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.

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.

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.

Value-driven attentional capture.

Attention selects which aspects of sensory input are brought to awareness. To promote survival and well-being, attention prioritizes stimuli both voluntarily, according to context-specific goals (e.g., searching for car keys), and involuntarily, through attentional capture driven by physical salience (e.g., looking toward a sudden noise). Valuable stimuli strongly modulate voluntary attention allocation, but there is little evidence that high-value but contextually irrelevant stimuli capture attention as a consequence of reward learning. Here we show that visual search for a salient target is slowed by the presence of an inconspicuous, task-irrelevant item that was previously associated with monetary reward during a brief training session. Thus, arbitrary and otherwise neutral stimuli imbued with value via associative learning capture attention powerfully and persistently during extinction, independently of goals and salience. Vulnerability to such value-driven attentional capture covaries across individuals with working memory capacity and trait impulsivity. This unique form of attentional capture may provide a useful model for investigating failures of cognitive control in clinical syndromes in which value assigned to stimuli conflicts with behavioral goals (e.g., addiction, obesity).

Comparing machines and humans on a visual categorization test.

Automated scene interpretation has benefited from advances in machine learning, and restricted tasks, such as face detection, have been solved with sufficient accuracy for restricted settings. However, the performance of machines in providing rich semantic descriptions of natural scenes from digital images remains highly limited and hugely inferior to that of humans. Here we quantify this "semantic gap" in a particular setting: We compare the efficiency of human and machine learning in assigning an image to one of two categories determined by the spatial arrangement of constituent parts. The images are not real, but the category-defining rules reflect the compositional structure of real images and the type of "reasoning" that appears to be necessary for semantic parsing. Experiments demonstrate that human subjects grasp the separating principles from a handful of examples, whereas the error rates of computer programs fluctuate wildly and remain far behind that of humans even after exposure to thousands of examples. These observations lend support to current trends in computer vision such as integrating machine learning with parts-based modeling.

Visuotopic cortical connectivity underlying attention revealed with white-matter tractography.

Visual attention selects behaviorally relevant information for detailed processing by resolving competition for representation among stimuli in retinotopically organized visual cortex. The signals that control this attentional biasing are thought to arise in a frontoparietal network of several brain regions, including posterior parietal cortex. Recent studies have revealed a topographic organization in the intraparietal sulcus (IPS) that mirrors the retinotopic organization in visual cortex, suggesting that connectivity between these regions might provide the mechanism by which attention acts on early cortical representations. Using white-matter imaging and functional MRI, we examined the connectivity between two topographic regions of IPS and six retinotopically defined areas in visual cortex. We observed a strong positive correlation between attention modulations in visual cortex and connectivity of posterior IPS, suggesting that these white-matter connections mediate the attention signals that resolve competition among stimuli for representation in visual cortex. Furthermore, we found that connectivity between IPS and V1 consistently respects visuotopic boundaries, whereas connections to V2 and V3/VP disperse by 60%. This pattern is consistent with changes in receptive field size across regions and suggests that a primary role of posterior IPS is to code spatially specific visual information. In summary, we have identified white-matter pathways that are ideally suited to carry attentional biasing signals in visuotopic coordinates from parietal control regions to sensory regions in humans. These results provide critical evidence for the biased competition theory of attention and specify neurobiological constraints on the functional brain organization of visual attention.

Decoding cognitive control in human parietal cortex.

Efficient execution of perceptual-motor tasks requires rapid voluntary reconfiguration of cognitive task sets as circumstances unfold. Such acts of cognitive control, which are thought to rely on a network of cortical regions in prefrontal and posterior parietal cortex, include voluntary shifts of attention among perceptual inputs or among memory representations, or switches between categorization or stimulus-response mapping rules. A critical unanswered question is whether task set shifts in these different domains are controlled by a common, domain-independent mechanism or by separate, domain-specific mechanisms. Recent studies have implicated a common region of medial superior parietal lobule (mSPL) as a domain-independent source of cognitive control during shifts between perceptual, mnemonic, and rule representations. Here, we use fMRI and event-related multivoxel pattern classification to show that spatial patterns of brain activity within mSPL reliably express which of several domains of cognitive control is at play on a moment-by-moment basis. Critically, these spatiotemporal brain patterns are stable over time within subjects tested several months apart and across a variety of tasks, including shifting visuospatial attention, switching categorization rules, and shifting attention in working memory.

Control of spatial and feature-based attention in frontoparietal cortex.

