From learned value to sustained bias: how reward conditioning changes attentional priority.

Introduction: Attentional bias to reward-associated stimuli can occur even when it interferes with goal-driven behavior. One theory posits that dopaminergic signaling in the striatum during reward conditioning leads to changes in visual cortical and parietal representations of the stimulus used, and this, in turn, sustains attentional bias even when reward is discontinued. However, only a few studies have examined neural activity during both rewarded and unrewarded task phases. Methods: In the current study, participants first completed a reward-conditioning phase, during which responses to certain stimuli were associated with monetary reward. These stimuli were then included as non-predictive cues in a spatial cueing task. Participants underwent functional brain imaging during both task phases. Results: The results show that striatal activity during the learning phase predicted increased visual cortical and parietal activity and decreased ventro-medial prefrontal cortex activity in response to conditioned stimuli during the test. Striatal activity was also associated with anterior cingulate cortex activation when the reward-conditioned stimulus directed attention away from the target. Discussion: Our findings suggest that striatal activity during reward conditioning predicts the degree to which reward history biases attention through learning-induced changes in visual and parietal activities.

Mild traumatic brain injury history is associated with lower brain network resilience in soldiers.

Special Operations Forces combat soldiers sustain frequent blast and blunt neurotrauma, most often classified as mild traumatic brain injuries. Exposure to repetitive mild traumatic brain injuries is associated with persistent behavioural, cognitive, emotional and neurological symptoms later in life. Identifying neurophysiological changes associated with mild traumatic brain injury exposure, in the absence of present-day symptoms, is necessary for detecting future neurological risk. Advancements in graph theory and functional MRI have offered novel ways to analyse complex whole-brain network connectivity. Our purpose was to determine how mild traumatic brain injury history, lifetime incidence and recency affected whole-brain graph theoretical outcome measures. Healthy male Special Operations Forces combat soldiers (age = 33.2 ± 4.3 years) underwent multimodal neuroimaging at a biomedical research imaging centre using 3T Siemens Prisma or Biograph MRI scanners in this cross-sectional study. Anatomical and functional scans were preprocessed. The blood-oxygen-level-dependent signal was extracted from each functional MRI time series using the Big Brain 300 atlas. Correlations between atlas regions were calculated and Fisher z-transformed to generate subject-level correlation matrices. The Brain Connectivity Toolbox was used to obtain functional network measures for global efficiency (the average inverse shortest path length), local efficiency (the average global efficiency of each node and its neighbours), and assortativity coefficient (the correlation coefficient between the degrees of all nodes on two opposite ends of a link). General linear models were fit to compare mild traumatic brain injury lifetime incidence and recency. Nonparametric ANOVAs were used for tests on non-normally distributed data. Soldiers with a history of mild traumatic brain injury had significantly lower assortativity than those who did not self-report mild traumatic brain injury (t148 = 2.44, P = 0.016). The assortativity coefficient was significantly predicted by continuous mild traumatic brain injury lifetime incidence [F1,144 = 6.51, P = 0.012]. No differences were observed between recency groups, and no global or local efficiency differences were observed between mild traumatic brain injury history and lifetime incidence groups. Brain networks with greater assortativity have more resilient, interconnected hubs, while those with lower assortativity indicate widely distributed, vulnerable hubs. Greater lifetime mild traumatic brain injury incidence predicted lower assortativity in our study sample. Less resilient brain networks may represent a lack of physiological recovery in mild traumatic brain injury patients, who otherwise demonstrate clinical recovery, more vulnerability to future brain injury and increased risk for accelerated age-related neurodegenerative changes. Future longitudinal studies should investigate whether decreased brain network resilience may be a predictor for long-term neurological dysfunction.

Blind Subgrouping of Task-based fMRI.

Significant heterogeneity in network structures reflecting individuals' dynamic processes can exist within subgroups of people (e.g., diagnostic category, gender). This makes it difficult to make inferences regarding these predefined subgroups. For this reason, researchers sometimes wish to identify subsets of individuals who have similarities in their dynamic processes regardless of any predefined category. This requires unsupervised classification of individuals based on similarities in their dynamic processes, or equivalently, in this case, similarities in their network structures of edges. The present paper tests a recently developed algorithm, S-GIMME, that takes into account heterogeneity across individuals with the aim of providing subgroup membership and precise information about the specific network structures that differentiate subgroups. The algorithm has previously provided robust and accurate classification when evaluated with large-scale simulation studies but has not yet been validated on empirical data. Here, we investigate S-GIMME's ability to differentiate, in a purely data-driven manner, between brain states explicitly induced through different tasks in a new fMRI dataset. The results provide new evidence that the algorithm was able to resolve, in an unsupervised data-driven manner, the differences between different active brain states in empirical fMRI data to segregate individuals and arrive at subgroup-specific network structures of edges. The ability to arrive at subgroups that correspond to empirically designed fMRI task conditions, with no biasing or priors, suggests this data-driven approach can be a powerful addition to existing methods for unsupervised classification of individuals based on their dynamic processes.

