Encoded and updated spatial working memories share a common representational format in alpha activity.

Working memory (WM) flexibly updates information to adapt to the dynamic environment. Here, we used alpha-band activity in the EEG to reconstruct the content of dynamic WM updates and compared this representational format to static WM content. An inverted encoding model using alpha activity precisely tracked both the initially encoded position and the updated position following an auditory cue signaling mental updating. The timing of the update, as tracked in the EEG, correlated with reaction times and saccade latency. Finally, cross-training analyses revealed a robust generalization of alpha-band reconstruction of WM contents before and after updating. These findings demonstrate that alpha activity tracks the dynamic updates to spatial WM and that the format of this activity is preserved across the encoded and updated representations. Thus, our results highlight a new approach for measuring updates to WM and show common representational formats during dynamic mental updating and static storage.

Distinguishing guesses from fuzzy memories: Further evidence for item limits in visual working memory.

There is consistent debate over whether capacity in working memory (WM) is subject to an item limit, or whether an unlimited number of items can be held in this online memory system. The item limit hypothesis clearly predicts guessing responses when capacity is exceeded, and proponents of this view have highlighted evidence for guessing in visual working memory tasks. Nevertheless, various models that deny item limits can explain the same empirical patterns by asserting extremely low fidelity representations that cannot be distinguished from guesses. To address this ambiguity, we employed a task for which guess responses elicited a qualitatively distinct pattern from low fidelity memories. Inspired by work from Rouder et al. (2014), we employed an orientation WM task that required subjects to recall the precise orientation of each of six memoranda presented 1 s earlier. The orientation stimuli were created by rotating the position of a "clock hand" inside a circular region that was demarcated by four colored quadrants. Critically, when observers guess with these stimuli, the distribution of responses is biased towards the center of these quadrants, creating a "banded" pattern that cannot be explained by a low precision memory. We confirmed the presence of this guessing pattern using formal model comparisons, and we show that the prevalence of this pattern matches observers' own reports of when they thought they were guessing. Thus, these findings provide further evidence for guessing behaviors predicted by item limit models of WM capacity.

The cost of divided attention for detection of simple visual features primarily reflects limits in post-perceptual processing.

Covert spatial attention allows us to prioritize processing at relevant locations. Perception is generally poorer when attention is distributed across multiple locations than when attention is focused on a single location. However, while divided attention typically impairs performance, recent work suggests that divided attention does not seem to impair detection of simple visual features. Here, we re-examined this possibility. In two experiments, observers detected a simple target (a vertical Gabor), and we manipulated whether attention was focused at one location (focal-cue condition) or distributed across two locations (distributed-cue condition). In Experiment 1, targets could appear independently at each location, such that observers needed to judge target presence for each location separately in the distributed-cue condition. Under these conditions, we found a robust cost of dividing attention. Next, we further probed what stage of processing gave rise to this cost. In Experiment 1, the cost of dividing attention could reflect a limit in the ability to make concurrent judgments about target presence. In Experiment 2, we simplified the task to test whether this was the case: just one target could appear on each trial, such that observers made a single judgment ("was a target present?") in both the focal-cue and distributed-cue conditions. Here, we found a marginal cost of dividing attention that was weaker than the cost in Experiment 1. Together, our results suggest that divided attention does impair detection of simple visual features, but that this cost is primarily due to a limit in post-perceptual processes.

Feature-based attention multiplicatively scales the fMRI-BOLD contrast-response function.

