biases occurred even without any conscious awareness of the asymmetric reward contingencies. These results show that reward-induced modulations of space representation are preserved despite a dysfunction of fronto-parietal networks associated with neglect, and therefore suggest that they may arise through spared subcortical networks directly acting on sensory processing and/or oculomotor circuits. These effects could be usefully exploited for potentiating rehabilitation strategies in neglect patients.     

Orienting of attention in left unilateral neglect

After right posterior brain damage, patients may ignore events occurring on their left, a condition known as unilateral neglect. Although deficits at different levels of impairment may be at work in different patients, the frequency and severity of attentional problems in neglect patients have been repeatedly underlined. Recent advances in the knowledge of the mechanisms of spatial attention in normals may help characterizing these deficits. The present review focuses on studies exploring several aspect of attentional processing in unilateral neglect, with particular reference to the dichotomy between 'exogenous', or stimulus-related, and 'endogenous', or strategy-driven, orienting of attention. A large amount of neuropsychological evidence suggests that a basic mechanism leading to left neglect behavior is an impaired exogenous orienting toward left-sided targets. In contrast, endogenous processes seem to be relatively preserved, if slowed, in left unilateral neglect. Other component deficits, such as a general slowing of the operations of spatial attention, might contribute to neglect behavior. These results are presented and discussed, and their implications for hemispheric specialization in attentional orienting and for the mechanisms of visual consciousness are explored.     

How does phasic alerting improve performance in patients with unilateral neglect? A systematic analysis of attentional processing capacity and spatial weighting mechanisms

In visual hemi-neglect, non-spatial deficits such as reduced intrinsic alertness can significantly modulate the degree of left visual field inattention. However, to date, the precise mechanisms mediating this effect are hardly understood. In the present study, we assessed the influence of increased alertness on both general attentional capacity (perceptual processing speed) and spatial attentional selection processes (spatial distribution of attentional weighting). For this purpose, a whole-report paradigm based on Bundesen's 'theory of visual attention' (TVA) was combined with a non-spatial, visual alerting cue. Three different cue-target stimulus onset asynchronies (SOAs; of 80, 200, and 650 ms), allowed us to observe the time course of the alerting-cue effects. A group of six patients with visual hemi-neglect was examined and their performance compared with six healthy control subjects matched for age, gender, and education. In neglect patients, the alerting cue evoked a phasic increase of perceptual processing speed. However, this effect was mainly found in the ipsilateral, i.e. in the "preserved" hemifield. Importantly, however, patients displayed a fast-evolving and short-lasting, phasic modulation of spatial attentional weighting, with a re-distribution of attentional weights from the pathological rightward bias to a normal, more balanced distribution of visual attention. In control participants, the cueing effects on perceptual processing speed and spatial weighting were generally less pronounced than in neglect patients. Replicating results of a prior study, cueing induced a stable, slightly leftward, distribution of attentional weights, whilst in the no-cue condition, a temporary rightward shift of attentional weights was found. This pattern of effects suggests a close interaction between alertness and spatial-attentional weighting in the syndrome of visual hemi-neglect. It supports the hypothesis that the manifestation of spatial neglect involves at least in part intrinsic alertness deficits. It also provides clues to a more detailed account of the mechanisms responsible for alleviating neglect in patients following manipulations of the alertness level, both in the short (cueing) and in the long term (alertness training).     

A demonstration of endogenous modulation of unilateral spatial neglect: the impact of apparent time-pressure on spatial bias.

Unilateral neglect, a lack of awareness for one side of space, is a common and debilitating consequence of stroke. Previous work has identified a relationship between enduring left neglect and diminished general alertness and shown that increasing alertness can temporarily reduce the severity of the spatial bias. In that research, alertness was modulated by loud tones or with pharmacological stimulants. Here we examine whether cognitive, endogenously driven changes can produce similar short-term improvements. Time-pressure is associated with increased subjective arousal and increased activation in cortical regions associated with alertness. Here five patients completed a spatial cancellation task with and without instructions regarding a time limit. Significant reductions in neglect severity were observed when patients believed that they were acting under time-pressure, despite the conditions being equivalent in the actual (unlimited) time available. Functional imaging work has highlighted the secondary effects that damage to networks mediating alertness can have on structurally intact spatial systems. The results here suggest that activation of presumably spared function in these damaged networks can induce moment-by-moment changes in spatial function and, crucially, that this can be achieved using entirely endogenous means.     