Reward history impacts attentional orienting and inhibitory control on untrained tasks.

It has been robustly shown that stimuli with reward history receive attentional priority. However, the majority of this research tests reward history effects on attentional bias using similar tasks for both the reward learning phase and the unrewarded testing phase, which limits our understanding of how the effects of reward history generalize beyond the trained tasks and mental sets. Across two new experiments, the current study addresses these issues by first associating reward with a stimulus in a visual search paradigm, and then testing value-driven effects of that stimulus in untrained and unrewarded tasks, including a cueing paradigm, a go/no-go task, and a delay discounting task. Results of Experiment 1 demonstrate that history of reward association in a visual search task generalizes to value-driven attentional bias in a different attention paradigm (i.e., cueing), indicating these effects are indeed attributable to imbued value that can transfer to other tasks beyond that in which the reward was trained. The results of Experiment 2 demonstrate that in addition to eliciting attentional orienting on untrained tasks, reward history can lead to better inhibitory control in the go/no-go task. We find no evidence for reward history effects in the delay discounting task. Together, these experiments demonstrate that when the reward association task is in the attention domain, reward history modulates attentional priority, and this effect generalizes to untrained and unrewarded tasks that utilize both spatial and nonspatial attention.

Top-down versus bottom-up attention differentially modulate frontal-parietal connectivity.

The moment-to-moment focus of our mind's eye results from a complex interplay of voluntary and involuntary influences on attention. Previous neuroimaging studies suggest that the brain networks of voluntary versus involuntary attention can be segregated into a frontal-versus-parietal or a dorsal-versus-ventral partition-although recent work suggests that the dorsal network may be involved in both bottom-up and top-down attention. Research with nonhuman primates has provided evidence that a key distinction between top-down and bottom-up attention may be the direction of connectivity between frontal and parietal areas. Whereas typical fMRI connectivity analyses cannot disambiguate the direction of connections, dynamic causal modeling (DCM) can model directionality. Using DCM, we provide new evidence that directed connections within the dorsal attention network are differentially modulated for voluntary versus involuntary attention. These results suggest that the intraparietal sulcus exerts a baseline inhibitory effect on the frontal eye fields that is strengthened during exogenous orienting and attenuated during endogenous orienting. Furthermore, the attenuation from endogenous attention occurs even with salient peripheral cues when those cues are known to be counter predictive. Thus, directed connectivity between frontal and parietal regions of the dorsal attention network is highly influenced by the type of attention that is engaged.

Attentional Control and Executive Function.

The processes of attentional control and executive function are critical for navigating and operating efficiently in everyday life, and deficits in these core processes have serious consequences. Despite a long history of research into these topics, much is still unknown about the brain mechanisms supporting these processes. This special issue of Cognitive Neuroscience: Current Debates, Research & Reports presents nine new empirical papers investigating the dynamic neural mechanisms of attentional selection, working memory, and executive control. The papers in this special issue utilize electrophysiological and neuroimaging methods, along with advanced analysis techniques, to identify the neural substrates and dynamic mechanisms underlying the orienting and shifting of attention, as well as the representation and maintenance of information in working memory. These articles inform theories of attentional selection by providing a deeper understanding of social influences on the allocation of attention as well as illuminating the role of selection history in biasing neural activity and behavior. Finally, the research presented here has broader impacts on the field of cognitive neuroscience, as results from studies investigating the coupling between bands of oscillatory neural activity provide exciting new insights into the coordination between widespread brain networks.

Impaired conflict monitoring near the hands: Neurophysiological evidence.

