Task Termination Triggers Spontaneous Removal of Information From Visual Working Memory.

Working memory (WM) is a goal-directed memory system that actively maintains a limited amount of task-relevant information to serve the current goal. By this definition, WM maintenance should be terminated after the goal is accomplished, spontaneously removing no-longer-relevant information from WM. Past studies have failed to provide direct evidence of spontaneous removal of WM content by allowing participants to engage in a strategic reallocation of WM resources to competing information within WM. By contrast, we provide direct neural and behavioral evidence that visual WM content can be largely removed less than 1 s after it becomes obsolete, in the absence of a strategic allocation of resources (total N = 442 adults). These results demonstrate that visual WM is intrinsically a goal-directed system, and spontaneous removal provides a means for capacity-limited WM to keep up with ever-changing demands in a dynamic environment.

Behavioral signatures of the rapid recruitment of long-term memory to overcome working memory capacity limits.

Working- and long-term memory are often studied in isolation. To better understand the specific limitations of working memory, effort is made to reduce the potential influence of long-term memory on performance in working memory tasks (e.g., asking participants to remember artificial, abstract items rather than familiar real-world objects). However, in everyday life we use working- and long-term memory in tandem. Here, our goal was to characterize how long-term memory can be recruited to circumvent capacity limits in a typical visual working memory task (i.e., remembering colored squares). Prior work has shown that incidental repetitions of working memory arrays often do not improve visual working memory performance - even after dozens of incidental repetitions, working memory performance often shows no improvement for repeated arrays. Here, we used a whole-report working memory task with explicit rather than incidental repetitions of arrays. In contrast to prior work with incidental repetitions, in two behavioral experiments we found that explicit repetitions of arrays yielded robust improvement to working memory performance, even after a single repetition. Participants performed above chance at recognizing repeated arrays in a later long-term memory test, consistent with the idea that long-term memory was used to rapidly improve performance across array repetitions. Finally, we analyzed inter-item response times and we found a response time signature of chunk formation that only emerged after the array was repeated (inter-response time slowing after two to three items); thus, inter-item response times may be useful for examining the coordinated interaction of visual working and long-term memory in future work.

Storage in Visual Working Memory Recruits a Content-Independent Pointer System.

Past work has shown that storage in working memory elicits stimulus-specific neural activity that tracks the stored content. Here, we present evidence for a distinct class of load-sensitive neural activity that indexes items without representing their contents per se. We recorded electroencephalogram (EEG) activity while adult human subjects stored varying numbers of items in visual working memory. Multivariate analysis of the scalp topography of EEG voltage enabled precise tracking of the number of individuated items stored and robustly predicted individual differences in working memory capacity. Critically, this signature of working memory load generalized across variations in both the type and number of visual features stored about each item, suggesting that it tracked the number of individuated memory representations and not the content of those memories. We hypothesize that these findings reflect the operation of a capacity-limited pointer system that supports on-line storage and attentive tracking.

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.

Controlling the Flow of Distracting Information in Working Memory.

Visual working memory (WM) must maintain relevant information, despite the constant influx of both relevant and irrelevant information. Attentional control mechanisms help determine which of this new information gets access to our capacity-limited WM system. Previous work has treated attentional control as a monolithic process-either distractors capture attention or they are suppressed. Here, we provide evidence that attentional capture may instead be broken down into at least two distinct subcomponent processes: (1) Spatial capture, which refers to when spatial attention shifts towards the location of irrelevant stimuli and (2) item-based capture, which refers to when item-based WM representations of irrelevant stimuli are formed. To dissociate these two subcomponent processes of attentional capture, we utilized a series of electroencephalography components that track WM maintenance (contralateral delay activity), suppression (distractor positivity), item individuation (N2pc), and spatial attention (lateralized alpha power). We show that new, relevant information (i.e., a task-relevant distractor) triggers both spatial and item-based capture. Irrelevant distractors, however, only trigger spatial capture from which ongoing WM representations can recover more easily. This fractionation of attentional capture into distinct subcomponent processes provides a refined framework for understanding how distracting stimuli affect attention and WM.

Perceptual Grouping Reveals Distinct Roles for Sustained Slow Wave Activity and Alpha Oscillations in Working Memory.