Functional MRI (fMRI) plays a key role in the study of attention. However, there remains a puzzling discrepancy between attention effects measured with fMRI and with electrophysiological methods. While electrophysiological studies find that attention increases sensory gain, amplifying stimulus-evoked neural responses by multiplicatively scaling the contrast-response function (CRF), fMRI appears to be insensitive to these multiplicative effects. Instead, fMRI studies typically find that attention produces an additive baseline shift in the blood-oxygen-level-dependent (BOLD) signal. These findings suggest that attentional effects measured with fMRI reflect top-down inputs to visual cortex, rather than the modulation of sensory gain. If true, this drastically limits what fMRI can tell us about how attention improves sensory coding. Here, we examined whether fMRI is sensitive to multiplicative effects of attention using a feature-based attention paradigm designed to preclude any possible additive effects. We measured BOLD activity evoked by a probe stimulus in one visual hemifield while participants (6 male, 6 female) attended to the probe orientation (attended condition), or to an orthogonal orientation (unattended condition), in the other hemifield. To measure CRFs in visual areas V1-V3, we parametrically varied the contrast of the probe stimulus. In all three areas, feature-based attention increased contrast gain, improving sensitivity by shifting CRFs towards lower contrasts. In V2 and V3, we also found an increase in response gain, an increase in the responsivity of the CRF, that was greatest at inner eccentricities. These results provide clear evidence that the fMRI-BOLD signal is sensitive to multiplicative effects of attention.SIGNIFICANCE STATEMENTFunctional MRI (fMRI) plays a central role in the study of attention because it allows researchers to precisely and non-invasively characterize the effects of attention throughout the brain. Electrophysiological studies have shown that attention increases sensory gain, amplifying stimulus-evoked neural responses. However, a growing body of work suggests that the BOLD signal that is measured with fMRI is not sensitive to these multiplicative effects of attention, calling into question what we can learn from fMRI about how attention improves sensory codes. Here, using a feature-based attention paradigm, we provide evidence that the BOLD signal can pick up multiplicative effects of attention.

Shared Representational Formats for Information Maintained in Working Memory and Information Retrieved from Long-Term Memory.

Current theories propose that the short-term retention of information in working memory (WM) and the recall of information from long-term memory (LTM) are supported by overlapping neural mechanisms in occipital and parietal cortex. However, the extent of the shared representations between WM and LTM is unclear. We designed a spatial memory task that allowed us to directly compare the representations of remembered spatial information in WM and LTM with carefully matched behavioral response precision between tasks. Using multivariate pattern analyses on functional magnetic resonance imaging data, we show that visual memories were represented in a sensory-like code in both memory tasks across retinotopic regions in occipital and parietal cortex. Regions in lateral parietal cortex also encoded remembered locations in both tasks, but in a format that differed from sensory-evoked activity. These results suggest a striking correspondence in the format of representations maintained in WM and retrieved from LTM across occipital and parietal cortex. On the other hand, we also show that activity patterns in nearly all parietal regions, but not occipital regions, contained information that could discriminate between WM and LTM trials. Our data provide new evidence for theories of memory systems and the representation of mnemonic content.

Temporal attention selectively enhances target features.

Temporal attention, the allocation of attention to a moment in time, improves perception. Here, we examined the computational mechanism by which temporal attention improves perception, under a divisive normalization framework. Under this framework, attention can improve perception of a target signal in three ways: stimulus enhancement (increasing gain across all sensory channels), signal enhancement (selectively increasing gain in channels that encode the target stimulus), or external noise exclusion (reducing the gain in channels that encode irrelevant features). These mechanisms make diverging predictions when a target is embedded in varying levels of noise: stimulus enhancement improves performance only when noise is low, signal enhancement improves performance at all noise intensities, and external noise exclusion improves performance only when noise is high. To date, temporal attention studies have used noise-free displays. Therefore, it is unclear whether temporal attention acts via stimulus enhancement (amplifying both target features and noise) or signal enhancement (selectively amplifying target features) because both mechanisms predict improved performance in the absence of noise. To tease these mechanisms apart, we manipulated temporal attention using an auditory cue while parametrically varying external noise in a fine-orientation discrimination task. Temporal attention improved perceptual thresholds across all noise levels. Formal model comparisons revealed that this cuing effect was best accounted for by a combination of signal enhancement and stimulus enhancement, suggesting that temporal attention improves perceptual performance, in part, by selectively increasing gain for target features.