Recent evidence suggests that hand-stimulus proximity enhances the visuo-motor Simon effect. The present study used event-related potentials (ERP) to examine the timing at which hand-stimulus proximity modulates the Simon effect. The results show that the P1 and N1 components were not modulated by hand-stimulus proximity, suggesting that early sensory processing is not altered by hand-stimulus proximity. However, the interference effect (the difference between incompatible versus compatible trials) on the N2 component was significantly attenuated near the hands compared to far from the hands, indicating that hand-stimulus proximity impairs conflict monitoring. We also found significant effects on a later component, as the P3 was reduced and had a shorter latency for the hand-proximal condition relative to the hand-distal condition. These new findings suggest that the critical stage at which hand-stimulus proximity affects cognitive processing lies past the early perceptual processing, acting instead on later stages of processing related to executive functioning.

Exogenous vs. endogenous attention: Shifting the balance of fronto-parietal activity.

Despite behavioral and electrophysiological evidence for dissociations between endogenous (voluntary) and exogenous (reflexive) attention, fMRI results have yet to consistently and clearly differentiate neural activation patterns between these two types of attention. This study specifically aimed to determine whether activity in the dorsal fronto-parietal network differed between endogenous and exogenous conditions. Participants performed a visual discrimination task in endogenous and exogenous attention conditions while undergoing fMRI scanning. Analyses revealed robust and bilateral activation throughout the dorsal fronto-parietal network for each condition, in line with many previous results. In order to investigate possible differences in the balance of neural activity within this network with greater sensitivity, a priori regions of interest (ROIs) were selected for analysis, centered on the frontal eye fields (FEF) and intraparietal sulcus (IPS) regions identified in previous studies. The results revealed a significant interaction between region, condition, and hemisphere. Specifically, in the left hemisphere, frontal areas were more active than parietal areas, but only during endogenous attention. Activity in the right hemisphere, in contrast, remained relatively consistent for these regions across conditions. Analysis of this activity over time indicates that this left-hemispheric regional imbalance is present within the FEF early, at 3-6.5 s post-stimulus presentation, whereas a regional imbalance in the exogenous condition is not evident until 6.5-8 s post-stimulus presentation. Overall, our results provide new evidence that although the dorsal fronto-parietal network is indeed associated with both types of attentional orienting, regions of the network are differentially engaged over time and across hemispheres depending on the type of attention.

Replication and innovation versus a perfect '.05'.

Slotnick (this issue) makes a strong case that any attempt to assess the reliabiltiy of statistical correction procedures should use truly random data. In addition, however, there is an important side effect of the over-reliance on any given threshold to determine the worth of an experiment. Placing too much faith in any method of correction obscures the point that replication across labs remains a most critical part of scientific study. Especially for expensive methods, such as fMRI, an overemphasis on increasingly conservative thresholds can negatively impact the potential for replication of studies and the pursuit and reporting of innovative results.

Introduction to special issue: Attention & Plasticity.

Mechanisms of attention are a prime target for investigating the plasticity of the adult brain, as these core mechanisms act at the intersection of top-down and bottom-up processing, and the wide variety of methods used in attention research can be utilized to elucidate the mechanisms of plasticity. This special issue of Cognitive Neuroscience presents three new empirical papers and a discussion paper with peer commentaries. In the first article, Voelker, Sheese, and colleagues investigate the influence of genetic variation on the effectiveness of attention training. Della Libera and colleagues then present a study investigating how individual differences in personality traits affect the acquisition of reward-based attention biases. In the final empirical paper, Hopfinger and colleagues present a transcranial stimulation study investigating the influence of different oscillatory stimulations on the efficiency of attentional reorienting. Finally, Voelker, Piscopo, and colleagues present a discussion paper in which they suggest that successful training of attention is linked to changes in the underlying white matter. The papers in this special issue present a sampling of the range of issues and methodologies being brought to bear to further our understanding of the malleability of the mechanisms of attention and of the plasticity of the brain.

Relation of higher-frequency oscillatory activity to white matter changes and to core mechanisms of attention.

Voelker et al. discuss the potentially critical role of white matter changes underlying the effects of training. In regard to the specific types of neural activities and processes related to these changes, the authors focus on theta rhythms and the speed of manual response times. However, white matter changes likely affect brain oscillatory activity at multiple frequencies, and recent findings suggest structural connections may be even more important for higher frequency functional connectivity. Furthermore, activity in the gamma frequency range has been implicated in basic mechanisms of attention, and changes in these core processes could underlie improvements across multiple tasks.

Differential effects of 10-Hz and 40-Hz transcranial alternating current stimulation (tACS) on endogenous versus exogenous attention.

