Attention scaling modulates the effective capacity of visual sensory memory.

Visual sensory memory (VSM) has a high capacity, but its contents are fleeting. Recent evidence that the breadth of attention strongly influences the efficiency of visual processing suggests that it might also modulate the effective capacity of VSM. We manipulated the breadth of attention with different cue sizes and used the partial-report technique to estimate the capacity of VSM. Whether attention was deployed voluntarily or captured by a salient cue, narrowly focused attention increased the effective capacity of VSM. This study reveals, for the first time, a direct influence of the breadth of attention on the effective capacity of VSM.

Correction to: Reduced Value-Driven Attentional Capture among Children with ADHD Compared to Typically Developing Controls.

The authors would like to correct a few minor errors in our article, none of which change the conclusions or interpretations presented.

Reduced Value-Driven Attentional Capture Among Children with ADHD Compared to Typically Developing Controls.

The current study examined whether children with ADHD were more distracted by a stimulus previously associated with reward, but currently goal-irrelevant, than their typically-developing peers. In addition, we also probed the associated cognitive and motivational mechanisms by examining correlations with other behavioral tasks. Participants included 8-12 year-old children with ADHD (n = 30) and typically developing controls (n = 26). Children were instructed to visually search for color-defined targets and received monetary rewards for accurate responses. In a subsequent search task in which color was explicitly irrelevant, we manipulated whether a distractor item appeared in a previously reward-associated color. We examined whether children responded more slowly on trials with the previously-rewarded distractor present compared to trials without this distractor, a phenomenon referred to as value-driven attentional capture (VDAC), and whether children with and without ADHD differed in the extent to which they displayed VDAC. Correlations among working memory performance, immediate reward preference (delay discounting) and attentional capture were also examined. Children with ADHD were significantly less affected by the presence of the previously rewarded distractor than were control participants. Within the ADHD group, greater value-driven attentional capture was associated with poorer working memory. Although both ADHD and control participants were initially distracted by previously reward-associated stimuli, the magnitude of distraction was larger and persisted longer among control participants.

Neural Basis of Cognitive Control over Movement Inhibition: Human fMRI and Primate Electrophysiology Evidence.

Executive control involves the ability to flexibly inhibit or change an action when it is contextually inappropriate. Using the complimentary techniques of human fMRI and monkey electrophysiology in a context-dependent stop signal task, we found a functional double dissociation between the right ventrolateral prefrontal cortex (rVLPFC) and the bi-lateral frontal eye field (FEF). Different regions of rVLPFC were associated with context-based signal meaning versus intention to inhibit a response, while FEF activity corresponded to success or failure of the response inhibition regardless of the stimulus response mapping or the context. These results were validated by electrophysiological recordings in rVLPFC and FEF from one monkey. Inhibition of a planned behavior is therefore likely not governed by a single brain system as had been previously proposed, but instead depends on two distinct neural processes involving different sub-regions of the rVLPFC and their interactions with other motor-related brain regions.

Tracking the will to attend: Cortical activity indexes self-generated, voluntary shifts of attention.

The neural substrates of volition have long tantalized philosophers and scientists. Over the past few decades, researchers have employed increasingly sophisticated technology to investigate this issue, but many studies have been limited considerably by their reliance on intrusive experimental procedures (e.g., abrupt instructional cues), measures of brain activity contaminated by overt behavior, or introspective self-report techniques of questionable validity. Here, we used multivoxel pattern time-course analysis of functional magnetic resonance imaging data to index voluntary, covert perceptual acts-shifts of visuospatial attention-in the absence of instructional cues, overt behavioral indices, and self-report. We found that these self-generated, voluntary attention shifts were time-locked to activity in the medial superior parietal lobule, supporting the hypothesis that this brain region is engaged in voluntary attentional reconfiguration. Self-generated attention shifts were also time-locked to activity in the basal ganglia, a novel finding that motivates further research into the role of the basal ganglia in acts of volition. Remarkably, prior to self-generated shifts of attention, we observed early and selective increases in the activation of medial frontal (dorsal anterior cingulate) and lateral prefrontal (right middle frontal gyrus) cortex-activity that likely reflects processing related to the intention or preparation to reorient attention. These findings, which extend recent evidence on freely chosen motor movements, suggest that dorsal anterior cingulate and lateral prefrontal cortices play key roles in both overt and covert acts of volition, and may constitute core components of a brain network underlying the will to attend.