Covert Attention Increases the Gain of Stimulus-Evoked Population Codes.

Covert spatial attention has a variety of effects on the responses of individual neurons. However, relatively little is known about the net effect of these changes on sensory population codes, even though perception ultimately depends on population activity. Here, we measured the EEG in human observers (male and female), and isolated stimulus-evoked activity that was phase-locked to the onset of attended and ignored visual stimuli. Using an encoding model, we reconstructed spatially selective population tuning functions from the pattern of stimulus-evoked activity across the scalp. Our EEG-based approach allowed us to measure very early visually evoked responses occurring ∼100 ms after stimulus onset. In Experiment 1, we found that covert attention increased the amplitude of spatially tuned population responses at this early stage of sensory processing. In Experiment 2, we parametrically varied stimulus contrast to test how this effect scaled with stimulus contrast. We found that the effect of attention on the amplitude of spatially tuned responses increased with stimulus contrast, and was well described by an increase in response gain (i.e., a multiplicative scaling of the population response). Together, our results show that attention increases the gain of spatial population codes during the first wave of visual processing.SIGNIFICANCE STATEMENT We know relatively little about how attention improves population codes, even though perception is thought to critically depend on population activity. In this study, we used an encoding-model approach to test how attention modulates the spatial tuning of stimulus-evoked population responses measured with EEG. We found that attention multiplicatively scales the amplitude of spatially tuned population responses. Furthermore, this effect was present within 100 ms of stimulus onset. Thus, our results show that attention improves spatial population codes by increasing their gain at this early stage of processing.

Covert Spatial Attention Speeds Target Individuation.

Covert spatial attention has long been thought to speed visual processing. Psychophysics studies have shown that target information accrues faster at attended locations than at unattended locations. However, with behavioral evidence alone, it is difficult to determine whether attention speeds visual processing of the target or subsequent postperceptual stages of processing (e.g., converting sensory responses into decision signals). Moreover, although many studies have shown that attention can boost the amplitude of visually evoked neural responses, no robust effect has been observed on the latency of those neural responses. Here, we offer new evidence that may reconcile the neural and behavioral findings. We examined whether covert attention influenced the latency of the N2pc component, an electrophysiological marker of visual selection that has been linked with object individuation-the formation of an object representation that is distinct from the background and from other objects in the scene. To this end, we manipulated whether or not human observers (male and female) covertly attended the location of an impending search target. We found that the target evoked N2pc onset ∼20 ms earlier when the target location was cued than when it was not cued. In a second experiment, we provided a direct replication of this effect, confirming that the effect of attention on N2pc latency is robust. Thus, although attention may not speed the earliest stages of sensory processing, attention does speed the critical transition between raw sensory encoding and the formation of individuated object representations.SIGNIFICANCE STATEMENT Covert spatial attention improves processing at attended locations. Past behavioral studies have shown that information about visual targets accrues faster at attended than at unattended locations. However, it has remained unclear whether attention speeds perceptual analysis or subsequent postperceptual stages of processing. Here, we present robust evidence that attention speeds the N2pc, an electrophysiological signal that indexes the formation of individuated object representations. Our findings show that attention speeds a relatively early stage of perceptual processing while also elucidating the specific perceptual process that is speeded.

Alpha-band oscillations track the retrieval of precise spatial representations from long-term memory.

