A cortical zoom-in operation underlies covert shifts of visual spatial attention.

Shifting the focus of attention without moving the eyes poses challenges for signal coding in visual cortex in terms of spatial resolution, signal routing, and cross-talk. Little is known how these problems are solved during focus shifts. Here, we analyze the spatiotemporal dynamic of neuromagnetic activity in human visual cortex as a function of the size and number of focus shifts in visual search. We find that large shifts elicit activity modulations progressing from highest (IT) through mid-level (V4) to lowest hierarchical levels (V1). Smaller shifts cause those modulations to start at lower levels in the hierarchy. Successive shifts involve repeated backward progressions through the hierarchy. We conclude that covert focus shifts arise from a cortical coarse-to-fine process progressing from retinotopic areas with larger toward areas with smaller receptive fields. This process localizes the target and increases the spatial resolution of selection, which resolves the above issues of cortical coding.

Mind-wandering Is Accompanied by Both Local Sleep and Enhanced Processes of Spatial Attention Allocation.

Mind-wandering (MW) is a subjective, cognitive phenomenon, in which thoughts move away from the task toward an internal train of thoughts, possibly during phases of neuronal sleep-like activity (local sleep, LS). MW decreases cortical processing of external stimuli and is assumed to decouple attention from the external world. Here, we directly tested how indicators of LS, cortical processing, and attentional selection change in a pop-out visual search task during phases of MW. Participants' brain activity was recorded using magnetoencephalography, MW was assessed via self-report using randomly interspersed probes. As expected, the performance decreased under MW. Consistent with the occurrence of LS, MW was accompanied by a decrease in high-frequency activity (HFA, 80-150 Hz) and an increase in slow wave activity (SWA, 1-6 Hz). In contrast, visual attentional selection as indexed by the N2pc component was enhanced during MW with the N2pc amplitude being directly linked to participants' performance. This observation clearly contradicts accounts of attentional decoupling that would predict a decrease in attention-related responses to external stimuli during MW. Together, our results suggest that MW occurs during phases of LS with processes of attentional target selection being upregulated, potentially to compensate for the mental distraction during MW.

Attention expedites target selection by prioritizing the neural processing of distractor features.

Whether doing the shopping, or driving the car - to navigate daily life, our brain has to rapidly identify relevant color signals among distracting ones. Despite a wealth of research, how color attention is dynamically adjusted is little understood. Previous studies suggest that the speed of feature attention depends on the time it takes to enhance the neural gain of cortical units tuned to the attended feature. To test this idea, we had human participants switch their attention on the fly between unpredicted target color alternatives, while recording the electromagnetic brain response to probes matching the target, a non-target, or a distracting alternative target color. Paradoxically, we observed a temporally prioritized processing of distractor colors. A larger neural modulation for the distractor followed by its stronger attenuation expedited target identification. Our results suggest that dynamic adjustments of feature attention involve the temporally prioritized processing and elimination of distracting feature representations.

Decoding the covert shift of spatial attention from electroencephalographic signals permits reliable control of a brain-computer interface.

OBJECTIVE: One of the main goals of brain-computer interfaces (BCI) is to restore communication abilities in patients. BCIs often use event-related potentials (ERPs) like the P300 which signals the presence of a target in a stream of stimuli. The P300 and related approaches, however, are inherently limited, as they require many stimulus presentations to obtain a usable control signal. Many approaches depend on gaze direction to focus the target, which is also not a viable approach in many cases, because eye movements might be impaired in potential users. Here we report on a BCI that avoids both shortcomings by decoding spatial target information, independent of gaze shifts. APPROACH: We present a new method to decode from the electroencephalogram (EEG) covert shifts of attention to one out of four targets simultaneously presented in the left and right visual field. The task is designed to evoke the N2pc component-a hemisphere lateralized response, elicited over the occipital scalp contralateral to the attended target. The decoding approach involves decoding of the N2pc based on data-driven estimation of spatial filters and a correlation measure. MAIN RESULTS: Despite variability of decoding performance across subjects, 22 out of 24 subjects performed well above chance level. Six subjects even exceeded 80% (cross-validated: 89%) correct predictions in a four-class discrimination task. Hence, the single-trial N2pc proves to be a component that allows for reliable BCI control. An offline analysis of the EEG data with respect to their dependence on stimulation time and number of classes demonstrates that the present method is also a workable approach for two-class tasks. SIGNIFICANCE: Our method extends the range of strategies for gaze-independent BCI control. The proposed decoding approach has the potential to be efficient in similar applications intended to decode ERPs.