The Role of Dopamine in Value-Based Attentional Orienting.

Reward learning gives rise to strong attentional biases. Stimuli previously associated with reward automatically capture visual attention regardless of intention. Dopamine signaling within the ventral striatum plays an important role in reward learning, representing the expected reward initiated by a cue. How dopamine and the striatum may be involved in maintaining behaviors that have been shaped by reward learning, even after reward expectancies have changed, is less well understood. Nonspecific measures of brain activity have implicated the striatum in value-based attention. However, the neurochemical mechanisms underlying the attentional priority of learned reward cues remain unexplored. Here, we investigated the contribution of dopamine to value-based attention using positron emission tomography (PET) with [(11)C]raclopride. We show that, in the explicit absence of reward, the magnitude of attentional capture by previously reward-associated but currently task-irrelevant distractors is correlated across individuals with changes in available D2/D3 dopamine receptors (presumably due to intrasynaptic dopamine) linked to distractor processing within the right caudate and posterior putamen. Our findings provide direct evidence linking dopamine signaling within the striatum to the involuntary orienting of attention, and specifically to the attention-grabbing quality of learned reward cues. These findings also shed light on the neurochemical basis of individual susceptibility to value-driven attentional capture, which is known to play a role in addiction. More broadly, the present study highlights the value and feasibility of using PET to relate changes in the release of a neurotransmitter to learning-dependent changes in healthy adults.

Spontaneous Fluctuations in the Flexible Control of Covert Attention.

Spontaneous fluctuations in cognitive flexibility are characterized by moment-to-moment changes in the efficacy of control over attentional shifts. We used fMRI to investigate the neural correlates in humans of spontaneous fluctuations in readiness to covertly shift attention between two peripheral rapid serial visual presentation streams. Target detection response time (RT) after a shift or hold of covert spatial attention served as a behavioral index of fluctuations in attentional flexibility. In particular, the cost associated with shifting attention compared with holding attention varied as a function of pretrial brain activity in key regions of the default mode network (DMN), but not the dorsal attention network. High pretrial activity within the DMN was associated with a greater increase in shift trial RT relative to hold trial RT, revealing that these areas are associated with a state of attentional stability. Conversely, high pretrial activity within bilateral anterior insula and the presupplementary motor area/supplementary motor area was associated with a greater decrease in shift trial RT relative to hold trial RT, reflecting increased flexibility. Our results importantly clarify the roles of the precuneus, medial prefrontal cortex, and lateral parietal cortex, indicating that reduced activity may not simply indicate greater task engagement, but also, specifically, a readiness to update the focus of attention. Investigation of the neural correlates of spontaneous changes in attentional flexibility may contribute to our understanding of disorders of cognitive control as well as healthy variability in the control of spatial attention. SIGNIFICANCE STATEMENT: Individuals regularly experience fluctuations in preparatory cognitive control that affect performance in everyday life. For example, individuals are able to more quickly initiate a spatial shift of attention at some moments than at others. The current study revealed that pretrial brain activity in specific cortical regions predicted trial-by-trial changes in participants' abilities to flexibly shift the focus of attention. Intrinsically generated fluctuations in brain activity within several key default mode network regions, as well as within the anterior insula and presupplementary/supplementary motor areas, carried behavioral consequences for preparatory attentional control beyond lapses of attentional engagement. Our results are the first to link intrinsic variation in pretrial brain activity to moment-by-moment changes in preparatory attentional control over spatial selection.

Valuable Orientations Capture Attention.