Visual attention selects task-relevant information from scenes to help achieve behavioral goals. Attention can be deployed within multiple domains to select specific spatial locations, features, or objects. Recent evidence has shown that voluntary shifts of attention in multiple domains are consistently associated with transient increases in cortical activity in medial superior parietal lobule, suggesting that this may be the source of a domain-independent control signal that initiates the reconfiguration of attention. To investigate this hypothesis, we used fMRI to measure changes in cortical activation while human subjects shifted attention between spatial locations or between colors at a location. Univariate multiple regression analysis revealed a common, domain-independent transient signal [in posterior parietal cortex (PPC) and prefrontal cortex] time-locked to shifts of attention in both domains. However, multivariate pattern classification conducted on the cortical surface revealed that the spatiotemporal pattern of activity within PPC differed reliably for spatial and feature-based attention shifts. These results suggest that the posterior parietal cortex is a common hub for the control of attention shifts but contains subpopulations of neurons with domain-specific tuning for cognitive control.

Cortical mechanisms of cognitive control for shifting attention in vision and working memory.

Organisms operate within both a perceptual domain of objects and events, and a mnemonic domain of past experiences and future goals. Each domain requires a deliberate selection of task-relevant information, through deployments of external (perceptual) and internal (mnemonic) attention, respectively. Little is known about the control of attention shifts in working memory, or whether voluntary control of attention in these two domains is subserved by a common or by distinct functional networks. We used human fMRI to examine the neural basis of cognitive control while participants shifted attention in vision and in working memory. We found that these acts of control recruit in common a subset of the dorsal fronto-parietal attentional control network, including the medial superior parietal lobule, intraparietal sulcus, and superior frontal sulcus/gyrus. Event-related multivoxel pattern classification reveals, however, that these regions exhibit distinct spatio-temporal patterns of neural activity during internal and external shifts of attention, respectively. These findings constrain theoretical accounts of selection in working memory and perception by showing that populations of neurons in dorsal fronto-parietal network regions exhibit selective tuning for acts of cognitive control in different cognitive domains.

Decoding task-based attentional modulation during face categorization.

Attention is a neurocognitive mechanism that selects task-relevant sensory or mnemonic information to achieve current behavioral goals. Attentional modulation of cortical activity has been observed when attention is directed to specific locations, features, or objects. However, little is known about how high-level categorization task set modulates perceptual representations. In the current study, observers categorized faces by gender (male vs. female) or race (Asian vs. White). Each face was perceptually ambiguous in both dimensions, such that categorization of one dimension demanded selective attention to task-relevant information within the face. We used multivoxel pattern classification to show that task-specific modulations evoke reliably distinct spatial patterns of activity within three face-selective cortical regions (right fusiform face area and bilateral occipital face areas). This result suggests that patterns of activity in these regions reflect not only stimulus-specific (i.e., faces vs. houses) responses but also task-specific (i.e., race vs. gender) attentional modulation. Furthermore, exploratory whole-brain multivoxel pattern classification (using a searchlight procedure) revealed a network of dorsal fronto-parietal regions (left middle frontal gyrus and left inferior and superior parietal lobule) that also exhibit distinct patterns for the two task sets, suggesting that these regions may represent abstract goals during high-level categorization tasks.

Perceptual expectation evokes category-selective cortical activity.

Selective visual attention directed to a location (even in the absence of a stimulus) increases activity in the corresponding regions of visual cortex and enhances the speed and accuracy of target perception. We further explored top-down influences on perceptual representations by manipulating observers' expectations about the category of an upcoming target. Observers viewed a display in which an object (either a face or a house) gradually emerged from a state of phase-scrambled noise; a cue established expectation about the object category. Observers were faster to categorize faces (gender discrimination) or houses (structural discrimination) when the category of the partially scrambled object matched their expectation. Functional magnetic resonance imaging revealed that this expectation was associated with anticipatory increases in category-specific visual cortical activity, even in the absence of object- or category-specific visual information. Expecting a face evoked increased activity in face-selective cortical regions in the fusiform gyrus and superior temporal sulcus. Conversely, expecting a house increased activity in parahippocampal gyrus. These results suggest that visual anticipation facilitates subsequent perception by recruiting, in advance, the same cortical mechanisms as those involved in perception.

A domain-independent source of cognitive control for task sets: shifting spatial attention and switching categorization rules.

To optimize task performance as circumstances unfold, cognitive control mechanisms configure the brain to prepare for upcoming events through voluntary shifts in task set. A foundational unanswered question concerns whether different domains of cognitive control (e.g., spatial attention shifts, shifts between categorization rules, or shifts between stimulus-response mapping rules) are associated with separate, domain-specific control mechanisms, or whether a common, domain-independent source of control initiates shifts in all domains. Previous studies have tested different domains of cognitive control in separate groups of subjects using different paradigms, yielding equivocal conclusions. Here, using rapid event-related MRI, we report evidence from a single paradigm in which subjects were cued to perform both shifts of spatial attention and switches between categorization rules. A conjunction analysis revealed a common transient signal evoked by switch cues in medial superior parietal lobule for both domains of control, revealing a single domain-independent control mechanism.

Avoiding non-independence in fMRI data analysis: leave one subject out.

