Adam S. Greenberg

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.

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.

Estimating linear cortical magnification in human primary visual cortex via dynamic programming.

Human primary visual cortex is organized retinotopically, with adjacent locations in cortex representing adjacent locations on the retina. The spatial sampling in cortex is highly nonuniform: the amount of cortex devoted to a unit area of retina decreases with increasing retinal eccentricity. This sampling property can be quantified by the linear cortical magnification factor, which is expressed in terms of millimeters of cortex per degree of visual angle. In this paper, we present a new method using dynamic programming and fMRI retinotopic eccentricity mapping to estimate the linear cortical magnification factor in human primary visual cortex (V1). We localized cortical activity while subjects viewed each of seven stationary contrast- reversing radial checkerboard rings of equal thickness that tiled the visual field from 1.62 to 12.96 degrees of eccentricity. Imaging data from all epochs of each ring were contrasted with data from fixation epochs on a subject-by-subject basis. The resulting t statistic maps were then superimposed on a local coordinate system constructed from the gray/white matter boundary surface of each individual subjects occipital lobe, separately for each ring. Smoothed maps of functional activity on the cortical surface were constructed using orthonormal bases of the Laplace-Beltrami operator that incorporate the geometry of the cortical surface. This allowed us to stably track the ridge of maximum activation due to each ring via dynamic programming optimization over all possible paths on the cortical surface. We estimated the linear cortical magnification factor by calculating geodesic distances between activation ridges on the cortical surface in a population of five normal subjects. The reliability of these estimates was assessed by comparing results based on data from one quadrant to those based on data from the full hemifield along with a split-half reliability analysis.

Are you listening? Brain activation associated with sustained nonspatial auditory attention in the presence and absence of stimulation

Neuroimaging studies investigating the voluntary (top‐down) control of attention largely agree that this process recruits several frontal and parietal brain regions. Since most studies used attention tasks requiring several higher‐order cognitive functions (e.g. working memory, semantic processing, temporal integration, spatial orienting) as well as different attentional mechanisms (attention shifting, distractor filtering), it is unclear what exactly the observed frontoparietal activations reflect. The present functional magnetic resonance imaging study investigated, within the same participants, signal changes in (1) a “Simple Attention” task in which participants attended to a single melody, (2) a “Selective Attention” task in which they simultaneously ignored another melody, and (3) a “Beep Monitoring” task in which participants listened in silence for a faint beep. Compared to resting conditions with identical stimulation, all tasks produced robust activation increases in auditory cortex, cross‐modal inhibition in visual and somatosensory cortex, and decreases in the default mode network, indicating that participants were indeed focusing their attention on the auditory domain. However, signal increases in frontal and parietal brain areas were only observed for tasks 1 and 2, but completely absent for task 3. These results lead to the following conclusions: under most conditions, frontoparietal activations are crucial for attention since they subserve higher‐order cognitive functions inherently related to attention. However, under circumstances that minimize other demands, nonspatial auditory attention in the absence of stimulation can be maintained without concurrent frontal or parietal activations. Hum Brain Mapp 35:2233–2252, 2014.

Strategic Control of Attention to Objects and Locations

Humans have a highly developed expertise to selectively process sensory input that is relevant to their goals, an ability known as attention. Visual attention to spatial locations modulates the activity of retinotopically organized neurons within visual cortex. However, attention can also be

The Role of Visual Attention In Internet Advertising: Eleven Questions and a Score of Answers