Visual attention has long been known to be drawn to stimuli that are physically salient or congruent with task-specific goals. Several recent studies have shown that attention is also captured by stimuli that are neither salient nor task-relevant, but that are rendered in a color that has previously been associated with reward. We investigated whether another feature dimension-orientation-can be associated with reward via learning and thereby elicit value-driven attentional capture. In a training phase, participants received a monetary reward for identifying the color of Gabor patches exhibiting one of two target orientations. A subsequent test phase in which no reward was delivered required participants to search for Gabor patches exhibiting one of two spatial frequencies (orientation was now irrelevant to the task). Previously rewarded orientations robustly captured attention. We conclude that reward learning can imbue features other than color-in this case, specific orientations-with persistent value.

Learned states of preparatory attentional control.

Individuals regularly experience fluctuations in the ability to perform cognitive operations. Although previous research has focused on predicting cognitive flexibility from persistent individual traits, as well as from spontaneous fluctuations in neural activity, the role of learning in shaping preparatory attentional control remains poorly understood. Across 3 experiments, we manipulated the statistical regularities of an attentional orienting paradigm to examine whether individuals modulated attentional flexibility, the readiness to perform a spatial shift of attention, across learned contexts. We found evidence of learning-based modulations in preparatory attentional control settings when the probability of shifting the focus of attention differed based on temporally or color-defined contexts. Furthermore, in the case of color-defined contexts, these modulations in preparatory control persisted even after a change in the underlying statistical properties. Our results indicate that dynamic adjustments in preparatory attentional control are sensitive to the underlying statistical regularities of an environment. This finding has implications for understanding disordered patterns of attentional control and how these patterns might be modified with training.

Multi-regional investigation of the relationship between functional MRI blood oxygenation level dependent (BOLD) activation and GABA concentration.

Several recent studies have reported an inter-individual correlation between regional GABA concentration, as measured by MRS, and the amplitude of the functional blood oxygenation level dependent (BOLD) response in the same region. In this study, we set out to investigate whether this coupling generalizes across cortex. In 18 healthy participants, we performed edited MRS measurements of GABA and BOLD-fMRI experiments using regionally related activation paradigms. Regions and tasks were the: occipital cortex with a visual grating stimulus; auditory cortex with a white noise stimulus; sensorimotor cortex with a finger-tapping task; frontal eye field with a saccade task; and dorsolateral prefrontal cortex with a working memory task. In contrast to the prior literature, no correlation between GABA concentration and BOLD activation was detected in any region. The origin of this discrepancy is not clear. Subtle differences in study design or insufficient power may cause differing results; these and other potential reasons for the discrepant results are discussed. This negative result, although it should be interpreted with caution, has a larger sample size than prior positive results, and suggests that the relationship between GABA and the BOLD response may be more complex than previously thought.

Value-driven attentional priority signals in human basal ganglia and visual cortex.

Goal-directed and stimulus-driven factors determine attentional priority through a well defined dorsal frontal-parietal and ventral temporal-parietal network of brain regions, respectively. Recent evidence demonstrates that reward-related stimuli also have high attentional priority, independent of their physical salience and goal-relevance. The neural mechanisms underlying such value-driven attentional control are unknown. Using human functional magnetic resonance imaging, we demonstrate that the tail of the caudate nucleus and extrastriate visual cortex respond preferentially to task-irrelevant but previously reward-associated objects, providing an attentional priority signal that is sensitive to reward history. The caudate tail has not been implicated in the control of goal-directed or stimulus-driven attention, but is well suited to mediate the value-driven control of attention. Our findings reveal the neural basis of value-based attentional priority.

The role of reward prediction in the control of attention.