A hallmark of episodic memory is the phenomenon of mentally reexperiencing the details of past events, and a well-established concept is that the neuronal activity that mediates encoding is reinstated at retrieval. Evidence for reinstatement has come from multiple modalities, including functional magnetic resonance imaging and electroencephalography (EEG). These EEG studies have shed light on the time course of reinstatement but have been limited to distinguishing between a few categories. The goal of this work was to use recently developed experimental and technical approaches, namely continuous report tasks and inverted encoding models, to determine which frequencies of oscillatory brain activity support the retrieval of precise spatial memories. In experiment 1, we establish that an inverted encoding model applied to multivariate alpha topography tracks the retrieval of precise spatial memories. In experiment 2, we demonstrate that the frequencies and patterns of multivariate activity at study are similar to the frequencies and patterns observed during retrieval. These findings highlight the broad potential for using encoding models to characterize long-term memory retrieval.NEW & NOTEWORTHY Previous EEG work has shown that category-level information observed during encoding is recapitulated during memory retrieval, but studies with this time-resolved method have not demonstrated the reinstatement of feature-specific patterns of neural activity during retrieval. Here we show that EEG alpha-band activity tracks the retrieval of spatial representations from long-term memory. Moreover, we find considerable overlap between the frequencies and patterns of activity that track spatial memories during initial study and at retrieval.

Item-specific delay activity demonstrates concurrent storage of multiple active neural representations in working memory.

Persistent neural activity that encodes online mental representations plays a central role in working memory (WM). However, there has been debate regarding the number of items that can be concurrently represented in this active neural state, which is often called the "focus of attention." Some models propose a strict single-item limit, such that just 1 item can be neurally active at once while other items are relegated to an activity-silent state. Although past studies have decoded multiple items stored in WM, these studies cannot rule out a switching account in which only a single item is actively represented at a time. Here, we directly tested whether multiple representations can be held concurrently in an active state. We tracked spatial representations in WM using alpha-band (8-12 Hz) activity, which encodes spatial positions held in WM. Human observers remembered 1 or 2 positions over a short delay while we recorded electroencephalography (EEG) data. Using a spatial encoding model, we reconstructed active stimulus-specific representations (channel-tuning functions [CTFs]) from the scalp distribution of alpha-band power. Consistent with past work, we found that the selectivity of spatial CTFs was lower when 2 items were stored than when 1 item was stored. Critically, data-driven simulations revealed that the selectivity of spatial representations in the two-item condition could not be explained by models that propose that only a single item can exist in an active state at once. Thus, our findings demonstrate that multiple items can be concurrently represented in an active neural state.

The role of alpha oscillations in spatial attention: limited evidence for a suppression account.

Covert spatial attention allows us to prioritize visual processing at relevant locations. A fast growing literature suggests that alpha-band (8-12 Hz) oscillations play a key role in this core cognitive process. It is clear that alpha-band activity tracks both the locus and timing of covert spatial orienting. There is limited evidence, however, for the widely embraced view that alpha oscillations suppress irrelevant visual information during spatial selection. Extant evidence is equally compatible with an account in which alpha activity enables spatial selection through signal enhancement rather than distractor suppression. Thus, more work is needed to characterize the computational role of alpha activity in spatial attention.

Spatially Selective Alpha Oscillations Reveal Moment-by-Moment Trade-offs between Working Memory and Attention.

Current theories assume a functional role for covert attention in the maintenance of spatial information in working memory. Consistent with this view, both the locus of attention and positions stored in working memory can be decoded based on the topography of oscillatory alpha-band (8-12 Hz) activity on the scalp. Thus far, however, alpha modulation has been studied in isolation for covert attention and working memory tasks. Here, we applied an inverted spatial encoding model in combination with EEG to study the temporal dynamics of spatially specific alpha activity during a task that required observers to visually select a target location while maintaining another independently varying location in working memory. During the memory delay period, alpha-based spatial tuning functions shifted from the position stored in working memory to the covertly attended position and back again after the attention task was completed. The findings provide further evidence for a common oscillatory mechanism in both the selection and the maintenance of relevant spatial visual information and demonstrate the dynamic trade-off in prioritization between two spatial tasks.

Alpha-Band Activity Reveals Spontaneous Representations of Spatial Position in Visual Working Memory.