Multiple neural signals have been found to track the number of items stored in working memory (WM). These signals include oscillatory activity in the alpha band and slow-wave components in human EEG, both of which vary with storage loads and predict individual differences in WM capacity. However, recent evidence suggests that these two signals play distinct roles in spatial attention and item-based storage in WM. Here, we examine the hypothesis that sustained negative voltage deflections over parieto-occipital electrodes reflect the number of individuated items in WM, whereas oscillatory activity in the alpha frequency band (8-12 Hz) within the same electrodes tracks the attended positions in the visual display. We measured EEG activity while participants stored the orientation of visual elements that were either grouped by collinearity or not. This grouping manipulation altered the number of individuated items perceived while holding constant the number of locations occupied by visual stimuli. The negative slow wave tracked the number of items stored and was reduced in amplitude in the grouped condition. By contrast, oscillatory activity in the alpha frequency band tracked the number of positions occupied by the memoranda and was unaffected by perceptual grouping. Perceptual grouping, then, reduced the number of individuated representations stored in WM as reflected by the negative slow wave, whereas the location of each element was actively maintained as indicated by alpha power. These findings contribute to the emerging idea that distinct classes of EEG signals work in concert to successfully maintain on-line representations in WM.

Sustained Attention and Spatial Attention Distinctly Influence Long-term Memory Encoding.

Our attention is critically important for what we remember. Prior measures of the relationship between attention and memory, however, have largely treated "attention" as a monolith. Here, across three experiments, we provide evidence for two dissociable aspects of attention that influence encoding into long-term memory. Using spatial cues together with a sensitive continuous report procedure, we find that long-term memory response error is affected by both trial-by-trial fluctuations of sustained attention and prioritization via covert spatial attention. Furthermore, using multivariate analyses of EEG, we track both sustained attention and spatial attention before stimulus onset. Intriguingly, even during moments of low sustained attention, there is no decline in the representation of the spatially attended location, showing that these two aspects of attention have robust but independent effects on long-term memory encoding. Finally, sustained and spatial attention predicted distinct variance in long-term memory performance across individuals. That is, the relationship between attention and long-term memory suggests a composite model, wherein distinct attentional subcomponents influence encoding into long-term memory. These results point toward a taxonomy of the distinct attentional processes that constrain our memories.

Phase-coding memories in mind.

Temporarily holding information in mind is an important part of many cognitive processes, such as reasoning and language. The amount of information that can be actively held "in mind" at any time is greatly limited-research suggests that we can only actively hold three or four pieces of information at once. A central question in cognitive neuroscience is how a system comprised of billions of neurons can actively maintain such a limited amount of information. A new study published in this issue of PLOS Biology by Bahramisharif and colleagues provides significant insights into this question.

Unconscious Number Discrimination in the Human Visual System.

How do humans compute approximate number? According to one influential theory, approximate number representations arise in the intraparietal sulcus and are amodal, meaning that they arise independent of any sensory modality. Alternatively, approximate number may be computed initially within sensory systems. Here we tested for sensitivity to approximate number in the visual system using steady state visual evoked potentials. We recorded electroencephalography from humans while they viewed dotclouds presented at 30 Hz, which alternated in numerosity (ranging from 10 to 20 dots) at 15 Hz. At this rate, each dotcloud backward masked the previous dotcloud, disrupting top-down feedback to visual cortex and preventing conscious awareness of the dotclouds' numerosities. Spectral amplitude at 15 Hz measured over the occipital lobe (Oz) correlated positively with the numerical ratio of the stimuli, even when nonnumerical stimulus attributes were controlled, indicating that subjects' visual systems were differentiating dotclouds on the basis of their numerical ratios. Crucially, subjects were unable to discriminate the numerosities of the dotclouds consciously, indicating the backward masking of the stimuli disrupted reentrant feedback to visual cortex. Approximate number appears to be computed within the visual system, independently of higher-order areas, such as the intraparietal sulcus.

Perturbing Neural Representations of Working Memory with Task-irrelevant Interruption.

Working memory maintains information so that it can be used in complex cognitive tasks. A key challenge for this system is to maintain relevant information in the face of task-irrelevant perturbations. Across two experiments, we investigated the impact of task-irrelevant interruptions on neural representations of working memory. We recorded EEG activity in humans while they performed a working memory task. On a subset of trials, we interrupted participants with salient but task-irrelevant objects. To track the impact of these task-irrelevant interruptions on neural representations of working memory, we measured two well-characterized, temporally sensitive EEG markers that reflect active, prioritized working memory representations: the contralateral delay activity and lateralized alpha power (8-12 Hz). After interruption, we found that contralateral delay activity amplitude momentarily sustained but was gone by the end of the trial. Lateralized alpha power was immediately influenced by the interrupters but recovered by the end of the trial. This suggests that dissociable neural processes contribute to the maintenance of working memory information and that brief irrelevant onsets disrupt two distinct online aspects of working memory. In addition, we found that task expectancy modulated the timing and magnitude of how these two neural signals responded to task-irrelevant interruptions, suggesting that the brain's response to task-irrelevant interruption is shaped by task context.

Distinguishing cognitive effort and working memory load using scale-invariance and alpha suppression in EEG.