Dissociating Reward- and Attention-driven Biasing of Global Feature-based Selection in Human Visual Cortex.

Objects that promise rewards are prioritized for visual selection. The way this prioritization shapes sensory processing in visual cortex, however, is debated. It has been suggested that rewards motivate stronger attentional focusing, resulting in a modulation of sensory selection in early visual cortex. An open question is whether those reward-driven modulations would be independent of similar modulations indexing the selection of attended features that are not associated with reward. Here, we use magnetoencephalography in human observers to investigate whether the modulations indexing global color-based selection in visual cortex are separable for target- and (monetary) reward-defining colors. To assess the underlying global color-based activity modulation, we compare the event-related magnetic field response elicited by a color probe in the unattended hemifield drawn either in the target color, the reward color, both colors, or a neutral task-irrelevant color. To test whether target and reward relevance trigger separable modulations, we manipulate attention demands on target selection while keeping reward-defining experimental parameters constant. Replicating previous observations, we find that reward and target relevance produce almost indistinguishable gain modulations in ventral extratriate cortex contralateral to the unattended color probe. Importantly, increasing attention demands on target discrimination increases the response to the target-defining color, whereas the response to the rewarded color remains largely unchanged. These observations indicate that, although task relevance and reward influence the very same feature-selective area in extrastriate visual cortex, the associated modulations are largely independent.

Enhanced spatial focusing increases feature-based selection in unattended locations.

Attention is a multifaceted phenomenon, which operates on features (e.g., colour or motion) and over space. A fundamental question is whether the attentional selection of features is confined to the spatially-attended location or operates independently across the entire visual field (global feature-based attention, GFBA). Studies providing evidence for GFBA often employ feature probes presented at spatially unattended locations, which elicit enhanced brain responses when they match a currently-attended target feature. However, the validity of this interpretation relies on consistent spatial focusing onto the target. If the probe were to temporarily attract spatial attention, the reported effects could reflect transient spatial selection processes, rather than GFBA. Here, using magnetoencephalographic recordings (MEG) in humans, we manipulate the strength and consistency of spatial focusing to the target by increasing the target discrimination difficulty (Experiment 1), and by demarcating the upcoming target's location with a placeholder (Experiment 2), to see if GFBA effects are preserved. We observe that motivating stronger spatial focusing to the target did not diminish the effects of GFBA. Instead, aiding spatial pre-focusing with a placeholder enhanced the feature response at unattended locations. Our findings confirm that feature selection effects measured with spatially-unattended probes reflect a true location-independent neural bias.

Cortical Mechanisms of Prioritizing Selection for Rejection in Visual Search.

In visual search, the more one knows about a target, the faster one can find it. Surprisingly, target identification is also faster with knowledge about distractor-features. The latter is paradoxical, as it implies that to avoid the selection of an item, the item must somehow be selected to some degree. This conundrum has been termed the "ignoring paradox", and, to date, little is known about how the brain resolves it. Here, in data from four experiments using neuromagnetic brain recordings in male and female humans, we provide evidence that this paradox is resolved by giving distracting information priority in cortical processing. This attentional priority to distractors manifests as an enhanced early neuromagnetic index, which occurs before target-related processing, and regardless of distractor predictability. It is most pronounced on trials for which a response rapidly occurred, and is followed by a suppression of the distracting information. These observations together suggest that in visual search items cannot be ignored without first being selected.SIGNIFICANCE STATEMENT How can we ignore distracting stimuli in our environment? To do this successfully, a logical hypothesis is that as few neural resources as possible should be devoted to distractor processing. Yet, to avoid devoting resources to a distractor, the brain must somehow mark what to avoid; this is a philosophical problem, which has been termed the "ignoring paradox" or "white bear phenomenon". Here, we use MEG recordings to determine how the human brain resolves this paradox. Our data show that distractors are not only processed, they are given temporal priority, with the brain building a robust representation of the to-be-ignored items. Thus, successful suppression of distractors can only be achieved if distractors are first strongly neurally represented.