An emerging view suggests that spatial position is an integral component of working memory (WM), such that non-spatial features are bound to locations regardless of whether space is relevant [1, 2]. For instance, past work has shown that stimulus position is spontaneously remembered when non-spatial features are stored. Item recognition is enhanced when memoranda appear at the same location where they were encoded [3-5], and accessing non-spatial information elicits shifts of spatial attention to the original position of the stimulus [6, 7]. However, these findings do not establish that a persistent, active representation of stimulus position is maintained in WM because similar effects have also been documented following storage in long-term memory [8, 9]. Here we show that the spatial position of the memorandum is actively coded by persistent neural activity during a non-spatial WM task. We used a spatial encoding model in conjunction with electroencephalogram (EEG) measurements of oscillatory alpha-band (8-12 Hz) activity to track active representations of spatial position. The position of the stimulus varied trial to trial but was wholly irrelevant to the tasks. We nevertheless observed active neural representations of the original stimulus position that persisted throughout the retention interval. Further experiments established that these spatial representations are dependent on the volitional storage of non-spatial features rather than being a lingering effect of sensory energy or initial encoding demands. These findings provide strong evidence that online spatial representations are spontaneously maintained in WM-regardless of task relevance-during the storage of non-spatial features.

Alpha-Band Oscillations Enable Spatially and Temporally Resolved Tracking of Covert Spatial Attention.

Covert spatial attention is essential for humans' ability to direct limited processing resources to the relevant aspects of visual scenes. A growing body of evidence suggests that rhythmic neural activity in the alpha frequency band (8-12 Hz) tracks the spatial locus of covert attention, which suggests that alpha activity is integral to spatial attention. However, extant work has not provided a compelling test of another key prediction: that alpha activity tracks the temporal dynamics of covert spatial orienting. In the current study, we examined the time course of spatially specific alpha activity after central cues and during visual search. Critically, the time course of this activity tracked trial-by-trial variations in orienting latency during visual search. These findings provide important new evidence for the link between rhythmic brain activity and covert spatial attention, and they highlight a powerful approach for tracking the spatial and temporal dynamics of this core cognitive process.

The topography of alpha-band activity tracks the content of spatial working memory.

Working memory (WM) is a system for the online storage of information. An emerging view is that neuronal oscillations coordinate the cellular assemblies that code the content of WM. In line with this view, previous work has demonstrated that oscillatory activity in the alpha band (8-12 Hz) plays a role in WM maintenance, but the exact contributions of this activity have remained unclear. Here, we used an inverted spatial encoding model in combination with electroencephalography (EEG) to test whether the topographic distribution of alpha-band activity tracks spatial representations held in WM. Participants in three experiments performed spatial WM tasks that required them to remember the precise angular location of a sample stimulus for 1,000-1,750 ms. Across all three experiments, we found that the topographic distribution of alpha-band activity tracked the specific location that was held in WM. Evoked (i.e., activity phase-locked to stimulus onset) and total (i.e., activity regardless of phase) power across a range of low-frequency bands transiently tracked the location of the sample stimulus following stimulus onset. However, only total power in the alpha band tracked the content of spatial WM throughout the memory delay period, which enabled reconstruction of location-selective channel tuning functions (CTFs). These findings demonstrate that alpha-band activity is directly related to the coding of spatial representations held in WM and provide a promising method for tracking the content of this online memory system.

Frontal and parietal EEG asymmetries interact to predict attentional bias to threat.

Frontal and parietal electroencephalographic (EEG) asymmetries mark vulnerability to depression and anxiety. Drawing on cognitive theories of vulnerability, we hypothesise that cortical asymmetries predict attention to threat. Participants completed a dot-probe task in which bilateral face displays were followed by lateralised targets at either short (300ms) or long (1050ms) SOA. We also measured N2pc to face onset as an index of early attentional capture. At long SOA only, frontal and parietal asymmetry interacted to predict attentional bias to angry faces. Those with leftward frontal asymmetry showed no attentional bias. Among those with rightward frontal asymmetry those with low right parietal activity showed vigilance for threat, and those with high right parietal activity showed avoidance. Asymmetry was not related to the N2pc or to attentional bias at the short SOA. Findings suggest that trait asymmetries reflect function in a fronto-parietal network that controls attention to threat.