Despite being intuitive, cognitive effort has proven difficult to define quantitatively. Here, we proposed to study cognitive effort by investigating the degree to which the brain deviates from its default state, where brain activity is scale-invariant. Specifically, we measured such deviations by examining changes in scale-invariance of brain activity as a function of task difficulty and posited suppression of scale-invariance as a proxy for exertion of cognitive effort. While there is some fMRI evidence supporting this proposition, EEG investigations on the matter are scant, despite the EEG signal being more suitable for analysis of scale invariance (i.e., having a much broader frequency range). In the current study we validated the correspondence between scale-invariance (H) of cortical activity recorded by EEG and task load during two working memory (WM) experiments with varying set sizes. Then, we used this neural signature to disentangle cognitive effort from the number of items stored in WM within participants. Our results showed monotonic decreases in H with increased set size, even after set size exceeded WM capacity. This behavior of H contrasted with behavioral performance and an oscillatory indicator of WM load (i.e., alpha-band desynchronization), both of which showed a plateau at difficulty levels surpassing WM capacity. This is the first reported evidence for the suppression of scale-invariance in EEG due to task difficulty, and our work suggests that H suppression may be used to quantify changes in cognitive effort even when working memory load is at maximum capacity.

Neural Evidence for the Contribution of Active Suppression During Working Memory Filtering.

In order to efficiently process incoming visual information, selective attention acts as a filter that enhances relevant and suppresses irrelevant information. In this study, we used an event-related potential (ERP) approach with systematic lateralization to investigate enhancement and suppression during encoding of information into visual working memory (WM) separately. We used a change detection task in which observers had to memorize some items while ignoring other items. We found that the to-be-ignored items elicited a PD component in the ERP, suggesting that irrelevant information is actively suppressed from WM. The PD amplitude increased with distractor load and decreased with the ability to group distractors according to Gestalt principles. This suggests that the PD can be used as an indicator of how efficiently items can be suppressed from entering WM. Furthermore, while lateral memory-targets elicited a "traditional" CDA (starting ~300 ms), lateral memory-distractors elicited a sustained positivity contralateral to memory-distractors (CDAp, starting ~400 ms). In sum the results suggest that inhibition of irrelevant information is an important factor for efficient WM and is reflected in spontaneous (PD) and sustained suppression (CDAp).

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.

Dissecting the Neural Focus of Attention Reveals Distinct Processes for Spatial Attention and Object-Based Storage in Visual Working Memory.

Complex cognition relies on both on-line representations in working memory (WM), said to reside in the focus of attention, and passive off-line representations of related information. Here, we dissected the focus of attention by showing that distinct neural signals index the on-line storage of objects and sustained spatial attention. We recorded electroencephalogram (EEG) activity during two tasks that employed identical stimulus displays but varied the relative demands for object storage and spatial attention. We found distinct delay-period signatures for an attention task (which required only spatial attention) and a WM task (which invoked both spatial attention and object storage). Although both tasks required active maintenance of spatial information, only the WM task elicited robust contralateral delay activity that was sensitive to mnemonic load. Thus, we argue that the focus of attention is maintained via a collaboration between distinct processes for covert spatial orienting and object-based storage.

Visual short-term memory capacity predicts the "bandwidth" of visual long-term memory encoding.

We are capable of storing a virtually infinite amount of visual information in visual long-term memory (VLTM) storage. At the same time, the amount of visual information we can encode and maintain in visual short-term memory (VSTM) at a given time is severely limited. How do these two memory systems interact to accumulate vast amount of VLTM? In this series of experiments, we exploited interindividual and intraindividual differences VSTM capacity to examine the direct involvement of VSTM in determining the encoding rate (or "bandwidth") of VLTM. Here, we found that the amount of visual information encoded into VSTM at a given moment (i.e., VSTM capacity), but neither the maintenance duration nor the test process, predicts the effective encoding "bandwidth" of VLTM.

Contralateral Delay Activity Indexes Working Memory Storage, Not the Current Focus of Spatial Attention.

Contralateral delay activity (CDA) has long been argued to track the number of items stored in visual working memory (WM). Recently, however, Berggren and Eimer [Berggren, N., & Eimer, M. Does contralateral delay activity reflect working memory storage or the current focus of spatial attention within visual working memory? Journal of Cognitive Neuroscience, 28, 2003-2020, 2016] proposed the alternative hypothesis that the CDA tracks the current focus of spatial attention instead of WM storage. This hypothesis was based on the finding that, when two successive arrays of memoranda were placed in opposite hemifields, CDA amplitude was primarily determined by the position and number of items in the second display, not the total memory load across both displays. Here, we considered the alternative interpretation that participants dropped the first array from WM when they encoded the second array because the format of the probe display was spatially incompatible with the initial sample display. In this case, even if the CDA indexes active storage rather than spatial attention, CDA activity would be determined by the second array. We tested this idea by directly manipulating the spatial compatibility of sample and probe displays. With spatially incompatible displays, we replicated Berggren and Eimer's findings. However, with spatially compatible displays, we found clear evidence that CDA activity tracked the full storage load across both arrays, in line with a WM storage account of CDA activity. We propose that expectations of display compatibility influenced whether participants viewed the arrays as parts of a single extended event or two independent episodes. Thus, these findings raise interesting new questions about how event boundaries may shape the interplay between passive and active representations of task-relevant information.