Concerns regarding certain fMRI data analysis practices have recently evoked lively debate. The principal concern regards the issue of non-independence, in which an initial statistical test is followed by further non-independent statistical tests. In this report, we propose a simple, practical solution to reduce bias in secondary tests due to non-independence using a leave-one-subject-out (LOSO) approach. We provide examples of this method, show how it reduces effect size inflation, and suggest that it can serve as a functional localizer when within-subject methods are impractical.

Cortical mechanisms for shifting and holding visuospatial attention.

Access to visual awareness is often determined by covert, voluntary deployments of visual attention. Voluntary orienting without eye movements requires decoupling attention from the locus of fixation, a shift to the desired location, and maintenance of attention at that location. We used event-related functional magnetic resonance imaging to dissociate these components while observers shifted attention among 3 streams of letters and digits, one located at fixation and 2 in the periphery. Compared with holding attention at the current location, shifting attention between the peripheral locations was associated with transient increases in neural activity in the superior parietal lobule (SPL) and frontal eye fields (FEF), as in previous studies. The supplementary eye fields and separate portions of SPL and FEF were more active for decoupling attention from fixation than for shifting attention to a new location. Large segments of precentral sulcus (PreCS) and posterior parietal cortex (PPC) were more active when attention was maintained in the periphery than when it was maintained at fixation. We conclude that distinct subcomponents of the dorsal frontoparietal network initiate redeployments of covert attention to new locations and disengage attention from fixation, while sustained activity in lateral regions of PPC and PreCS represents sustained states of peripheral attention.

Learning to attend: effects of practice on information selection.

Though practice can lead to improved performance in many domains, it is currently unknown how practice affects the deployment of selective attention to filter distracting information. We conducted a series of experiments to address this issue by examining how performance on a task changed after repeated exposure to distractors. Distraction initially slowed response time during task performance, an effect that diminished with repeated exposure to the distractors. When the distractors were consistent in appearance, the practice effect developed quickly but was stimulus-specific. When the distractors were more variable in appearance, the practice effect developed slowly but transferred more readily to other conditions. These data indicate that practice with overcoming distraction leads to improvements in information filtering mechanisms that generalize beyond the training regimen when variable distractor stimuli are experienced.

Human adult cortical reorganization and consequent visual distortion.

Neural and behavioral evidence for cortical reorganization in the adult somatosensory system after loss of sensory input (e.g., amputation) has been well documented. In contrast, evidence for reorganization in the adult visual system is far less clear: neural evidence is the subject of controversy, behavioral evidence is sparse, and studies combining neural and behavioral evidence have not previously been reported. Here, we report converging behavioral and neuroimaging evidence from a stroke patient (B.L.) in support of cortical reorganization in the adult human visual system. B.L.'s stroke spared the primary visual cortex (V1), but destroyed fibers that normally provide input to V1 from the upper left visual field (LVF). As a consequence, B.L. is blind in the upper LVF, and exhibits distorted perception in the lower LVF: stimuli appear vertically elongated, toward and into the blind upper LVF. For example, a square presented in the lower LVF is perceived as a rectangle extending upward. We hypothesized that the perceptual distortion was a consequence of cortical reorganization in V1. Extensive behavioral testing supported our hypothesis, and functional magnetic resonance imaging (fMRI) confirmed V1 reorganization. Together, the behavioral and fMRI data show that loss of input to V1 after a stroke leads to cortical reorganization in the adult human visual system, and provide the first evidence that reorganization of the adult visual system affects visual perception. These findings contribute to our understanding of the human adult brain's capacity to change and has implications for topics ranging from learning to recovery from brain damage.

Transient neural activity in human parietal cortex during spatial attention shifts.

Observers viewing a complex visual scene selectively attend to relevant locations or objects and ignore irrelevant ones. Selective attention to an object enhances its neural representation in extrastriate cortex, compared with those of unattended objects, via top-down attentional control signals. The posterior parietal cortex is centrally involved in this control of spatial attention. We examined brain activity during attention shifts using rapid, event-related fMRI of human observers as they covertly shifted attention between two peripheral spatial locations. Activation in extrastriate cortex increased after a shift of attention to the contralateral visual field and remained high during sustained contralateral attention. The time course of activity was substantially different in posterior parietal cortex, where transient increases in activation accompanied shifts of attention in either direction. This result suggests that activation of the parietal cortex is associated with a discrete signal to shift spatial attention, and is not the source of a signal to continuously maintain the current attentive state.

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.

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.

Parietal cortex mediates voluntary control of spatial and nonspatial auditory attention.

The human posterior parietal cortex (PPC) is widely believed to subserve visually guided spatial behavior, including the control of visual attention, eye movements, and reaching. To explore the generality of this function, we measured human brain activity using functional magnetic resonance imaging during spatial and nonspatial shifts of auditory attention. Both spatial and nonspatial shifts of auditory attention evoked transient activity in the medial superior parietal cortex. These results reveal that the PPC is not exclusively devoted to visuospatial behavior; similar regions within a dorsomedial subcompartment provide a domain-independent reconfiguration signal for the control of spatial and nonspatial attention in both visual and nonvisual modalities.