Attention to Color Sharpens Neural Population Tuning via Feedback Processing in the Human Visual Cortex Hierarchy.

Attention can facilitate the selection of elementary object features such as color, orientation, or motion. This is referred to as feature-based attention and it is commonly attributed to a modulation of the gain and tuning of feature-selective units in visual cortex. Although gain mechanisms are well characterized, little is known about the cortical processes underlying the sharpening of feature selectivity. Here, we show with high-resolution magnetoencephalography in human observers (men and women) that sharpened selectivity for a particular color arises from feedback processing in the human visual cortex hierarchy. To assess color selectivity, we analyze the response to a color probe that varies in color distance from an attended color target. We find that attention causes an initial gain enhancement in anterior ventral extrastriate cortex that is coarsely selective for the target color and transitions within ∼100 ms into a sharper tuned profile in more posterior ventral occipital cortex. We conclude that attention sharpens selectivity over time by attenuating the response at lower levels of the cortical hierarchy to color values neighboring the target in color space. These observations support computational models proposing that attention tunes feature selectivity in visual cortex through backward-propagating attenuation of units less tuned to the target.SIGNIFICANCE STATEMENT Whether searching for your car, a particular item of clothing, or just obeying traffic lights, in everyday life, we must select items based on color. But how does attention allow us to select a specific color? Here, we use high spatiotemporal resolution neuromagnetic recordings to examine how color selectivity emerges in the human brain. We find that color selectivity evolves as a coarse to fine process from higher to lower levels within the visual cortex hierarchy. Our observations support computational models proposing that feature selectivity increases over time by attenuating the responses of less-selective cells in lower-level brain areas. These data emphasize that color perception involves multiple areas across a hierarchy of regions, interacting with each other in a complex, recursive manner.

The Rapid Capture of Attention by Rewarded Objects.

When a stimulus is associated with a reward, it becomes prioritized, and the allocation of attention to that stimulus increases. For low-level features, such as color, this reward-based allocation of attention can manifest early in time and as a faster and stronger shift of attention to targets with that color, as reflected by the N2pc (a parieto-occipital electrophysiological component peaking at ∼250 msec). It is unknown, however, if reward associations can similarly modulate attentional shifts to complex objects or object categories, or if reward-related modulation of attentional allocation to such stimuli would occur later in time or through a different mechanism. Here, we used magnetoencephalographic recordings in 24 participants to investigate how object categories with a reward association would modulate the shift of attention. On each trial, two colored squares were presented, one in a target color and the other in a distractor color, each with an embedded object. Participants searched for the target-colored square and performed a corner discrimination task. The embedded objects were from either a rewarded or non-rewarded category, and if a rewarded-category object were present within the target-colored square, participants could earn extra money for correct performance. We observed that when the target color contained an object from a rewarded versus a non-rewarded category, the neural shift of attention to the target was faster and of greater magnitude, although the rewarded objects were not relevant for correct task performance. These results suggest that reward associations of complex objects can rapidly modulate attentional allocation to a target.

Determinants of Global Color-Based Selection in Human Visual Cortex.

Feature attention operates in a spatially global way, with attended feature values being prioritized for selection outside the focus of attention. Accounts of global feature attention have emphasized feature competition as a determining factor. Here, we use magnetoencephalographic recordings in humans to test whether competition is critical for global feature selection to arise. Subjects performed a color/shape discrimination task in one visual field (VF), while irrelevant color probes were presented in the other unattended VF. Global effects of color attention were assessed by analyzing the response to the probe as a function of whether or not the probe's color was a target-defining color. We find that global color selection involves a sequence of modulations in extrastriate cortex, with an initial phase in higher tier areas (lateral occipital complex) followed by a later phase in lower tier retinotopic areas (V3/V4). Importantly, these modulations appeared with and without color competition in the focus of attention. Moreover, early parts of the modulation emerged for a task-relevant color not even present in the focus of attention. All modulations, however, were eliminated during simple onset-detection of the colored target. These results indicate that global color-based attention depends on target discrimination independent of feature competition in the focus of attention.