Contralateral Delay Activity Tracks Fluctuations in Working Memory Performance.

Neural measures of working memory storage, such as the contralateral delay activity (CDA), are powerful tools in working memory research. CDA amplitude is sensitive to working memory load, reaches an asymptote at known behavioral limits, and predicts individual differences in capacity. An open question, however, is whether neural measures of load also track trial-by-trial fluctuations in performance. Here, we used a whole-report working memory task to test the relationship between CDA amplitude and working memory performance. If working memory failures are due to decision-based errors and retrieval failures, CDA amplitude would not differentiate good and poor performance trials when load is held constant. If failures arise during storage, then CDA amplitude should track both working memory load and trial-by-trial performance. As expected, CDA amplitude tracked load (Experiment 1), reaching an asymptote at three items. In Experiment 2, we tracked fluctuations in trial-by-trial performance. CDA amplitude was larger (more negative) for high-performance trials compared with low-performance trials, suggesting that fluctuations in performance were related to the successful storage of items. During working memory failures, participants oriented their attention to the correct side of the screen (lateralized P1) and maintained covert attention to the correct side during the delay period (lateralized alpha power suppression). Despite the preservation of attentional orienting, we found impairments consistent with an executive attention theory of individual differences in working memory capacity; fluctuations in executive control (indexed by pretrial frontal theta power) may be to blame for storage failures.

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.

Clear evidence for item limits in visual working memory.

There is a consensus that visual working memory (WM) resources are sharply limited, but debate persists regarding the simple question of whether there is a limit to the total number of items that can be stored concurrently. Zhang and Luck (2008) advanced this debate with an analytic procedure that provided strong evidence for random guessing responses, but their findings can also be described by models that deny guessing while asserting a high prevalence of low precision memories. Here, we used a whole report memory procedure in which subjects reported all items in each trial and indicated whether they were guessing with each response. Critically, this procedure allowed us to measure memory performance for all items in each trial. When subjects were asked to remember 6 items, the response error distributions for about 3 out of the 6 items were best fit by a parameter-free guessing model (i.e. a uniform distribution). In addition, subjects' self-reports of guessing precisely tracked the guessing rate estimated with a mixture model. Control experiments determined that guessing behavior was not due to output interference, and that there was still a high prevalence of guessing when subjects were instructed not to guess. Our novel approach yielded evidence that guesses, not low-precision representations, best explain limitations in working memory. These guesses also corroborate a capacity-limited working memory system - we found evidence that subjects are able to report non-zero information for only 3-4 items. Thus, WM capacity is constrained by an item limit that precludes the storage of more than 3-4 individuated feature values.

α Power Modulation and Event-Related Slow Wave Provide Dissociable Correlates of Visual Working Memory.

Traditionally, electrophysiological correlates of visual working memory (VWM) capacity have been characterized using a lateralized VWM task in which participants had to remember items presented on the cued hemifield while ignoring the distractors presented on the other hemifield. Though this approach revealed a lateralized parieto-occipital negative slow wave (i.e., the contralateral delay activity) and lateralized α power modulation as neural correlates of VWM capacity that may be mechanistically related, recent evidence suggested that these measures might be reflecting individuals' ability to ignore distractors rather than their ability to maintain VWM representations. To better characterize the neural correlates of VWM capacity, we had human participants perform a whole-field VWM task in which they remembered all the items on the display. Here, we found that both the parieto-occipital negative slow wave and the α power suppression showed the characteristics of VWM capacity in the absence of distractors, suggesting that they reflect the maintenance of VWM representations rather than filtering of distractors. Furthermore, the two signals explained unique portions of variance in individual differences of VWM capacity and showed differential temporal characteristics. This pattern of results clearly suggests that individual differences in VWM capacity are determined by dissociable neural mechanisms reflected in the ERP and the oscillatory measures of VWM capacity. SIGNIFICANCE STATEMENT: Our work demonstrates that there exist event-related potential and oscillatory correlates of visual working memory (VWM) capacity even in the absence of task-irrelevant distractors. This clearly shows that the two neural correlates are directly linked to maintenance of task-relevant information rather than filtering of task-irrelevant information. Furthermore, we found that these two correlates show differential temporal characteristics. These results are inconsistent with proposals that the two neural correlates are byproducts of asymmetric α power suppression and indicate that they reflect dissociable neural mechanisms subserving VWM.