like any reputable academic journal, takes a great deal of fierce pride in the deliberate steps it takes in bringing a study to publication. Our review process insists that the route to these pages is a course protected by a long, deliberate peer-to-peer program. And, as any author will attest, we do not stop fine-tuning until we are convinced that an article is ready to provide service to our dual audience of academic and marketing-research/advertising practitioners. We are proud of the diligence we bring to our process but, in publishing and in horseshoes, sometimes you get lucky by simply being in the right place at the right time. Briefly: Ted McConnell, EVP/digital at the Advertising Research Foundation (ARF)—the publisher of this Journal—was scouting for some fresh answers on some vexing questions about digital marketing. Colleague Stephen D. Rappaport, the ARF’s director of knowledge solutions, had a most untraditional source for McConnell—a post-doctoral researcher at Carnegie Mellon University whose career started in biomedical engineering and had veered into cognitive neuroscience. With a PhD degree from Johns Hopkins University, Adam Greenberg had done a lot of thinking about thinking—particularly about how humans control their behavior in response to a visual stimulus and which brain mechanisms are involved. Recalls McConnell, “Steve suggested this guy would have a fresh perspective because of his exhaustive work on attention and cognition and that, oddly, he had never considered advertising as a field that would benefit from his work.” It may have been Greenberg’s only misstep. McConnell picks up the story: “I sent him a base set of research and asked him to look at it, add to it, and connect the research to the questions in a balanced way.” And, in the pages that follow, we present the verbatim exchange between McConnell and Greenberg. ARF: What are the stages of attention to an advertisement? How does attention work? Greenberg: Attention is typically described in terms of mode of selection. In general, attention can be “captured” by the features of a stimulus or it can be “directed” toward an item by some goals of the individual. Attention capture often is called bottom-up because it relies on the low-level properties of the stimulus; directed attention is often called top-down because it depends on the moment-by-moment desires of the animal (Egeth and Yantis, 1997). Of course, at any point in time, one’s attention is guided by some combination of top-down and bottom-up attention. This is particularly true when it comes to advertising. A very salient advertisement can capture one’s (bottom-up) attention when involved with unrelated tasks, or (top-down) attention can be directed toward an advertisement because it is relevant to the task at hand (Jessen and Rodway, 2010). Attention also is known to fluctuate between more focused and dispersed states over a relatively short time course (~seconds) and has been shown to occur when viewing advertisements (Wedel, Pieters, and Liechty, 2008). Advertisers may want their advertisements to appeal to these two different modes of attentional selection at different times (or via different forms of advertising). There is some evidence that Internet advertising operates differently, depending on the context in which the ad is placed. For example, advertisements placed on search results pages are more likely to evoke top-down attention when appropriately targeted to the search terms (Kim and Lee, 2011). By contrast, advertisements appearing on non-search Web sites may be more likely to capture attention in a bottom-up manner when features are sufficiently distinctive (Simola, Kuisma, Oorni, Uusitalo, and Hyona, 2011). The time course of attention is different for bottom-up versus top-down selection. The Role of Visual Attention In Internet Advertising Eleven Questions and a Score of Answers

Retinotopic information interacts with category selectivity in human ventral cortex

Until recently, the general consensus with respect to the organization of ventral visual cortex is that early, retinotopic regions are sensitive to the spatial position of the input stimuli whereas later, higher-order regions are sensitive to the category of the input stimuli. Growing recognition of the bidirectional connectivity of the visual system has challenged this view and recent empirical evidence suggests a more interactive and graded system. Here, based on findings from functional MRI in adult observers, in which meridians and category selective regions are localized and their activation sampled, we support this latter perspective by showing that category effects are present in retinotopic cortical areas and spatial position effects are present in higher-order regions. Furthermore, the results indicate that the retinotopic and later areas are functionally connected suggesting a possible mechanism by which these seemingly disparate effects come to be intermixed in both early and later regions of the visual system.

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.

Visual field meridians modulate the reallocation of object-based attention

Object-based attention (OBA) enhances processing within the boundaries of a selected object. Larger OBA effects have been observed for horizontal compared to vertical rectangles, which were eliminated when controlling for attention shifts across the visual field meridians. We aimed to elucidate the modulatory role of the meridians on OBA. We hypothesized that the contralateral organization of visual cortex accounts for these differences in OBA prioritization. Participants viewed “L”-shaped objects and, following a peripheral cue at the object vertex, detected the presence of a target at the cued location (valid), or at a non-cued location (invalid) offset either horizontally or vertically. In Experiment 1, the single displayed object contained components crossing both meridians. In Experiment 2, one cued object and one non-cued object were displayed such that both crossed the meridians. In Experiment 3, one cued object was sequestered into one screen quadrant, with its vertex either near or far from fixation. Results from Experiments 1 and 2 revealed a horizontal shift advantage (faster RTs for horizontal shifts across the vertical meridian compared to vertical shifts across the horizontal meridian), regardless of whether shifts take place within a cued object (Experiment 1) or between objects (Experiment 2). Results from Experiment 3 revealed no difference between horizontal and vertical shifts for objects that were positioned far from fixation, although the horizontal shift advantage reappeared for objects near fixation. These findings suggest a critical modulatory role of visual field meridians in the efficiency of reorienting object-based attention.

The effects of visual search efficiency on object-based attention

The attentional prioritization hypothesis of object-based attention (Shomstein & Yantis in Perception & Psychophysics, 64, 41–51, 2002) suggests a two-stage selection process comprising an automatic spatial gradient and flexible strategic (prioritization) selection. The combined attentional priorities of these two stages of object-based selection determine the order in which participants will search the display for the presence of a target. The strategic process has often been likened to a prioritized visual search. By modifying the double-rectangle cueing paradigm (Egly, Driver, & Rafal in Journal of Experimental Psychology: General, 123, 161–177, 1994) and placing it in the context of a larger-scale visual search, we examined how the prioritization search is affected by search efficiency. By probing both targets located on the cued object and targets external to the cued object, we found that the attentional priority surrounding a selected object is strongly modulated by search mode. However, the ordering of the prioritization search is unaffected by search mode. The data also provide evidence that standard spatial visual search and object-based prioritization search may rely on distinct mechanisms. These results provide insight into the interactions between the mode of visual search and object-based selection, and help define the modulatory consequences of search efficiency for object-based attention.