Previously rewarded stimuli involuntarily capture attention. The learning mechanisms underlying this value-driven attentional capture remain less understood. We tested whether theories of prediction-based associative reward learning explain the conditions under which reward feedback leads to value-based modulations of attentional priority. Across 4 experiments, we manipulated whether stimulus features served as unique predictors of reward outcomes. Participants received monetary rewards for correctly identifying a color-defined target in an initial search task (training phase) and then immediately completed a second, unrewarded visual search task in which color was irrelevant (test phase). In Experiments 1-3, monetary reward followed correct target selection during training, but critically, no target-defining features carried uniquely predictive information about reward outcomes. Under these conditions, we found no evidence of attentional capture by the previous target colors in the subsequent test phase. Conversely, when target colors in the training phase of Experiment 4 carried uniquely predictive information about reward magnitude, we observed significant attentional capture by the previously rewarded color. Our findings show that value-based attentional priority only develops for stimulus features that carry uniquely predictive information about reward, ruling out a purely motivational account and suggesting that mechanisms of reward prediction play an important role in shaping attentional priorities.

The attribution of value-based attentional priority in individuals with depressive symptoms.

The capture of attention by stimuli previously associated with reward has been demonstrated across a wide range of studies. Such value-based attentional priority appears to be robust, and cases where reward feedback fails to modulate subsequent attention have not been reported. However, individuals differ in their sensitivity to external rewards, and such sensitivity is abnormally blunted in depression. Here, we show that depressive symptomology is accompanied by insensitivity to value-based attentional bias. We replicate attentional capture by stimuli previously associated with reward in a control sample and show that these same reward-related stimuli do not capture attention in individuals experiencing symptoms of depression. This sharp contrast in performance indicates that value-based attentional biases depend on the normal functioning of the brain's reward system and suggests that a failure to preferentially attend to reward-related information may play a role in the experience of depression.

Attending to illusory differences in object size.

Focused visual attention can be shifted between objects and locations (attentional orienting) or expanded and contracted in spatial extent (attentional focusing). Although orienting and focusing both modulate visual processing, they have been shown to be distinct, independent modes of attentional control. Objects play a central role in visual attention, and it is known that high-level object representations guide attentional orienting. It not known, however, whether attentional focusing is driven by low-level object representations (which code object size in terms of retinotopic extent) or by high-level representations (which code perceived size). We manipulated the perceived size of physically identical objects by using line drawings or photographs that induced the Ponzo illusion, in a task requiring the detection of a target within these objects. The distribution of attention was determined by the perceived size and not by the retinotopic size of an attended object, indicating that attentional focusing is guided by high-level object representations.

Attentional bias for nondrug reward is magnified in addiction.

Attentional biases for drug-related stimuli play a prominent role in addiction, predicting treatment outcomes. Attentional biases also develop for stimuli that have been paired with nondrug rewards in adults without a history of addiction, the magnitude of which is predicted by visual working-memory capacity and impulsiveness. We tested the hypothesis that addiction is associated with an increased attentional bias for nondrug (monetary) reward relative to that of healthy controls, and that this bias is related to working-memory impairments and increased impulsiveness. Seventeen patients receiving methadone-maintenance treatment for opioid dependence and 17 healthy controls participated. Impulsiveness was measured using the Barratt Impulsiveness Scale (BIS-11; Patton, Stanford, & Barratt, 1995), visual working-memory capacity was measured as the ability to recognize briefly presented color stimuli, and attentional bias was measured as the magnitude of response time slowing caused by irrelevant but previously reward-associated distractors in a visual-search task. The results showed that attention was biased toward the distractors across all participants, replicating previous findings. It is important to note, this bias was significantly greater in the patients than in the controls and was negatively correlated with visual working-memory capacity. Patients were also significantly more impulsive than controls as a group. Our findings demonstrate that patients in treatment for addiction experience greater difficulty ignoring stimuli associated with nondrug reward. This nonspecific reward-related bias could mediate the distracting quality of drug-related stimuli previously observed in addiction.

Computational analysis of LDDMM for brain mapping.