Revisiting unilateral neglect

Unilateral neglect, a neurological disorder in which patients fail to detect or respond to contralesional stimuli, has long been considered a failure of attentional orienting mechanisms. This review provides a selective overview of the prominent biases in spatial orienting and exploratory motor behaviour observed in these patients before considering the impact of other factors on the presentation of the disorder and how those factors might inform current neurological models of neglect. In the latter part of the review, we intend to suggest that neglect is likely to be a combination of distinct but interacting impairments including biases in attentional orienting, exploratory motor behaviours and a deficit of spatial working memory. That is, we suggest that the cardinal symptom of neglect - a loss of awareness for contralesional stimuli and events - arises as a result of a combination of these impairments rather than being associated solely with the more dramatic and immediately evident biases in spatial attention.     

Integrating conflict detection and attentional control mechanisms

Human behavior involves monitoring and adjusting performance to meet established goals. Performance-monitoring systems that act by detecting conflict in stimulus and response processing have been hypothesized to influence cortical control systems to adjust and improve performance. Here we used fMRI to investigate the neural mechanisms of conflict monitoring and resolution during voluntary spatial attention. We tested the hypothesis that the ACC would be sensitive to conflict during attentional orienting and influence activity in the frontoparietal attentional control network that selectively modulates visual information processing. We found that activity in ACC increased monotonically with increasing attentional conflict. This increased conflict detection activity was correlated with both increased activity in the attentional control network and improved speed and accuracy from one trial to the next. These results establish a long hypothesized interaction between conflict detection systems and neural systems supporting voluntary control of visual attention.     

Modulation of non-spatial attention and the global/local processing bias

Amelioration of the rightward spatial attention bias in patients with hemispatial neglect following manipulations of non-spatial attention suggests that spatial attention and mechanisms related to the regulation of attention are interrelated. Studies in normal, healthy subjects have shown similar modulation in spatial bias following tonic and phasic changes in attention suggesting that this interaction is a general mechanism of attention rather than a curiosity of the neglect disorder. The current study examined this attentional interaction to determine if perceptual processes favoring one hemisphere over the other are affected by this relationship. Participants first made rapid discriminations of Navon figures presented at central fixation. As expected, when participants attended to either the local or global dimension, incongruence in the orthogonal dimension resulted in longer reaction times for accurate discrimination compared to congruent trials. However, following a brief (16-min) continuous performance task designed to elicit behaviors associated with greater tonic and phasic alertness, participants showed significantly less local interference when attending the global dimension and more global interference when attending the local dimension on the Navon discrimination task compared to a control task condition. The results indicate that exercising tonic and phasic alertness produces a global processing bias.     

Conflict control processing in adults with developmental dyslexia: An event related potentials study

ObjectiveThe present study investigated the time course for processing conflict in dyslexic adults using a flanker task.MethodsSixteen dyslexic and 15 control adults performed a flanker task comprising congruent and incongruent trials in which participants had to indicate the direction of targets surrounded by flankers. Early negative potentials associated with orienting of attention (i.e., N1) and conflict monitoring (i.e., N2) and two positive potentials associated with conflict resolution (i.e., P3b and Nogo P3) were recorded.ResultsThe behavioral data showed differences between incongruent and congruent trials for reaction times in both groups but for error rate only in dyslexics. As in previous studies, controls displayed greater N1, N2 and NoGo P3 as well as a smaller P3b in incongruent trials. Dyslexics lacked N1, N2 and P3b modulation whereas NoGo P3 effect was preserved.ConclusionDyslexics showed impairments in conflict monitoring and in some aspects of conflict resolution (i.e., the allocation of attentional resources) whereas other aspects of conflict resolution (i.e., the inhibition) were preserved.SignificanceThis is the first study to investigate conflict control processing in dyslexic adults using ERPs. Results provide evidence for deficits in orienting of attention, conflict monitoring and allocation of attentional resources in dyslexics.     