Previous electrophysiological studies implicate both alpha (8-12 Hz) and gamma (>30 Hz) neural oscillations in the mechanisms of selective attention. Here, participants preformed two separate visual attention tasks, one endogenous and one exogenous, while transcranial alternating current stimulation (tACS), at 10 Hz, 40 Hz, or sham, was applied to the right parietal lobe. Our results provide new evidence for the roles of gamma and alpha oscillations in voluntary versus involuntary shifts of attention. Gamma (40 Hz) stimulation resulted in improved disengagement from invalidly cued targets in the endogenous attention task, whereas alpha stimulation (10 Hz) had no effect on endogenous attention, but increased the exogenous cuing effect. These findings agree with previous studies suggesting that right inferior parietal regions may be especially important for the disengagement of attention, and go further to provide details about the specific type of oscillatory neural activity within that brain region that is differentially involved in endogenous versus exogenous attention. Our results also have potential implications for the plasticity and training of attention systems.

The persistence of distraction: a study of attentional biases by fear, faces, and context.

Efficient processing of the visual world requires that distracting items be avoided, or at least rapidly disengaged from. The mechanisms by which highly salient, yet irrelevant, stimuli lead to distraction, however, are not well understood. Here, we utilized a particularly strong type of distractor--images of human faces--to investigate the mechanisms of distraction and the involuntarily biasing of attention. Across three experiments using a novel discrimination task, we provided new evidence that the robust distraction triggered by faces may not reflect enhanced attraction but, instead, may reflect an extended holding of attention. Specifically, the onset of a task-irrelevant distractor initially impaired target performance regardless of the identity of that distractor (fearful faces, neutral faces, or places). In contrast, an extended period of distraction was observed only when the distractor was a face. Our results thus demonstrate two distinct mechanisms contributing to distraction: an initial involuntary capture to any sudden event and a subsequent holding of attention to a potentially meaningful, yet task-irrelevant stimulus-in this case, a human face. Critically, the latter holding of attention by faces was not unique to fearful faces but also occurred for neutral faces. The present results dissociate attentional capture from hold in another way as well, since the capture occurred regardless of the nature of the distractors, but the extended holding of attention was dependent upon the ongoing distractor context.

ERPs reveal similar effects of social gaze orienting and voluntary attention, and distinguish each from reflexive attention.

Spatial attention can be reflexively captured by a physically salient stimulus, effortfully directed toward a relevant location, or involuntarily oriented in the direction of another person's gaze (i.e., social gaze orienting). Here, we used event-related potentials to compare the effects of these three types of orienting on multiple stages of subsequent target processing. Although gaze orienting has been associated more strongly with reflexive capture than with voluntary attention, the present data provide new evidence that the neural effects of social gaze orienting are markedly different from the effects of reflexive attentional capture by physically salient stimuli. Specifically, despite their similar behavioral effects, social gaze orienting and reflexive capture produce different effects on both early sensory processing (~120 ms; P1/N1 components) and later, higher-order processing (~300 ms; P3 component). In contrast, the effects of social gaze orienting were highly similar to those of voluntary orienting at these stages of target processing.

Magnocellular and parvocellular influences on reflexive attention.

Previous studies have provided conflicting evidence regarding whether the magnocellular (M) or parvocellular (P) visual pathway is primarily responsible for triggering involuntary orienting. Here, we used event-related potentials (ERPs) to provide new evidence that both the M and P pathways can trigger attentional capture and bias visual processing at multiple levels. Specifically, cued-location targets elicited enhanced activity, relative to uncued-location targets, at both early sensory processing levels (indexed by the P1 component) and later higher-order processing stages (as indexed by the P300 component). Furthermore, the present results show these effects of attentional capture were not contingent on the feature congruency between the cue and expected target, providing evidence that this biasing of visual processing was not dependant on top-down expectations or within-pathway priming.

Electrophysiological evidence of alcohol-related attentional bias in social drinkers low in alcohol sensitivity.

Low sensitivity to the acute effects of alcohol is a known risk factor for alcoholism. However, little is known concerning potential information-processing routes by which this risk factor might contribute to increased drinking. We tested the hypothesis that low-sensitivity (LS) participants would show biased attention to alcohol cues, compared with their high-sensitivity (HS) counterparts. Participants performed a task in which alcoholic and nonalcoholic beverage cues were presented bilaterally followed by a target that required categorization by color. Response times were faster for targets appearing in alcohol-cued than non-alcohol-cued locations for LS but not for HS participants. Event-related potential markers of early attention orienting (P1 amplitude) and subsequent attention reorienting (ipsilateral invalid negativity amplitude) indicated preferential selective attention to alcohol-cued locations among LS individuals. Controlling for recent drinking and family history of alcoholism did not affect these patterns, except that among HS participants, relatively heavy recent drinking was associated with difficulty reorienting attention away from alcohol-cued locations. These findings suggest a potential information-processing bias through which low sensitivity could lead to heavy alcohol involvement.