One goal of computational anatomy (CA) is to develop tools to accurately segment brain structures in healthy and diseased subjects. In this paper, we examine the performance and complexity of such segmentation in the framework of the large deformation diffeomorphic metric mapping (LDDMM) registration method with reference to atlases and parameters. First we report the application of a multi-atlas segmentation approach to define basal ganglia structures in healthy and diseased kids' brains. The segmentation accuracy of the multi-atlas approach is compared with the single atlas LDDMM implementation and two state-of-the-art segmentation algorithms-Freesurfer and FSL-by computing the overlap errors between automatic and manual segmentations of the six basal ganglia nuclei in healthy subjects as well as subjects with diseases including ADHD and Autism. The high accuracy of multi-atlas segmentation is obtained at the cost of increasing the computational complexity because of the calculations necessary between the atlases and a subject. Second, we examine the effect of parameters on total LDDMM computation time and segmentation accuracy for basal ganglia structures. Single atlas LDDMM method is used to automatically segment the structures in a population of 16 subjects using different sets of parameters. The results show that a cascade approach and using fewer time steps can reduce computational complexity as much as five times while maintaining reliable segmentations.

Reward predictions bias attentional selection.

Attention selects stimuli for perceptual and cognitive processing according to an adaptive selection schedule. It has long been known that attention selects stimuli that are task relevant or perceptually salient. Recent evidence has shown that stimuli previously associated with reward persistently capture attention involuntarily, even when they are no longer associated with reward. Here we examine whether the capture of attention by previously reward-associated stimuli is modulated by the processing of current but unrelated rewards. Participants learned to associate two color stimuli with different amounts of reward during a training phase. In a subsequent test phase, these previously rewarded color stimuli were occasionally presented as to-be-ignored distractors while participants performed visual search for each of two differentially rewarded shape-defined targets. The results reveal that attentional capture by formerly rewarded distractors was the largest when both recently received and currently expected reward were the highest in the test phase, even though such rewards were unrelated to the color distractors. Our findings support a model in which value-driven attentional biases acquired through reward learning are maintained via the cognitive mechanisms involved in predicting future rewards.

Persistence of value-driven attentional capture.

Stimuli that have previously been associated with the delivery of reward involuntarily capture attention when presented as unrewarded and task-irrelevant distractors in a subsequent visual search task. It is unknown how long such effects of reward learning on attention persist. One possibility is that value-driven attentional biases are plastic and constantly evolve to reflect only recent reward history. According to such a mechanism of attentional control, only consistently reinforced patterns of attention allocation persist for extended periods of time. Another possibility is that reward learning creates enduring changes in attentional priority that can persist indefinitely without further learning. Here we provide evidence for an enduring effect of reward learning on attentional priority: stimuli previously associated with reward in a training phase capture attention when presented as irrelevant distractors over half a year later, without the need for further reward learning.

Reinforcement learning modulates the stability of cognitive control settings for object selection.

Cognitive flexibility reflects both a trait that reliably differs between individuals and a state that can fluctuate moment-to-moment. Whether individuals can undergo persistent changes in cognitive flexibility as a result of reward learning is less understood. Here, we investigated whether reinforcing a periodic shift in an object selection strategy can make an individual more prone to switch strategies in a subsequent unrelated task. Participants completed two different choice tasks in which they selected one of four objects in an attempt to obtain a hidden reward on each trial. During a training phase, objects were defined by color. Participants received either consistent reward contingencies in which one color was more often rewarded, or contingencies in which the color that was more often rewarded changed periodically and without warning. Following the training phase, all participants completed a test phase in which reward contingencies were defined by spatial location and the location that was more often rewarded remained constant across the entire task. Those participants who received inconsistent contingencies during training continued to make more variable selections during the test phase in comparison to those who received the consistent training. Furthermore, a difference in the likelihood to switch selections on a trial-by-trial basis emerged between training groups: participants who received consistent contingencies during training were less likely to switch object selections following an unrewarded trial and more likely to repeat a selection following reward. Our findings provide evidence that the extent to which priority shifting is reinforced modulates the stability of cognitive control settings in a persistent manner, such that individuals become generally more or less prone to shifting priorities in the future.