Development of attentional networks in childhood

Recent research in attention has involved three networks of anatomical areas that carry out the functions of orienting, alerting and executive control (including conflict monitoring). There have been extensive cognitive and neuroimaging studies of these networks in adults. We developed an integrated Attention Network Test (ANT) to measure the efficiency of the three networks with adults. We have now adapted this test to study the development of these networks during childhood. The test is a child-friendly version of the flanker task with alerting and orienting cues. We studied the development of the attentional networks in a cross-sectional experiment with four age groups ranging from 6 through 9 (Experiment 1). In a second experiment, we compared children (age 10 years) and adult performance in both child and adults versions of the ANT. Reaction time and accuracy improved at each age interval and positive values were found for the average efficiency of each of the networks. Alertness showed evidence of change up to and beyond age 10, while conflict scores appear stable after age seven and orienting scores do not change in the age range studied. A final experiment with forty 7-year-old children suggested that children like adults showed independence between the three networks under some conditions.     

Rightward shift in spatial awareness with declining alertness

Although transient neglect of contralesional space occurs following damage to either hemisphere, persistent forms are overwhelmingly associated with right hemisphere lesions. This has led to the suggestion that impairments in other right hemisphere systems--in particular those that mediate alertness--may undermine recovery. Reductions in neglect severity with stimulation, exacerbation with sedatives and the poor performance of chronic neglect patients on sustained attention tasks are consistent with this view. However, the question of whether changes in alertness exert a specific influence over spatial attention--or simply improve performance across many domains--is difficult to address using only patient studies. Here, we examine this question with individuals from the healthy adult population. On certain spatial tasks, adults show a modest but reliable leftward attentional bias. On the basis of the neglect studies, we hypothesised that this bias would diminish--or even reverse--as alertness levels declined. In the first study, participants were asked to judge the relative lengths of the left and right sections of a line when sleep deprived and when well rested. A significant rightward shift in attention was associated with sleep deprivation. A rightward shift was also observed over the course of the session. The second study replicated this time-on-task effect. The results suggest that a diminution in alertness may be sufficient to induce a rightward shift in visual attention in the healthy brain. Implications for the persistence of neglect in patients, for spatial biases in children and for normal free viewing asymmetries are discussed.     

Attentional deficit in dyslexia: a general or specific impairment?

Dyslexic and control children were tested in a visuomotor attentional task, which provides independent measures of the alerting, orienting and conflict components of the attentional system. Our results show that dyslexics are impaired with respect to controls in the attentional conflict component (resolution of conflict of incongruent peripheral information), while the alerting and orienting components remain preserved. It excludes an overall attentional impairment and points to more specific attentional processing difficulty i.e. distributed attention strategy. Generally, results of dyslexic boys are within the range of the control group, while reaction times of dyslexic girls are significantly slower than that of all other groups.     

Redes neurales atencionales en enfermedades neurodegenerativas: evidencias anatómico-funcionales empleando el Attention Network Test

IntroductionUnderstanding alterations to brain anatomy and cognitive function associated with neurodegenerative diseases remains a challenge for neuroscience today. In experimental neuroscience, several computerised tests have been developed to contribute to our understanding of neural networks involved in cognition. The Attention Network Test (ANT) enables us to measure the activity of 3 attentional networks (alertness, orienting, and executive function).ObjectivesThe main aim of this review is to describe all the anatomical and functional alterations found in diverse neurological diseases using the ANT.Material and methodsWe collected studies published since 2010 in the PubMed database that employed the ANT in different neurological diseases. Thirty-two articles were obtained, addressing multiple sclerosis, epilepsy, and Parkinson's disease, among other disorders.ConclusionsSome of the anatomical structures proposed in the 3 attentional networks model were confirmed. The most relevant structures in the alertness network are the prefrontal cortex, parietal region, thalamus, and cerebellum. The thalamus is also relevant in the orienting network, together with posterior parietal regions. The executive network does not depend exclusively on the prefrontal cortex and anterior cingulate cortex, but also involves such subcortical structures as the basal ganglia and cerebellum and their projections towards the entire cortex.     

Attentional network task performance in patients with schizophrenia-spectrum disorders: evidence of a specific deficit

Although attentional deficits are frequently displayed by schizophrenia and spectrum patients, the precise nature of the impairment is unclear. The present study investigates attentional performance in 26 schizophrenia-spectrum outpatients and 24 healthy controls using the Attentional Network Task (ANT). We assessed the efficiency of the segregated alerting, orienting, and executive control networks by measuring how response latencies were influenced by alerting cues, spatial cues, and flanking stimuli. In overall ANOVAs we found main effects of cue condition and flanker congruency. The data also revealed a significant interaction of group and flanker type, with schizophrenia-spectrum patients taking longer on average to resolve conflict. These results suggest that compared to the healthy nonpatients, schizophrenia-spectrum patients show a deficit in their executive control network. Considered together, these findings support the notion that schizophrenia-spectrum patients have a specific attentional deficit, rather than a global one. The significance of these findings is considered from both experimental and clinical perspectives.     