Endogenous saccade preparation does not produce inhibition of return: failure to replicate Rafal, Calabresi, Brennan, & Sciolto (1989).

Inhibition of Return (IOR, slower reaction times to previously cued or inspected locations) is observed both when eye movements are prohibited, and when the eyes move to the peripheral location and back to the centre before the target appears. It has been postulated that both effects are generated by a common mechanism, the activation of the oculomotor system. In strong support of this claim, IOR is not observed when attention is oriented endogenously and covertly, but it has been observed when eye movements are endogenously prepared, even when not executed. Here, we aimed to replicate and extend the finding that endogenous saccade preparation produces IOR. In five experiments using different paradigms, IOR was not observed when participants endogenously prepared an eye movement. These results lead us to conclude that endogenous saccade preparation is not sufficient to produce IOR.

Isolating the internal in endogenous attention.

Neuroimaging studies have provided evidence that a bilateral frontal-parietal network is involved in voluntary attentional control. However, because those studies used instructive cue stimuli, some of the activity may have been due to interactions between cue processing and voluntary orienting. Here, we show that self-initiated voluntary orienting, in the absence of any cue stimulus, evokes activity in this frontal-parietal network. In contrast to the typical symmetric activity observed with cued attentional shifts, self-initiated shifts showed a hemispheric asymmetry consistent with studies of unilateral neglect patients. Specifically, the right hemisphere was equally involved in orienting to either visual field, whereas the left hemisphere was biased toward the contralateral field. Our data show that the asymmetry of attentional control can be revealed in neuroimaging of healthy subjects, when voluntary orienting is effectively isolated.

Neural basis of visual distraction.

The ability to maintain focus and avoid distraction by goal-irrelevant stimuli is critical for performing many tasks and may be a key deficit in attention-related problems. Recent studies have demonstrated that irrelevant stimuli that are consciously perceived may be filtered out on a neural level and not cause the distraction triggered by subliminal stimuli. However, in everyday situations, suprathreshold stimuli often do capture attention, but the neural mechanisms by which some stimuli rapidly and automatically trigger distraction remain unknown. Here, we investigated the neural basis of distraction by utilizing a particularly strong form of distractor: the abrupt appearance of a new object. Our results revealed a competitive relation between brain regions coding the locations of the target and the distractor, with distractor processing increasing and target processing decreasing, but only when the distractor was a new object; an equivalent luminance change to an existing object neither generated distraction nor affected target processing. Results also revealed changes in neural activity in intraparietal sulcus (IPS) and temporo-parietal junction (TPJ) that were unique to the new object distractor condition. The strongest relations between behavioral distraction and neural activity were observed in these parietal regions. Furthermore, participants who were less susceptible to distraction showed a more consistent, albeit more moderate, level of activity in IPS and TPJ. The present results thus provide new evidence regarding the neural mechanisms underlying distraction and resistance to it.

Event-related potentials reveal temporal staging of dynamic facial expression and gaze shift effects on attentional orienting.

Multiple sources of information from the face guide attention during social interaction. The present study modified the Posner cueing paradigm to investigate how dynamic changes in emotional expression and eye gaze in faces affect the neural processing of subsequent target stimuli. Event-related potentials (ERPs) were recorded while participants viewed centrally presented face displays in which gaze direction (left, direct, right) and facial expression (fearful, neutral) covaried in a fully crossed design. Gaze direction was not predictive of peripheral target location. ERP analysis revealed several sequential effects, including: (1) an early enhancement of target processing following fearful faces (P1); (2) an interaction between expression and gaze (N1), with enhanced target processing following fearful faces with rightward gaze; and (3) an interaction between gaze and target location (P3), with enhanced processing for invalidly cued left visual field targets. Behaviorally, participants responded faster to targets following fearful faces and targets presented in the right visual field, in concordance with the P1 and N1 effects, respectively. The findings indicate that two nonverbal social cues-facial expression and gaze direction-modulate attentional orienting across different temporal stages of processing. Results have implications for understanding the mental chronometry of shared attention and social referencing.