Ipsilesional 'where' with contralesional 'what' neglect

Whereas contralesional spatial neglect is usually caused by right temporo-parietal lesions, ipsilesional spatial neglect is induced primarily by right frontal lesions. This report describes a 73-year-old woman with a right inferior parietal lesion who on 'where' tasks (line bisection and midline pointing) demonstrated ipsilesional neglect, but on 'what' tests (gap vs. no-gap detection cancellation and clothing tape removal) demonstrated contralesional neglect. This 'what' and 'where' directional dissociation provides evidence for independent 'what' and 'where' attentional networks; however, the reason this parietal lesion causes this contralesional vs. ipsilesional spatial attentional 'what' and 'where' dichotomy remains to be determined.     

Orienting attention to instants in time

My colleagues and I have investigated whether the temporal framework can be used to guide selective attention, and have applied non-invasive methodology to reveal the brain systems and mechanisms involved. Our findings show that we are able to orient attention selectively to different points in time, enhancing behavioral performance. These effects are mediated by a left-hemisphere dominant parietal-frontal system, which partially overlaps with the networks involved in spatial orienting. The neural system for temporal orienting also includes brain areas associated with motor preparation and anticipation, suggesting that sensorimotor areas with different specializations can contribute to attentional orienting depending on the stimulus attributes guiding selection. The optimization of behavior by temporal orienting involves enhancement of the latency and amplitude of event-related potentials that are associated with motor responses and decisions. The effects are distinct from those during visual spatial attention, indicating that behavioral advantages can be conferred by multiple types of neural mechanisms. Taken together, the findings illustrate the flexibility of attentional functions in the human brain.     

Right hemispatial ipsilesional neglect with chronic right hemisphere strokes

Background: Patients who present with spatial neglect after stroke often perform normally on tests for neglect after a few weeks. Whereas tests for neglect are often performed directly in front of a patient, in their actual environments many important stimuli may be present within their left or right hemispace. The presence and severity of neglect often depends on the hemisphere injured. It is possible, in chronic stroke, for spatial judgments to be influenced by an interaction of stroke laterality and the spatial location of stimuli. The objective of this study was to learn if unilateral hemispheric chronic strokes contribute to a spatial bias with laterally presented stimuli.

Method: There were 70 participants, 62 with unilateral chronic strokes (>6 months post onset) including 35 with left hemisphere damage (LHD), 27 with right hemisphere damage (RHD), and 8 demographically similar people without history of stroke. Participants were asked to bisect 300 lines presented with distractors on the left, right, or both sides of the line, or no distractor, on a touch-screen monitor in right, center or left hemispace.

Results: There was a significant interaction between the side of the hemispheric lesion and the side of the body where these lines were presented. Specifically, in right space, patients with RHD deviated leftward in comparison to the other groups. Furthermore, there was an interaction between group and distractor induced bias. All three groups approached the left distractor, and the patients with LHD also approached the right distractor.

Conclusions: Although spatial neglect is more severe in contralesional than ipsilesional hemispace in the period immediately following a stroke, over time patients with RHD may develop ipsilesional neglect that is more severe in ipsilesional than contralesional space. The mechanism underlying this bias is not known and may be related to attempted compensation or the development of a contralateral attentional/intentional grasp.     

Testing the efficiency and independence of attentional networks

In recent years, three attentional networks have been defined in anatomical and functional terms. These functions involve alerting, orienting, and executive attention. Reaction time measures can be used to quantify the processing efficiency within each of these three networks. The Attention Network Test (ANT) is designed to evaluate alerting, orienting, and executive attention within a single 30-min testing session that can be easily performed by children, patients, and monkeys. A study with 40 normal adult subjects indicates that the ANT produces reliable single subject estimates of alerting, orienting, and executive function, and further suggests that the efficiencies of these three networks are uncorrelated. There are, however, some interactions in which alerting and orienting can modulate the degree of interference from flankers. This procedure may prove to be convenient and useful in evaluating attentional abnormalities associated with cases of brain injury, stroke, schizophrenia, and attention-deficit disorder. The ANT may also serve as an activation task for neuroimaging studies and as a phenotype for the study of the influence of genes on attentional networks.     

Cognitive rehabilitation for unilateral neglect: Review

Unilateral spatial neglect, a striking difficulty in paying attention to one side of space, is a common consequence of cerebro-vascular disease. Although most patients appear to recover from this deficit relatively quickly, chronic forms of the disorder—usually resulting from right hemisphere damage and affecting left space—are associated with slowed motor recovery, poor response to rehabilitation, and difficulties in many everyday activities. This article reviews the theoretical underpinnings and efficacy of rehabilitation techniques including; behavioural training in leftward visual scanning, eye-patching, encouraging movement of the left limbs, and interventions designed to increase general alertness. Recent highly positive results from brief adaptation training with prism lenses are discussed. “Neglect” is a heterogeneous cluster of deficits that can arise following damage to a variety of brain structures. It is not yet clear whether one rehabilitation technique will be appropriate for all patients/manifestations of the disorder, or whether combining different interventions may produce additive benefits. There is growing evidence that chronic neglect is associated with—indeed possibly fostered by—limitations in a number of non-spatial attentional capacities. Whether reduction of the spatial bias is sufficient, in itself, to improve overall outcome for patients remains an open question.     

Distinct neural correlates for resolving stroop conflict at inhibited and noninhibited locations in inhibition of return

It is well documented that the anterior cingulate cortex (ACC) and the dorsolateral prefrontal cortex (DLPFC) are intensively involved in conflict control. However, it remains unclear how these "executive" brain regions will act when the conflict control process interacts with spatial attentional orienting. In the classical spatial cueing paradigm [Posner, M. I., & Cohen, Y. (1984). Components of visual orienting. In H. Bouma & D. G. Bouwhuis (Eds.), Attention and performance X (pp. 531-556). Hillsdale, NJ: Erlbaum], response to a target is delayed when it appears at the cued location compared with at the uncued location, if the time interval between the cue and the target is greater than 300 msec. This effect of inhibition of return (IOR) can alter the resolution of Stroop conflict such that the Stroop interference effect disappears at the cued (inhibited) location [Vivas, A. B., & Fuentes, L. J. Stroop interference is affected in inhibition of return. Psychonomic Bulletin and Review, 8, 315-323, 2001]. In this event-related functional magnetic resonance study, we investigate the differential neural mechanisms underlying interactions between pre-response interference, response interference, and spatial orienting. Two types of Stroop words [incongruent response-eligible words (IE), incongruent response-ineligible words (II)] and neutral words were presented either at the cued or uncued location. The significant pre-response interference at the uncued location activated the left rostral ACC as compared with at the cued location. Moreover, although the IE words which have conflicts at both pre-response and response levels did not cause significant behavioral interference at the cued location, they activated the left DLPFC as compared with at the uncued location. Furthermore, neutral words showed significant IOR effects behaviorally, and they activated the left frontal eye field (FEF) at the uncued location relative to the cued location. These results suggest that the left rostral ACC is involved in the interaction between pre-response conflict and IOR, whereas the left DLPFC is involved in the interaction between response conflict and IOR. Moreover, the FEF is involved in shifting attentional focus to novel locations during spatial search.     

Early rightwards orienting of attention on simple reaction time performance in patients with left-sided neglect.

A specific disruption in the ability to automatically disengage attention from its previous focus has been hypothesized to account for the extinction phenomenon often observed in the unilateral spatial neglect syndrome. Recent literature, however, also brings out the role played in neglect by an imbalance in the attentional orienting systems, resulting in an early shift of attention towards the side of space ipsilateral to the brain lesion. In the present study we hypothesized that this attentional bias in orienting of attention might be demonstrated in a paradigm of simple reaction time to lateralized visual stimuli by contrasting the presence vs the absence on the computer screen of the square boxes used to facilitate position expectancy. A main prediction was made that patients with neglect would show a significant increase in reaction time to contralateral visual stimuli in the presence of bilateral reference boxes as compared to conditions in which no boxes were displayed. The right-sided box was in fact expected to exert an early attraction on the patient's attention, thus modifying the pattern of reaction times to the proper targets. This prediction was confirmed in right brain-damaged patients with moderate to severe neglect.